PELLERIN M Sylvain

M Frédéric

M Olivier Pourret

Unilasalle Examinateur

M Michel-Pierre

HDR, Unilasalle Enseignant-Chercheur Faucon

M David

Unilasalle Co-Encadrant

Unilasalle Membre

Frédéric Gerard

Alain Mollier

Gilles Colinet

Olivier Pourret

Adeline Adam

Céline Roisin

Philippe Jacolot

Pascale Lestradet

Aurore Coutelier

Erika Bastien

Julien Pierre Olivier

Issifou Amadou

David Houben

Michel-Pierre Faucon

après avis des rapporteurs, devant le jury d'examen

Keywords: agroecology, biogeochemistry, cover crops, organic inputs, organic phosphorus, plant traits, rhizosphere soil, rhizosphere microbiomes Adsorption, desorption, organic phosphorus, phosphorus availability, soil fertility Mineral-P complexes Quantity of P adsorbed (µg g -1 )

In this part, I would like to express my thanks to all those who participated in the thesis project, whether directly by supervising the project, contributing to the reflections, articles or various events I participated in during the project, or indirectly by supporting me during these three years. On the other hand, it is ironic that, given the multiple approaches and tools used during the project, this section remains one of the most difficult, if not the most difficult, to write. While I'm sure some people will be overlooked (and I apologize in advance), rest assured that no help, no matter how small, went unnoticed, so thank you! Un grand merci à mes directeurs de thèse Michel-Pierre Faucon et David Houben, pour tout le temps qu'ils m'ont accordé pour superviser ce projet, m'aider à mieux comprendre et valoriser nos résultats et plus généralement faire de moi un meilleur chercheur. Merci également pour votre soutien constant tout au long du projet et notamment dans les périodes de stress. Merci pour toutes nos discussions autour d'un article, d'une présentation ou d'un verre. Merci pour ton humour et ta positivité. Merci pour ta réactivité aux embuscades que je pouvais te faire au détour de tes bureaux ou dans les couloirs avec de nombreuses questions auxquelles tu as toujours su répondre. Michel-Pierre, un frère et aussi un ami que je ne saurais assez remercier, merci pour ton incroyable réactivité, ton esprit communicatif et tout ce que tu m'as apporté d'un point de vue professionnel et personnel durant le projet. Je tiens également à remercier Sophie pour son accueil chaleureux lors de ma visite à BOMY. David, merci pour ta positivité et ton soutien durant ces trois années et toutes tes propositions pertinentes qui ont plus que contribué à la qualité du travail. J'en oublie beaucoup d'autres, alors encore merci à vous deux.

Thèse de Doctorat

Mention Sciences Ecologiques Spécialité Ecologie et Biogéochimie

FOREWORD

This thesis project started in October 2019 and is funded by FEDER/FSE Picardie 2014-2020 and UniLaSalle (attached to the University Picardie Jules Verne), based in Beauvais (France). The project is carried out within the AGHYLE (Agroecology, Hydrogeochemistry, Environments, and Resources)

research team of UniLaSalle.

The thesis manuscript is written as a thesis on articles in English. Chapters 1 and 2 as well as a review article (presented in the general introduction) have been published in international journals, and Chapters 3 and 4 are being edited for publication in an international journal. A list of publications is available at the end of the manuscript, as well as an extended abstract of the manuscript in French.

Je dédie ce manuscrit à mon grand-père, qui :

Parmi les conseils qu'il me donna, place ces paroles "Mon fils ! que le coq ne soit pas plus vigilant que toi lorsqu'il chante à l'aurore ; alors que toi, tu dors". Et Voici ces vers :

"Une colombe a gémi, dans la nuit, sur une branche :

Je dormais... Mon père ! ma mère ! Mon amour est un menteur :

Sur un véritable amour, elle n'eût pas pris d'avance... Je suis l'amant aux yeux secs, mais elle verse des pleurs !"

Mon fils, ''Sache, que celui qui croit toucher au but sans effort est un homme de désir ; et celui qui ne compte que sur l'effort fait acte de présomption".

J'ai alors appris que la clé du succès, à l'origine, était l'amour, le travail assidu et la détermination ; et Sache, lecteur, qu'être enseigné n'est pas un droit, c'est une chance, parce qu'il y en a qui n'en ont pas, malgré de grandes prières ;

Et si les anges ne s'appelaient pas vraiment anges, moi je les aurais appelés enseignants du primaire, du collège, du lycée et des universités ;

Et si le savoir est à l'humain ce que l'odeur est à l'encens, alors l'enseignant est pour demain ce que la mère est pour l'enfant ;

J'ai alors réalisé que personne ne peut être enseignant s'il n'a pas un diamant à la place du coeur ;

Et Je dis,

Merci au maître qui a su mettre un peu de bien-être dans mon piètre être Table 19 : GLM model results testing the impact of factors: N form (NO3-N or NH4-N), minerals (goethite and kaolinite), and P forms (IP, IHP, and GLY) on N: P ratio, total P uptake, and total biomass. Phosphorus (P) is a limiting nutrient for agroecosystem productivity (Filippelli, 2008;Jarvie et al., 2019;[START_REF] Withers | Stewardship to tackle global phosphorus inefficiency: The case of Europe[END_REF]. The application of phosphate to the soil is necessary to maintain or improve crop yields. However, the depletion of global phosphate rock reserves from which chemical fertilizers are produced is now threatening global food security [START_REF] Schoumans | Phosphorus management in Europe in a changing world[END_REF]Cordell et al.2009). Therefore, recycling P from organic amendment is becoming a necessity for sustainable P management in agroecosystems (Bennett and Schipanski, 2013). However, P in organic amendment is in various forms of inorganic P (IP) and organic P (OP) that differ in their availability to plants (Faucon et al., 2015).

LIST OF FIGURES

LIST OF TABLES

Most research on the fate of P applied to soil has focused on IP, showing that most of it is adsorbed to the soil surface, thus affecting its availability to plants [START_REF] Huang | Phosphate removal from wastewater using red mud[END_REF]Houben et al. 2011;Hinsinger 2001). In contrast, the fate of OP has been understudied to date, and knowledge of their dynamics and contribution to plant nutrition is still lacking (Faucon et al., 2015).

In soils treated with organic amendments, up to 80% of total P is present as OP [START_REF] Nash | Using organic phosphorus to sustain pasture productivity: A perspective[END_REF][START_REF] Harrison | Soil Organic Phosphorus: A Review of World Literature[END_REF]. Typically, OP compounds include phosphomonoesters, phosphodiesters, and organic polyphosphates even though their relative proportions in soils vary greatly between studies (Table 1). Among these OP compounds, forms such as inositol hexakisphosphate, IHP [START_REF] Turner | Inositol phosphates in the environment[END_REF]Vincent et al. 2013;Vestergren et al. 2012), glycerophosphate, GLY (Newman et Tate 1980;[START_REF] Doolette | Spiking Improved Solution Phosphorus31 Nuclear Magnetic Resonance Identification of Soil Phosphorus Compounds[END_REF]Doolette et al. 2011), and glucose-6-phosphate, G6P (Vincent et al. 2013;[START_REF] Cui | Development of a glucose-6-phosphate biosensor based on coimmobilized p-hydroxybenzoate hydroxylase and glucose-6-phosphate dehydrogenase[END_REF][START_REF] Hogema | Catabolite repression by glucose 6-phosphate, gluconate and lactose in Escherichia coli[END_REF]) are generally considered major forms. Despite the widely recognized importance of OP forms as a source of P to plants and its essential role in biogeochemical cycling and ecosystem functioning [START_REF] Nash | Using organic phosphorus to sustain pasture productivity: A perspective[END_REF][START_REF] Dalai | Soil Organic Phosphorus[END_REF], its chemical nature as well as its transformation is still largely neglected and remains poorly understood compared to IP forms. Organic P forms differ significantly in their behavior and bioavailability in soil (Condron et al. 2005). This is due to their relationship with the soil minerals, but also to their different biochemical properties and chemical nature: P content, type of P bonding and size of the molecules ( Ganta et al. 2021;[START_REF] Fang | Phosphorus adsorption onto clay minerals and iron oxide with consideration of heterogeneous particle morphology[END_REF]Turner et Engelbrecht 2011). Moreover, the identification of OP species is still incomplete and much more difficult than that of IP. Therefore, their dynamics among soil porperties and during the long-term development of ecosystems is unknown [START_REF] Fang | Phosphorus adsorption onto clay minerals and iron oxide with consideration of heterogeneous particle morphology[END_REF][START_REF] Pant | Identification of soil organic phosphorus by 31P nuclear magnetic resonance spectroscopy[END_REF][START_REF] Young | Phosphorus speciation in riparian soils: A phosphorus-31 nuclear magnetic resonance spectroscopy and enzyme hydrolysis study[END_REF]. This poor understanding of the sources and types of OP and their transformations in soils not only hinders the optimization of organic amendment and the development of sustainable management practices, but also limits our ability to predict the response of ecosystem processes to changes in nutrient stoichiometry.

Table 1 : Organic P accumulation according to some soil properties

Soil properties OP forms Refference

Neutral soils with high organic matter Phosphate monoesters (Turner et Engelbrecht 2011 ;[START_REF] Fang | Phosphorus adsorption onto clay minerals and iron oxide with consideration of heterogeneous particle morphology[END_REF] Acidic soils DNA;

Phosphonates (Turner et Blackwell 2013;[START_REF] Cheesman | Forms of organic phosphorus in wetland soils[END_REF] Acidic soils with low organic matter Phosphate diesters (Turner et Engelbrecht 2011) Low Fe /Al soils Phosphate diesters;

Polyphosphates (Vincent et al., 2012) High Fe /Al soils Myo-, scyllo-and unknown Inositol phosphates (Vincent et al., 2012) Forest soils Orthophosphates, Inositolhexaphosphate; α-Glycerophosphate (Vincent et al. 2012 ;Newman et Tate 1980 ;[START_REF] Turner | Inositol phosphates in the environment[END_REF][START_REF] Pant | Identification of soil organic phosphorus by 31P nuclear magnetic resonance spectroscopy[END_REF] Riparian soils Glycerophosphate (9.4-131.4 mg P kg -1 ) [START_REF] Young | Phosphorus speciation in riparian soils: A phosphorus-31 nuclear magnetic resonance spectroscopy and enzyme hydrolysis study[END_REF] Alfisols Glycerophosphate (45% of OP);

Other monoester [START_REF] Pant | Identification of soil organic phosphorus by 31P nuclear magnetic resonance spectroscopy[END_REF] Depending on the nature of the OP-containing molecule in organic amendment, there are large differences regarding their affinity to soil particles and mineralisation dynamics (i.e. the corresponding enzyme activity). After supply in soil, the dynamics of OP are greatly influenced by factors and processes such as adsorption and desorption, complexation and precipitation, redox state, and organic matter composition (Lü et al., 2017;Ruttenberg and Sulak, 2011).These physical, chemical, and biological factors are listed as the primary abiotic processes governing the fate of OP in the soil-plant system [START_REF] Turner | Inositol phosphates in the environment[END_REF]Turner 2008). Furthermore, the size and molecular structure of OP generally affect the rate of their sorption density. Thus, it has been suggested that the higher the degree of phosphorylation of OP compounds, the greater the sorption to the soil solid phase. Since OP fixation in soil is often much higher than that of anionic IP species (Gerke, 2015), their sorption process requires careful study.

Soil minerals such as Fe and Al oxyhydroxides and clay minerals, constitute a major component of soils and sediments and have high P adsorption capacity (Ryan et al. 2001;Bortoluzzi et al. 2015).

Their P bonding degree depends on their reactive surface groups as well as on their degree of crystallinity or porosity (Guan et al., 2006;Ruttenberg and Sulak, 2011). Minerals with a high concentration of reactive Fe/Al-OH groups would strongly bind OP forms (Ganta et al. 2019a). Until today, a large part of the main soil minerals is not considered in the OP adsorption processes. Among all soil constituents, the effect of humic substances on P dynamics is often ignored [START_REF] Borggaard | Influence of humic substances on phosphate adsorption by aluminium and iron oxides[END_REF][START_REF] Gerke | Humic (Organic Matter)-Al(Fe)-Phosphate Complexes: An Underestimated Phosphate Form in Soils and Source of Plant-Available Phosphate[END_REF].

However, soil humic substances possess several characteristics that affect the P distribution between the solid phase and the soil solution [START_REF] Gerke | Humic (Organic Matter)-Al(Fe)-Phosphate Complexes: An Underestimated Phosphate Form in Soils and Source of Plant-Available Phosphate[END_REF]. As OP is not only bound to minerals surfaces in soil but can also be bound, similar to IP, to humic surfaces via Fe or Al bridges, research on this topic is strongly required. Several surface complexation models that describe phosphate adsorption have been developed

and successfully applied to IP adsorption by specifics soil minerals and soils [START_REF] Houben | Multi-method characterization of the ferrihydrite to goethite transformation[END_REF][START_REF] Sheals | Adsorption of Glyphosate on Goethite: Molecular Characterization of Surface Complexes[END_REF]. However, little is nown about the OP surface complexation whith soil. In addition, conflicting discussions are still present on the nature of the bonding process of the adsorbed OP and IP species and their relative abundance in soil [START_REF] Olsson | Enzymatic Hydrolysis of Organic Phosphates Adsorbed on Mineral Surfaces[END_REF][START_REF] Kim | Phosphate adsorption on the iron oxyhydroxides goethite (α-FeOOH), akaganeite (β-FeOOH), and lepidocrocite (γ-FeOOH): a 31P NMR Study[END_REF].

Compared to the adsorption process, which is already less well known, the desorbability and mineralization of OP to plant nutrition are difficult to assess, but studies in soil [START_REF] Stewart | Dynamics of Soil Organic Phosphorus[END_REF] suggest that this contribution increases with the mineral composition and geological age of the soil as well as the plant community. Because desorption occurs slowly, several authors have suggested that the adsorbed OP complex is not available to plants. The reason for this is that the mineral-OP complexes are formed during the slow reaction of the adsorption process ( Ganta et al. 2019a). Factors such as percent of P saturation (Parfitt 1979;He et al. 1994;Celi et Barberis 2002), incubation time, and temperature [START_REF] Barrow | The Description of Phosphate Adsorption Curves[END_REF] may affect the release of P from mineral-OP complexes to the soil solution, and thus the availability of P to plants, but the type of relationship involved is not yet clear. It is also likely that desorbability of phosphate from mineral-OP complexes is influenced by different factors, which, in turn, dependent upon the type of soil mineral (Parfitt, 1979). Unfortunately, the impact of different types of minerals has not been sufficiently studied, despite their practical implications for P fate.

Clearly, it is very likely that the potential of organic amendments to improve P use efficiency depends on the forms and biochemical properties of their different forms of OP. Indeed, depending on the nature of the OP molecule, there could be large differences in their affinity to soil particles and mineralization dynamics (i.e., corresponding enzymatic activity). Understanding these dynamics and the differences that can occur between forms of P is necessary to improve P availability from OP compounds. In this paper, we review the dynamics of OP in soil-plant systems as well as differences among OP forms by focusing on their sorption phenomena. We first discuss in detail their adsorption to the surface of soil minerals and their potential availability from the mineral-OP bonding complex. Then, we summarize some knowledge on the molecular characteristics of the main forms of OP in soil as well as recent advances on the nature, mechanisms and bonding strengths of sorbed OP. Finally, we present some open questions that need to be addressed in future studies with emphasis on characteristics and relative proportions of OP derived from organic amendments and their relationship to existing soil OP pools; the establishment of quantitative models for the transformation of mineral-OP bonding complexes and sophisticated models to quantify the relative importance of mechanisms governing the sorption of different forms of OP in soil.

Characteristics and adsorption of the major OP forms in soils 1.Inositol phosphates

Inositol phosphates are a six-carbon cyclohexanehexol (inositol) ring that has phosphate moieties linked by an ester bond. The number of substituted phosphate groups on the inositol ring may vary between one and six, which is indicated by the prefix's mono, bis, tris, tetrakis, pentakis and hexakis [START_REF] Nomenclature | Nomenclature of Phosphorus-Containing Compounds of Biochemical Importance (Recommendations 1976)[END_REF]. Inositol phosphates exist in various states of phosphorylation and isomeric forms (e.g., myo, d-chiro, scyllo, neo). The myo stereoisomer is the most common in nature, although neo-, scyllo-and d-chiro are also present in terrestrial and aquatic environments [START_REF] Turner | Inositol phosphates in the environment[END_REF][START_REF] Cosgrove | Forms of Inositol Hexaphosphate in Soils[END_REF]. In terrestrial environments, Inositol phosphates are synthesized in plants (seeds), almost exclusively as the inositol hexakisphosphate (IHP) stereoisomer ( Turner 2008;[START_REF] Nash | Using organic phosphorus to sustain pasture productivity: A perspective[END_REF].

The IHP isomer is known under different names: "phytic acid" for the free acid form, and "phytate" for the salt of phytic acid. In older texts,"phytin" is sometimes used to refer specifically to the Ca-phytic acid or Mg-phytic acid salt [START_REF] Cosgrove | The chemical nature of soil organic phosphorus. I. Inositol phosphates[END_REF]Peperzak et al., 1959). Inositol hexakisphosphate represents the main OP form in most legumes, cereals and oil seeds [START_REF] Kasim | The analysis for inositol phosphate forms in feed ingredients[END_REF]. It has also been reported in animal wastes (2-60% total OP), bacteria and fungi [START_REF] Cosgrove | The chemical nature of soil organic phosphorus. I. Inositol phosphates[END_REF]Peperzak et al., 1959). Between pH 5 and 12 IHP possesses an axial structure and an equatorial structure outside this range [START_REF] Turner | Inositol phosphates in the environment[END_REF]. The chemical structure of IHP is shown in Figure 1. In most OP adsorption studies, IHP is found to exibit the higher adsorption capacity. This strong reaction means that IHP undergoes preferential stabilization, which prevents interaction with hydrolytic enzymes and results in its accumulation to form frequently the dominant fraction of OP in soils [START_REF] Harrison | Soil Organic Phosphorus: A Review of World Literature[END_REF].

In a study evaluating the affinity of OP forms, Celi et al. (1999) have reported an adsorption ratio of 3:2 between IHP and IP at pH 4.5. Later, Celi et al. (2004) confirmed the greater affinity of IHP than IP on goethite, with maximum values of 3.6 for IHP and IP for 2.4 mmol P m -2 . Similarly, based on Langmuir bonding strenght values, [START_REF] Celi | Abiotic reactions of inositol phosphates in soil[END_REF] found that goethite shows a higher affinity for IHP than for the other OP and IP forms. Li et al. (2018b) reported a maximum IHP adsorption of 1.95 mmol P m -2 at pH 5 which is close to the value of 1.20 mmol P m -2 obtained by Ganta et al. (2021). The details of IHP adsorption on goethite have been extensively studied (Celi et al. 1999;[START_REF] Celi | Abiotic reactions of inositol phosphates in soil[END_REF][START_REF] Celi | Effects of pH and Electrolytes on Inositol Hexaphosphate Interaction with Goethite[END_REF]Johnson et al. 2012). Comparing the adsorption capacity values of the Freundlish model for IHP and IP, Ganta et al. (2021) showed that the adsorption of IHP was about 1.58 times that of IP, very close to those reported by Celi et al. (1999). The adsorption of IHP generally leads to a faster saturation of the soil mineral surface than that of GLY and IP. This was confirmed on the basis of the order of Freundlich exponent values (IHP < GLY < IP) applied to goethite. This faster saturation is due to the fact that even if IHP binds to goethite via some phosphate groups, the remaining phosphate groups, often deprotonated, would induce a more negative charge on the surface compared to the IP and GLY cases (Xu et al. 2017;[START_REF] Celi | Effects of pH and Electrolytes on Inositol Hexaphosphate Interaction with Goethite[END_REF]). Furthermore, it was found that GLY leads to a more negatively charged surface than IP (Xu et al. 2017). This explains why the Freundlich exponent value for GLY is lower than for IP. The adsorption of IHP onto common soil mineral occurred through ligand exchange at the surface, releasing OH -and H2O into the solution, and the formation of an inner sphere complex (Lü et al. 2017;Ognalaga et al. 1994). Nevertheless, phosphate groups have been found to also form an outer sphere complex [START_REF] Yadav | Bioavailability of Soil P for Plant Nutrition[END_REF]. As a predominant mechanism, the binuclear-bidentate complex has been widely suggested to explain OP adsorption on soils (Johnson et al. 2012). The bonding stability between sorbate and sorbent can be expressed by the affinity constant. A high affinity constant means a rapid uptake and strong bonds or associations between P compound and soils components (Ruttenberg and Sulak, 2011). Some of the factors that influence the stability of IHP are soil texture, pH, organic matter content, climate and soil management/land use. The most important soil property controlling the variation in IHP content is the clay type and content in soil. Inositol hexakisphosphate is more strongly sorbed to illite than kaolinite (Celi et al. 1999). The pH significantly affects the stabilization of IHP.

Acidic soils are known to accumulate more IHP than alkaline soils, which is due to the higher concentration of Fe and Al in solution at acidic pH [START_REF] Harrison | Soil Organic Phosphorus: A Review of World Literature[END_REF][START_REF] Hawkes | A 31P nuclear magnetic resonance study of the phosphorus species in alkali extracts of soils from long-term field experiments[END_REF][START_REF] Goring | Reactions of biological organic phosphorus compounds with clays (Doctor of Philosophy)[END_REF][START_REF] Emsley | the structure of myo-inositol hexaphosphate in solution: 31p n.m.r. investigation[END_REF][START_REF] Celi | Effects of pH and Electrolytes on Inositol Hexaphosphate Interaction with Goethite[END_REF] . Moreover, in soils rich in constituents with variable charges (Al/Fe oxyhydroxides ), its sorption increases with decreasing pH due to the higher positive charge of these constituents [START_REF] Celi | Effects of pH and Electrolytes on Inositol Hexaphosphate Interaction with Goethite[END_REF]. Laboratory study models have provided a better understanding of the reactions of IHP with soil constituents. The higher adsorption of IHP to Fe and Al oxyhydroxides relative to clays reported in some studies was attributed to the electrostatic association of four of the six orthophosphate groups, while only two orthophosphate groups bind with clays. Because of the unattached phosphate groups in IHP, the electrochemical properties are altered and the net negative charge on the particle surface is increased ( Celi et al. 2000). Adsorption of IHP may also be affected by the type of electrolyte in solution. It has been reported that the adsorption of IHP decreases in KCl solution, but increases with CaCl2 (Giaveno et al. 2010;[START_REF] Celi | Effects of pH and Electrolytes on Inositol Hexaphosphate Interaction with Goethite[END_REF]. In any case, the highest affinities of IHP like that of ATP to soil constituents have been explained by the fact that their molecules have more phosphate groups that can coordinate with more hydroxyl (OH) groups on the surface of soil minerals. Also, the phosphate groups of IHP and ATP carry higher negative charges, which leads to a stronger electrostatic attraction with the surface of the soil minerals [START_REF] Celi | Effects of pH and Electrolytes on Inositol Hexaphosphate Interaction with Goethite[END_REF]).

Glucose-6-phosphate

Glucose-6-phosphate (Figure 2) is a glucose sugar phosphorylated at the hydroxy group on C six [START_REF] Adam | Insights into the complexation of glucose-6-phosphate (G6P) with V(III), Ru(III), Au(III), and Se(IV) ions in binary solvent system[END_REF]. It plays an important role in the carbohydrate metabolism of all bacterial and plant organisms [START_REF] Cui | Development of a glucose-6-phosphate biosensor based on coimmobilized p-hydroxybenzoate hydroxylase and glucose-6-phosphate dehydrogenase[END_REF]. It acts in several catabolic pathways to generate energy in the form of ATP. In the environment, we also have Glucose-1-phosphate which is only a stereoisomer of G6P.

Glucose-6-phosphate level can provide information on the activities of enzymes such as G6P dehydrogenase, phosphoglucomutase, hexokinase and phosphoglucose isomerase [START_REF] Coevoet | Irreversible Metabolic Transitions: The Glucose 6-Phosphate Metabolism in Yeast Cell-Free Extracts[END_REF]. Glucose-6-phosphate regulates the activity of certain enzymes, such as glycogen synthase, a protein kinase [START_REF] Bellaver | Ethanol formation and enzyme activities around glucose-6-phosphate in CBS 6556 exposed to glucose or lactose excess[END_REF][START_REF] Sergeeva | In situ staining of activities of enzymes involved in carbohydrate metabolism in plant tissues[END_REF]. Glucose-6-phosphate is a "low energy" phosphate compound because its free-hydrolysis energy is only -13.8 kJ mo1 -1 , which is significantly lower than some other OP forms such as IHP (approximately -58.5 kJ mol -1 ) [START_REF] Katti | The structure of the monobarium salt of glucose 6-phosphate heptahydrate[END_REF]. There are many studies that focus on intracellular biochemistry of G6P but there is limited information on the availability of P from these organic forms of P in soil. A couple of studies on G6P adsorption on soil minerals reported that G6P is potentially more available than IHP (Goebel et al., 2017;Yan et al., 2014). The G6P sorption density and rate is higher than IHP and ATP as a result of its lower molecular weight (Giaveno et al., 2008;Ruttenberg and Sulak, 2011). At low pH values, boehmite, hematite and goethite preferentially adsorb G6P and glucose-1-phosphate than the other forms of OP (Johnson al. 2012). Moreover, Olsson et al. (2010) showed that glucose-1-phosphate an isomer of G6P formed three types of surface complexes on goethite in a pH-dependent fashion. Furthermore, G6P was reported exibit higher adsorption at outer surface sites than IP due to it pore size effects (Goebel et al., 2017).

Glycerophosphate

Glycerophosphate is a phosphoric ester of glycerol. It is a phosphomonoester which is characterized by a single ester bond with the orthophosphate (Figure 3). Glycerophosphate like all the other OP forms acts as a donor of phosphate groups during its mineralization in the soil. In manure-amended soils, GLY is found in its α and β form, but β-glycerophosphate (β-GLY) is generally reported as the most common and important form (Li et al. 2018a;[START_REF] Doolette | Spiking Improved Solution Phosphorus31 Nuclear Magnetic Resonance Identification of Soil Phosphorus Compounds[END_REF]. β-glycerophosphate is also referred as βphosphoglycerol, glycerol 2-phosphate, or under the IUPAC name as 1,3-dihydroxypropan-2-yl dihydrogen phosphate. The plant availability of GLY has been established by a few studies and its use as a P source has been tested. Following incubation for 24 h in 5 ml of a solution containing 250 µg GLY at pH 5.1, samples of 18 mycorrhizal roots completely hydrolysed the ester. A second experiment showed that hydrolysis was rapid and that 10 root tips could completely hydrolyse within 90 min 300 µg contained in 2.5 ml at pH 4.8 [START_REF] Bartlett | Surface phosphatase activity of mycorrhizal roots of beech[END_REF]. [START_REF] Wang | Utilization of dissolved organic phosphorus by different groups of phytoplankton taxa[END_REF] reported that the contribution of GLY as a sole P source supported the growth of different phytoplankton taxa groups more than control with IP, with relative growth between 109% and 165%.

The adsorption of GLY are dependent on the properties of different soils. Li et al. (2018b) suggested that GLY adsorbs onto the goethite surface by forming inner-sphere complexes through the phosphate group. [START_REF] Hori | Preconcentration of some phosphoruscontaining anions by adsorption on hydrated iron(III) oxide[END_REF] showed that GLY adsorbs onto hydrated iron (Fe +3 ) oxide precipitates. In addition, GLY exhibits strong interaction with boehmite, α-Al2O3 and Al(OH)3 (Yan et al. 2014) , and also with ferric oxide (Anderson et Arlidge 1962). In soil, DNA of bacterial origin exists as linear chromosomal DNA, as well as supercoiled plasmids (Poly et al., 2000). Like other OP forms, phosphodiesters such as DNA can be protected from dephosphorylation by adsorption to the soil matrix, but several factors can affect that process [START_REF] Levy-Booth | Cycling of extracellular DNA in the soil environment[END_REF]. At pH 5 to 7, DNA and RNA are usually negatively charged and their adsorption to minerals is thus facilitated by cationic bridging. However, at a pH below 5, they are positively charged and thus less adsorbed [START_REF] Cai | Interactions of DNA with Clay Minerals and Soil Colloidal Particles and Protection against Degradation by DNase[END_REF][START_REF] Greaves | A Study of the Breakdown of Organic Phosphates by Micro-organisms from the Root Region of Certain Pasture Grasses[END_REF]. Structural changes in DNA molecules adsorbed by soil, sand, humic acids, and mineral or organomineral complexes may result in changes in their bioactivities and affect the degradation of DNA by nucleases [START_REF] Franchi | Clay-nucleic acid complexes: characteristics and implications for the preservation of genetic material in primeval habitats[END_REF][START_REF] Peters | Effect of molecular characteristics of DNA on its adsorption and binding on homoionic montmorillonite and kaolinite[END_REF]. The level of adsorption and protection of DNA by soil particles varied significantly with DNA configuration and the type of the adsorbent [START_REF] Lorenz | A methodological approach for deriving regional crop rotations as basis for the assessment of the impact of agricultural strategies using soil erosion as example[END_REF][START_REF] Demanèche | Evaluation of biological and physical protection against nuclease degradation of clay-bound plasmid DNA[END_REF]. [START_REF] Demanèche | Evaluation of biological and physical protection against nuclease degradation of clay-bound plasmid DNA[END_REF] showed that illite provided a lower level of protection for DNA molecules than montmorillonite and kaolinite. Higher level of adsorption and protection of DNA was found with montmorillonite and organic clays compared to kaolinite and clays [START_REF] Cai | Interactions of DNA with Clay Minerals and Soil Colloidal Particles and Protection against Degradation by DNase[END_REF]. The protection of DNA against nuclease degradation by soil colloids and minerals is apparently not controlled by the adsorption affinity of DNA molecules for the colloids and the conformational change of bound DNA.

The higher stability of DNA is likely to be attributed mainly to the presence of organic matter in the system and the adsorption of nucleases on soil colloids and minerals [START_REF] Cai | Interactions of DNA with Clay Minerals and Soil Colloidal Particles and Protection against Degradation by DNase[END_REF]). However, the adsorption and protection of DNA by soil particles to enzymatic degradation is not totally understood, as is also the influence of parameters such as mineral constituents, organic matter, and particle size of soil colloids [START_REF] Paget | On the track of natural transformation in soil[END_REF]. This information would be of fundamental significance for the understanding of the behavior of DNA and related P forms in soil environment.

Effect of OP characteristics on relative OP sorption in soils

The accumulation and distribution of OP from soils are greatly influenced by adsorption and desorption (Figures 4 and5) phenomenon ( Xu et al. 2017). In general, the molecular size and structure of OP compounds influence the sorption dynamics in soil (Yan et al., 2014). By using different synthetic soil constituents (goethite and hematite), the results of Lü et al. (2017) suggest that OP sorption rates might be classified as follows: IP > Adenosine monophosphate (AMP) = G6P > ATP, showing a downward trend in sorption levels with increasing molecular weight of the different OP forms. This means that the larger the molecular size, the higher the activation energy is required for desorption [START_REF] Shang | Bioavailability of organic and inorganic phosphates adsorbed on short-range ordered aluminum precipitate[END_REF].

The lower affinities of AMP and G6P to soil properties than those of IP are thought to be due to the higher steric hindrance effects caused by the C chain and glucose ring of these compounds (Ruttenberg and Sulak, 2011). Steric hindrance at a given atom in a molecule such as P is congestion caused by the physical presence of surrounding ligands, which can slow or prevent reactions to P. Steric hindrance occurs when the volume occupied by one part of a molecule interferes with the approach of a reagent or another part of the molecule.

Conversely, recent studies have shown a trend towards increasing rather than decreasing sorption levels with increasing molecular weight of the different forms of OP. Such as, for example, the work of Ganta et al. (2020) which shows on the basis of the Langmuir and Freundlich model that the adsorption capacity and strength increase in the following order: GLY < IP < IHP. Suggesting that despite the larger molecular size of IHP, the steric hindrance effect due to its large organic molecule would not have occurred. The explanation put forward was that the organic fraction of IHP might not influence the individual phosphate, but only the conformational flexibility of the overall bonding process (Ganta et al. 2019b). This is consistent with the observation of Celi et al. (1999) showing that the phosphate groups of IHP react with the goethite surface in the same way as the IP forms. A more recent additional explanation shows that on goethite, the Fe-P distances observed for IHP are close to the Fe-P distances for IP and suggest that the organic fraction of IHP may not influence the interaction of individual phosphate groups with goethite (Ganta et al. 2019b;Ganta et al. 2021).

Influence of soil constituents on OP sorption

Iron and Al oxyhydroxides (goethite, gibbsite...), clay minerals (kaolinite, montmorillonite...) and humic substances have attracted considerable attention because of their high P sorption capacity (Ryan et al. 2001;Bortoluzzi et al. 2015). Their P bonding degree depends on their surface areas, crystallinity, number of active surface sites, point of zero charge, and concentration of hydroxyl groups (Ruttenberg and Sulak, 2011). It is assumed that at pH 4-10, gibbsite and amorphous Al(OH)3 would have maximum sorption capacity for IHP (Guan et al., 2006;Yan et al., 2014). Yan et al. (2014) Humic substances, such as humic acids (HA), account for 40-90% of organic matter in soil [START_REF] Hur | Effects of pH and phosphate on the adsorptive fractionation of purified Aldrich humic acid on kaolinite and hematite[END_REF]. In most studies, the effect of humic substances on P dynamics has often been ignored due to previous results showing that humic substances would have no effect on P adsorption in soil [START_REF] Borggaard | Influence of humic substances on phosphate adsorption by aluminium and iron oxides[END_REF][START_REF] Gerke | Humic (Organic Matter)-Al(Fe)-Phosphate Complexes: An Underestimated Phosphate Form in Soils and Source of Plant-Available Phosphate[END_REF] . However, the chemical interaction between soil organic matter and IP or OP forms is an important reaction in the soil solid phase, soil solution and even in natural waters [START_REF] Gerke | Humic (Organic Matter)-Al(Fe)-Phosphate Complexes: An Underestimated Phosphate Form in Soils and Source of Plant-Available Phosphate[END_REF]. The adsorption of OP on HA and the effect of the latter on sorption processes have been studied with macroscopic sorption measurements. Large quantities of IHP have been found to be associated with fractions of humic substances in soil (Ruyter-Hooley et al. 2015;[START_REF] Borie | Macromolecule-P associations and inositol phosphates in some chilean volcanic soils of temperate regions[END_REF]). Humic acids can strongly complex metals, mainly by carboxylic and phenolic groups [START_REF] Ritchie | Analytical constraints on acidic functional groups in humic substances[END_REF][START_REF] Tipping | Cation binding by humic substances[END_REF]. Humic-Fe and Al oxyhydroxides complexes can adsorb P, thereby forming "humic-Fe and Al oxyhydroxides-P" complexes. The main bonding mechanism of OP is probably via Fe and/or Al-bridges to the humic matrix, similar to the bonding of the IP anion [START_REF] Gerke | Humic (Organic Matter)-Al(Fe)-Phosphate Complexes: An Underestimated Phosphate Form in Soils and Source of Plant-Available Phosphate[END_REF][START_REF] Negrin | P fractionation in sodium bicarbonate extracts of andic soils[END_REF]Urrutia et al. 2014). A great proportion of OP can be found associated with humic substances [START_REF] Thomas | The occurrence of high molecular weight organic phosphorus compounds in soil[END_REF]. The main sorption mechanisms involve electrostatic interaction and ligand exchange (Figure 4 and 5; [START_REF] Tombácz | The role of reactive surface sites and complexation by humic acids in the interaction of clay mineral and iron oxide particles[END_REF]. The presence of HA would be likely to affect the OP available to plants in soil systems (Ruyter-Hooley et al., 2015). However, more knowledge is needed to understand the nature of the interaction between HA and OP or via Fe or Al bridges in soil. Table 2 summarizes a qualitative annotation of the main research on the adsorption of organic forms of P to the surface of the main soil minerals at pH 4 to 6. (a) Outer-sphere complex electrostatic attraction pH = 1-7, (b) Outer-sphere complex electrostatic repulsion pH = 8-12.

Table 2 : Summary of the main investigations on the adsorption of OP forms on soil minerals under pH 4 to 6.

The sign (+) means that there is an adsorption. The more + signs are present, the greater the adsorption capacity. The sign (0) means that no studies were found concerning the adsorption of the form of P on the mineral. Phosphorus compounds (IHP: myo-inositol hexakisphosphate, GLY: glycerophosphate, G6P: glucose-6-phosphate and IP: KH2PO4); The dashes (-) identify the mineral-phosphorus complexes produced by the adsorption of P forms onto soil minerals. (Parfitt 1979;He et al. 1994) , pH and temperature [START_REF] Barrow | The Description of Phosphate Adsorption Curves[END_REF] may affect the release of P from mineral surfaces to the soil solution and thus the availability of P to plants, but the type of relationship involved is not yet clear. Several authors have suggested that the mineral-OP bridging forms are not available to plants because these complexes are formed during the slow reaction phase with soil minerals [START_REF] Hingston | ANION ADSORPTION BY GOETHITE AND GIBBSITE: II. DESORPTION OF ANIONS FROM HYDROUS OXIDE SURFACES[END_REF]Barrow et Shaw 1975). Hinsinger (2001a) through physicochemical findings, showed that Fe and Al oxyhydroxides bind very strongly to P via inner sphere complexes. This process has been hypothesized to be a major cause of limiting plant growth (Javaid, 2009). The desorption of OP compounds from mineral surfaces would be much lower than for IP.

P forms

Soil

Therefore, the question of the availability of sorbed OP on soil minerals is still not resolved. Recently, -López et al. (2020) showed that when IHP was used as P source for plants, P uptake decreased with increasing Fe oxides concentration in the growing media. Bollyn et al. (2017) showed that after several desorption cycles less than 5% P desorbed from IHP. Similar findings by Ruyter-Hooley et al.

García

(2015) showed limited desorption of IHP (<3% of P) on gibbsite, even in the presence of HA as a competing ligand. From goethite, the amount of IHP desorbed was less than 20% of the amount of desorbed IP, which was attributed to the strength of the bonds and the high negative charge of the complex [START_REF] Nash | Using organic phosphorus to sustain pasture productivity: A perspective[END_REF]. In any case, there is a greater affinity of the OP forms for soil minerals than that of the IP forms, indicating the formation of a very stable complex of OP with mineral surfaces.

Thus, it can be expected that desorption and plant availability of mineral-OP complexes are more difficult than those of IP forms, although this has never been quantitatively defined (Table 3).

Contrary to the result presented above which suggests that mineral-OP bridging forms are not available for plants, there is also some experimental evidence that most of the P taken up by plants comes from the soil mineral-P bridging complex, although sorbed P is not easily or widely desorbed.

This implies that P associated with soil minerals is potentially available to plants, although availability also depends on the type of soil minerals and the P form (Andrino et al., 2019;D'Amico et al., 2020).

Recently, D'Amico et al. ( 2020) exposed mesh bags filled with goethite associated with IP or IHP for 13 months to P-deficient soils in the Italian Alps. More P was lost from the mesh bags, indicating a direct release of P from the mineral surfaces. Parfitt (1979), showed that P sorbed to goethite was available to ryegrass, while Guzman et al. (1994) found that P sorbed to goethite was less available to sunflower than P sorbed to ferrihydrite and hematite. The type of extractor also influences the level of OP desorption. Desorption rates of G6P by KCl and citrate are generally very high compared to those of IHP, ATP and GLY (Yan et al., 2014). However, it was more easily desorbed by citrate than KCl (Table 3). This could be explained by the fact that citrate induces a more important ligand exchange mechanism than KCl. These ligands would compete for sorption sites with sorbed G6P to promote greater desorption [START_REF] Johnson | Role of Organic Acids in Phosphate Mobilization from Iron Oxide[END_REF]Violante 2013). Up to 32.4% of G6P, adsorbed by goethite could be desorbed from Goethite-G6P complexes.

Beyond the few studies on G6P and GLY desorption in soil, there is still limited information on the biogechemical cycling of G6P in agroecosystems; most of the available data refers specifically to IP and IHP. It is therefore important to carry out further research to understand all the mechanisms governing the mobility of G6P and GLY in soil systems in order to improve their availability. In addition, in all the above studies, the behavior of some importante Fe and Al oxyhydroxides minerals (gibbsite, ferrhydrite...) has not been adequately examined and comparable studies with other main soil components (clay minerals and humic substances) have not been conducted. Since OP can constitute up to 80% of the total P in soils amended with organic amendments (Anderson, 1980), it is likely that the phytoavailability (and desorbability) of the different specific OP compounds in soil surface complexes is influenced by their biogeochemical properties (P content, type of P bonding and molecule size...).

Thus, the amount of P available to plants from mineral-OP bridging complexes need to be evaluated and well understood.

Nature of bonding between OP and mineral surfaces

The fate of P in the ecosystem is strongly influenced by the mechanisms by which P is bound to soil mineral surfaces, and a good understanding of these mechanisms is a major key for the development of new strategies to increase P application efficiency. [START_REF] Nash | A comparison of some surface soil phosphorus tests that could be used to assess P export potential[END_REF]Martin et al. 2004;[START_REF] Martin | Soil organic phosphorus: IV. Fractionation of organic phosphorus in alkaline soil extracts and the identification of inositol phosphates[END_REF]Ganta et al. 2020). Recently, [START_REF] Li | Surface Speciation of Phosphate on Boehmite (γ-AlOOH) Determined from NMR Spectroscopy[END_REF] and [START_REF] Wang | Phosphate and phytate adsorption and precipitation on ferrihydrite surfaces[END_REF] investigated the sorption of phosphate onto boehmite using 31 P MAS NMR techniques. Both studies, concluded the formation of a binuclear inner-sphere complex. In previous studies, IHP sorption was suggested to involve only inner-sphere complexation (Ognalaga et al. 1994;Celi et al. 1999;Guan et al. 2006). Guan et al. (2006) and Yan et al. (2014) also proposed inner-sphere complexation to be the dominant sorption mechanism for IHP on amorphous Fe and Al oxyhydroxides. In contrast, work by Johnson et al. (2012) showed that IHP sorption to goethite occurs largely through the formation of outer-sphere complexes.. Furthermore, Ruyter-Hooley et al. (2015) investigated the sorption of IHP onto gibbsite using surface complexation modeling. The result indicated that outer-sphere complexation is important in the sorption process at higher pH, while inner-sphere complexation and surface precipitation are dominant at lower pH. The reactions described two inner-sphere surface complexes (1 and 2) and one outer-sphere complex

(3) as follows:

≡ AlOH + IHP 6 12-+ 5H + ↔ Al [IHP 6 H 4 ] 7-+ H 2 0 (1)
≡ 3AlOH + IHP 6 12-+ 6H + ↔ Al3 [IHP 6 H 3 ] 6-+ 3H 2 0 (2) ≡ 2AlOH + IHP 6 12-+ 4H + ↔ (Al0H 2 ) 2 2+ [IHP 6 H 2 ] 10- (3)
The surface complexation mechanism of P with soil components, especially goethite [START_REF] Cordell | The story of phosphorus: Global food security and food for thought[END_REF], as well as surface complexation models that describe P adsorption have been explored [START_REF] Ahmed | Interaction of polar and nonpolar organic pollutants with soil organic matter: Sorption experiments and molecular dynamics simulation[END_REF]. However, they are not generally successfully applied to the adsorption of OP to soil components and soils [START_REF] Houben | Multi-method characterization of the ferrihydrite to goethite transformation[END_REF][START_REF] Sheals | Adsorption of Glyphosate on Goethite: Molecular Characterization of Surface Complexes[END_REF]. As a result, little is known about the surface complexation of OP with soil.

The nature of the bonding patterns of the adsorbed OP and IP species is still a matter of conflicting debate. In addition, the relative abundance of monodentate (Mono) [START_REF] Sheals | Adsorption of Glyphosate on Goethite: Molecular Characterization of Surface Complexes[END_REF][START_REF] Olsson | Enzymatic Hydrolysis of Organic Phosphates Adsorbed on Mineral Surfaces[END_REF] versus bidentate (Bid) [START_REF] Kim | Phosphate adsorption on the iron oxyhydroxides goethite (α-FeOOH), akaganeite (β-FeOOH), and lepidocrocite (γ-FeOOH): a 31P NMR Study[END_REF]Ganta et al. 2019a) bonding of the soil minerals-P complexes is less known. This was reported in the literature to be related to the presence of different surface planes for soil minerals and multiple bonding motifs for mineral-P complexes. Thus, different views have been put forward to assign mineral-P bonding motifs based on infrared spectroscopy or molecular modeling. Molecular modeling is considered a powerful tool to resolve these conflicting discussions by providing a molecular level description of the nature of the minerals-P complexes formed. By molecular modeling, [START_REF] Kwon | Molecular Orbital Theory Study on Surface Complex Structures of Phosphates to Iron Hydroxides: Calculation of Vibrational Frequencies and Adsorption Energies[END_REF] studied the IP-bonding process to goethite and suggested the abundance of the diprotonated Bid complex at pH 4-6 and the deprotonated or monoprotonated Mono complex at pH 7.5-7.9. Similarly, Ganta et al. (2019a) microbes and plants overcome to recover P from the strong IHP-mineral bond. However, despite the presence of a significant number of studies reporting the bonding pattern of IP, IHP and GLY on the surface of goethite, such an in-depth atomistic investigation for the bonding mechanisms of OP at the interface of all major soil minerals is still lacking (Ganta et al. 2021). A more detailed knowledge of the interaction of P with these components will provide a better understanding of the interaction and availability of P with these soil mineral components.

There is no consensus in the literature on the number of phosphate groups of the IHP that bind to the goethite surface or on the dominant bonding motifs. Ganta (2020) and Ganta et al. (2021) found for goethite-IHP complexes the Mono and 3Mono bonding motifs, which is supported in the literature previously [START_REF] Arai | Phosphate Reaction Dynamics in Soils and Soil Components: A Multiscale Approach[END_REF]. However, no clarity on which bonding motif would be dominant.

The 3 Mono (Guan et al. 2006;Ganta, et al. 2019b), 2Mono (Guan et al. 2006;Ganta et al. 2020) and 1Mono ( Ganta et al. 2019) motifs are already reported for IHP on minerals. In contrast, Johnson et al. (2012) proposed that IHP interacts with goethite by forming outer-sphere complexes, which conflicts with much of the literature. Also, it is surprising to note that none of the above studies concerning IHP suggest that it forms a binuclear Bid motif, as suggested in other previous studies (Guan et al. 2006) .

However, this seems understandable since it was found that the initial Bid motif of IHP is not stable.

Compared to IP, the adsorption of GLY on soil minerals has not been extensively studied and, therefore, information on its bonding patterns is limited. Based on the analysis of FTIR spectra, GLY would form inner-sphere complexes with goethite with only Mono motifs on the surface [START_REF] Li | Adsorption of glycerophosphate on goethite (α-FeOOH): A macroscopic and infrared spectroscopic study[END_REF].

Similarly, studies of the bonding mechanisms of monomethyl phosphate (CH3-H2PO4), an organic P with a single phosphate group like GLY and that of glyphosate, have shown that it forms mainly Mono units with goethite [START_REF] Persson | Structure and Bonding of Orthophosphate Ions at the Iron Oxide-Aqueous Interface[END_REF][START_REF] Sheals | Adsorption of Glyphosate on Goethite: Molecular Characterization of Surface Complexes[END_REF]. It has also been suggested that the phosphate group of GLY interacts with the mineral surface in a very similar way to IP forms. This is because it has been suggested that the Fe-P distances observed in the GLY are in the range of the Fe-P distances observed for IP in the literature [START_REF] Rose | Genotypic variation in grain phosphorus concentration, and opportunities to improve P-use efficiency in rice[END_REF][START_REF] Tribe | Molecular Orbital Theory Study on Surface Complex Structures of Glyphosate on Goethite: Calculation of Vibrational Frequencies[END_REF]. Summarizing this literature data, the Mono motif would appear to be the dominant motif for GLY type molecules on the surface of soil minerals, more precisely goethite.

It is very important to keep in mind that the different bonding patterns reported depend very strongly on the properties of the soil, specifically the saturation level of the soil minerals. Tejedor-Tejedor et [START_REF] Tejedor-Tejedor | The protonation of phosphate on the surface of goethite as studied by CIR-FTIR and electrophoretic mobility[END_REF] and George Anderson (1980) proposed that the Bid motif is the dominant motif, for low surface coverage of IP on goethite in the pH range of 3.6-8.0. In addition, they proposed that the Mono motif exists at low surface coverage but as a non-dominant motif. Using Density functional theory (DFT) calculations, [START_REF] Kwon | Molecular Orbital Theory Study on Surface Complex Structures of Phosphates to Iron Hydroxides: Calculation of Vibrational Frequencies and Adsorption Energies[END_REF] concluded that the Bid motif is dominant between pH 4-6. Recently, a joint approach by [START_REF] Ahmed | Infrared spectroscopic characterization of phosphate binding at the goethite-water interface[END_REF] involving adsorption experiments and DFT simulations showed that the Mono motif is dominant at both extremely low and high pH values, while the Bid motif is dominant in the intermediate pH range.

Bonding energy and strength of OP sorption to soil mineral surfaces

A challenge for further studies and application is to understand and explore the mechanisms by which microbes and plants can overcome the strong OP-mineral bonding and incorporate or uptake the phosphate groups into their metabolism. This would requied better knowledge of the interaction energy of P and soil minerals. The interaction energy between P and the mineral surface could be calculated by using eq (4) ( Ganta et al. 2021;Ganta et al. 2020):

𝐸 𝑖𝑛𝑡 = 𝐸 𝑠-𝑃 𝑐𝑜𝑚𝑝𝑙𝑒𝑥 -(𝐸 𝑠 + 𝐸 𝑃 ) (4)
Here, ES-P complex denote the total electronic energies of the soil-phosphate complex, EP electronic energies of P forms and ES the soil minerals surface one.

It has been reported that mineral-GLY binding complexes exhibit a higher binding interaction energy for the Bid motif than the Mono motif by a factor of 2.4, probably due to a greater number of deprotonation steps. For the mineral-IHP complexes, the 3Mono motif of the IHP has a higher interaction energy than the more stable 3Mono motif, but shows a 1.2-fold lower interaction energy per bond (Ganta et al. 2021;[START_REF] Ahmed | Infrared spectroscopic characterization of phosphate binding at the goethite-water interface[END_REF]. Based on these results, it is clear that if the two species (Gly and IHP) are competing for the same active sites on the soil surfaces, the bonding of IHP will be dominant. Morever, molecular dynamics simulations on adsorption data have reported total interaction energies measured for goethite-IP and goethite-GLY complexes to range from -20 to -81 kcal mol -1 depending on the type of bond (Mono or Bid) [START_REF] Ahmed | Infrared spectroscopic characterization of phosphate binding at the goethite-water interface[END_REF]Ganta et al. 2021;Kubicki et al. 2012;Rakovan et al. 1999). But the interaction energies per P-bond for the GLY motif is higher than that of IP (Ganta et al. 2021). The difference comes from the glycerol group in GLY. Both IP and GLY interact through one phosphate groupe, but through the glycerol group, GLY has a higher solvent accessible surface area and shows a stronger interaction with water than IP [START_REF] Ahmed | Infrared spectroscopic characterization of phosphate binding at the goethite-water interface[END_REF]. A similar observation was made for GLY on the surface of diaspore [START_REF] Li | Adsorption of glycerophosphate on goethite (α-FeOOH): A macroscopic and infrared spectroscopic study[END_REF], which is isomorphic to goethite [START_REF] Cordell | The story of phosphorus: Global food security and food for thought[END_REF] . Morever, Xu et al. (2019) showed that GLY induces a more negative charge on hematite than IP, which could also influence the strength of Fe-OP covalent bonds. This helps to understand why the desorption of GLY would be under certain conditions more difficult than IP forms. The bonding energies of the IHP to minerals would be between -69 and -85 kcal mol -1 , generally higher than IP forms (Ganta et al. 2021;Ganta et al. 2020;[START_REF] Ahmed | Interaction of polar and nonpolar organic pollutants with soil organic matter: Sorption experiments and molecular dynamics simulation[END_REF]. Of the three types of the bonding motif reported in the literature for IHP on soil minerals, the 3Mono has a higher total interaction energy than the 2Mono due to the additional covalent bonds and proton transfer from IHP to the mineral surface. However, the interaction energy per bond between IHP and goethite for the 3Mono motif has been reported to be lower than that of the 2Mono motif. The Table 4 presents the bonding patterns of P-forms and their interaction energies per number of bonds on goethite and two diaspore surface planes.

In summary, there is still much to be known about the nature, interactions motif and strenght of OP forms at all soil mineral surfaces. Therefore, it is important to develop new methods that would provide a better understanding of these mechanism. Recently, Ganta et al. (2021) suggested that a molecular-level understanding of the mechanisms of P bonding to soil mineral surfaces may be key to developing new strategies for more efficient application of P. Thus, much experimental work has been done to understand P bonding to several reactive and abundant minerals, including goethite (α-FeOOH).

From our investigations, atomistic modeling of mineral-P complexes using molecular dynamics simulations is emerging as a new tool, which provides more detailed information on the mechanisms, nature and strength of bonding processes. However, it is mostly applied to IP forms than to OP. Since forms such as GLY, IHP, and G6P are abundant species in forest soils and soils amended with organic amendments, such a detailed atomistic investigation for their bonding mechanisms at the mineral interface needs to be further investigated. Diaspore (α-AlOOH) is isomorphous with goethite having an Al +3 oxidation state instead of Fe +3 . Compared with goethite it exhibits a higher surface energy [START_REF] Guo | Naturally occurring iron oxide nanoparticles: morphology, surface chemistry and environmental stability[END_REF]Ganta et al. 2021;Ganta et al. 2019b

Modeling OP sorption for sustainable P management

The mechanisms that govern the dynamics of the OP forms, even if they are still not well investigated in relation to IP, are in general understood, but we do not know the relative importance of each of these mechanisms on the fate of P in the soil and therefore models are needed in order to understand more.

Studies of OP composition across environmental gradients demonstrated that soil properties exert a strong control on the amounts and forms of OP in some Fe and Al oxyhydroxides (McDowell et Stewart (2005). Vincent et al. (2012) found that distribution of OP species in agricultural soil depend on level of Al and Fe sites, due to the stabilizing effect of these metal oxides. Therefore, sorption of OP on Fe and Al oxyhydroxides have attracted considerable attention (Ryan et al. 2001;Bortoluzzi et al. 2015), however clay minerals (kaolinite, montmorillonite...) effect on OP dynamic is less studies despite it is also major component of soils and sediments. Of all the soil minerals, the effect of humic substances on OP fate is often ignored because of results showing that humic substances have no or little effect on P adsorption to soil components. However, soil humic substances account for 40-90% of organic matter in soil and the bonding of the IP anion at the humic surface is found to be similar to the bonding to Fe/Al-hydroxides. Therefore, we strongly suggested to include humic substances effect on OP sorption process.

It is clear that the number of the P groups in a certain OP compound is determining the stability of its complex with the mineral surface however it depend on surface plane of soil minerals. Given the lack of knowledge on the surfaces plane of soil minerals and the chemical nature of OP species, the nature of their bonding is not well understood. Different opinions have been put forward to assign bonding motifs based on infrared (IR) spectroscopy (Tejedor-Tejedor et [START_REF] Tejedor-Tejedor | The protonation of phosphate on the surface of goethite as studied by CIR-FTIR and electrophoretic mobility[END_REF]. Molecular modeling is considered as a powerful tool to resolve such conflicting discussions by providing a molecular level description for the nature of the formed mineral-P complexes. However, this model has been generaly applied on goethite and IP form (Kubicki et al., 2012). Therefore, we suggested future investegation to introduce a molecular level understanding for the bonding mechanism of OP species via a joint experimental and theoretical approach. Further, simulation of adsorption experiments could be carried out by molecular modeling for the bonding processes of especially major OP forms (IHP, GLY, G6P), by applying hybrid quantum mechanics/molecular mechanics-based molecular dynamics simulations.

Soil minerals-OP transformation and availability in soil comprises a set of interconnected physical, chemical and biological processes such as percent P saturation (Parfitt 1979;He et al. 1994) , residences time, pH and temperature. It characterizes by multiple linear or nonlinear responses and thresholds depending on soil minerals. Future advances in P availlibility from minerals-OP complexes will require careful application of numerical models that quantitatively describe their past and present changes from laboratorie studies and forecast their variation trends in the future to fild level. The recent development of a numerical modeling approach for data evaluation by [START_REF] Müller | A 33P tracing model for quantifying gross P transformation rates in soil[END_REF] provides new opportunities to study OP transformations in a wide variety of native and agricultural ecosystems [START_REF] Huang | One-pot synthesis of Fe(III)-coordinated diamino-functionalized mesoporous silica: Effect of functionalization degrees on structures and phosphate adsorption[END_REF]Turner et Laliberté 2015). However, this model does not include any mineral-OP bridging complexes which dynamic are potential sources of P in soil. Similar approaches could therefore be applied to modeling mineral-OP bridging complexes transformation and availability in soil. Morever, data on rates of P desorption from mineral-OP bridging in the laboratory should be compared to rates derived in the field.

Summary and perspectives

Current knowledge has led to a better understanding and identification of the processes that limit the availability of P to crops and ways to improve it by increasing access to OP. Given the importance of OP for global food security and its critical roles in soil biogeochemical cycling (Vance et al. 2003), its dynamics in natural soils as well as experiments involving comparison of specific forms of OP in agricultural soils need to be studied in combination with the use of state-of-the-art techniques in order to understand better the basic principles and mechanisms governing the sorption process of OP forms with soil mineral surfaces. In addition, the transformation and availability of P from mineral-OP bonding complexes needs to be studied under different land use conditions in order to develop extensive databases to quantitatively model and predict the availability of P from such complexes. This would contribute to optimize the management of P in cropping systems, especially those amended with organic inputs, while limiting negative impacts on the environment.

Despite intensive efforts to understand and characterized the complexity of OP forms dynamics and behavior when they arrive in the soil, the relative proportions, pathways and thresholds of OP species transformation in organic amendments amended soil and especially its interaction or competition with existing OP pools in soils remain largely unknown [START_REF] Fang | Phosphorus adsorption onto clay minerals and iron oxide with consideration of heterogeneous particle morphology[END_REF]. Therefore, it is important to highlight the role of the OP form from organic amendments application in changes in existing soil P forms over time by well characterizing both chemical and soil properties involved in P dynamics. In addition to add different OP species to soil, decomposition of organic amendment may generate humic substances and organic acids that can be adsorbed into soil surfaces, decreasing the potential P adsorption by blocking sites for the formation of complexes with Al, Fe and Ca (Fuentes et al. 2006;[START_REF] Fuentes | Dynamics of phosphorus and phytate-utilizing bacteria during aerobic degradation of dairy cattle dung[END_REF]). Thus, the characteristics of organic amendments that could reduce or increase the sorption strength of the OP on soil minerals need to be further investigated. A thorough understanding of the amount of P in the soil-plant system and the time period during which P adsorbed in soil and organic matter is released for uptake by cops is strongly needed to improve P use in agricultural ecosystems.

In the course of our investigation, we noted that IHP, GLY and G6P mobility and availability for plants is limited due to its strong bonding to the soil solid phase. Moreover, despite several studies on some Fe and Al oxyhydroxides, their relationship with clay minerals and humic substances is scarce.

Their use as sole P fertilizer has been tested by some laboratory studies (Wang et al. 2012), but no recent studies have been done to determine its availability in agricultural production conditions. Hence, we strongly suggest that future research could focus on understanding the extent to which these P forms react on soil compounds, how they are used by plants and how this could be improved in the perspective of an efficient organic fertilization. Nevertheless, there has been substantial progress on adsorption rates of total OP or specifics OP (IHP) based on incubation experiments. However, the rates measured in the laboratory should be compared to rates derived in the field. Further, studies on the effect soil porperties on the OP residence time and turnover in different soils composition are also required to elucidate the relative importance of biological and biochemical processes in adsorbed OP transformation. There is also a need to investigate rates and changes in different OP forms such as IHP, GLY and G6P across various soil chronosequences in order to formulate numerical models that can predict future major OP forms adsorption and transformations process.

1.2 Unravelling the role of rhizosphere microbiome and root traits in organic phosphorus mobilization for a sustainable phosphorus fertilization. A review

Introduction

Phosphorus is a limiting nutrient for the productivity of agroecosystems (Filippelli, 2008;Jarvie et al., 2019;[START_REF] Withers | Stewardship to tackle global phosphorus inefficiency: The case of Europe[END_REF]. This is due to its low availability in soil which results from its low solubility and its strong affinity for mineral surfaces. Phosphorus fertilization is therefore needed to achieve high yields. Most of the P currently used in chemical fertilizers is derived from phosphate rocks [START_REF] Schoumans | Phosphorus management in Europe in a changing world[END_REF]. These resources are unevenly distributed at the Earth surface and, in European Union (EU), food production is dependent on imported primary P [START_REF] Cordell | The story of phosphorus: Global food security and food for thought[END_REF][START_REF] Schoumans | Phosphorus management in Europe in a changing world[END_REF].

Because the reserves are located only in a few places on Earth and thus controlled by few countries, the EU's P supply is vulnerable to geopolitical issues with possible problems with the accessibility and price of P fertilizers on the mid-term [START_REF] Cordell | The story of phosphorus: Global food security and food for thought[END_REF]. Additionally, phosphate rock is a strategic resource whose mining can lead to occupations and armed conflicts. Moving towards more sustainable sources for managing P in cropping systems, renewable nutrient-rich organic amendments are increasingly considered to complement P fertilizers produced from phosphate rocks, not only by scientists but also by politics and stakeholders (Bennett and Schipanski, 2013). The use of organic inputs represents shifting from a linear use of a limited resource towards a circular economy because it promotes the reduction of fossil fuel use and greenhouse gas emissions (McCormick and Kautto, 2013) while contributing to the development of new green markets (Zulkifli et al., 2019) and jobs by promoting the conversion of waste into value-added products [START_REF] Bracco | Assessing the Contribution of Bioeconomy to the Total Economy: A Review of National Frameworks[END_REF][START_REF] Mohanty | No title found[END_REF][START_REF] Scarlat | The role of biomass and bioenergy in a future bioeconomy: Policies and facts[END_REF]. The use of organic inputs could makes the transition to sustainable agriculture a priority, focusing on prevention of environmental impacts, through the adoption of innovative technological systems (Zulkifli et al., 2019). The sustainability benefit of using renewable organic P depends on farming systems types associated to a with low carbon emissions from renewable P traffic, such as livestock farming systems using which use effluents or digestates, or other farming systems using which use agroindustriesy coproducts at territory scale, and urban and peri-urban agri-culture systems that valorize sludges. Using organic inputs as a sustainable and renewable resource is a necessity to address the socioeconomic and scientific issues that have recently been raised concerning sustainable P management approaches.

Organic inputs cover a large diversity of matters, including raw or treated livestock manure, food industry, urban or domestic sludge from water purification operations or wastewater treatment, raw materials, water and sewage sludge, paper, petroleum, textile, chemical, bio-waste (green waste composts, organic household or domestic waste), the digestates composted or not from mechanization, ashes, in particular, biomass burning, sediments dredged and biochar's (materials resulting from the pyrolysis of certain wastes). The agronomic interests for organic inputs are well documented [START_REF] Houot | Intérêts et limites de la substitution par la fertilisation organique[END_REF]. For instance, in France, 78% and 62% of P and N respectively used in agriculture derive from organic inputs [START_REF] Houot | Recyclage de déchets organiques en agriculture : effets agronomiques et environnementaux de leur épandage, Matière à débattre et décider[END_REF]. However, unlike conventional P fertilizers, such as triple superphosphate, P is present in organic inputs in various inorganic and organic forms which vary in their availability to plants (Faucon et al., 2015). Most research on the fate of P applied to soil has focused on the dynamics of inorganic P (IP). In contrast, the fate of OP forms, that can account for up to 80% of total soil P (Andrino et al., 2019;[START_REF] Harrison | Soil Organic Phosphorus: A Review of World Literature[END_REF] has been neglected to date, and there is still a lack of knowledge about the contribution of these forms to plant nutrition (Faucon et al., 2015). A study by Kahiluoto et al. (Kahiluoto et al., 2015) shows that OP from organic inputs would be more available than P from chemical fertilizers. Nevertheless, this availability is affected by rhizosphere microbiome and root traits (Sulieman and Mühling, 2021;[START_REF] Sulieman | Phosphorus homeostasis in legume nodules as an adaptive strategy to phosphorus deficiency[END_REF][START_REF] Zogli | Physiological and Molecular Mechanisms and Adaptation Strategies in Soybean (Glycine max) Under Phosphate Deficiency[END_REF]. Therefore, a better understanding of the interactions between OP forms, root traits, and rhizosphere microbiomes can help to better manage P fertilization.

In its definition, OP is any compound that contains an organic moiety in addition to P. The P atoms are covalently bonded to C via a phosphoester linkage (P-O-C), or phosphodiester linkage (C-O-P-O-C), or directly bonded to C (P-C). In a wider definition, it would include phosphate which is associated with organic matter. Through the utilization of different technologies from sequential extractions to 31 P NMR spectroscopy, OP compounds have been identified and quantified in various organic inputs. This has been a major step in the better understanding of the different forms of OP, their quantities and dynamics. Globally, both organic input and soil contains numerous OP forms in varying amounts. The notable forms are those belonging to phosphomonoesters, e.g., inositol phosphates, phosphodiesters, e.g., nucleic acids, and organic polyphosphates, e.g., adenosine triphosphate [START_REF] Nash | Using organic phosphorus to sustain pasture productivity: A perspective[END_REF]Stutter et al., 2015). Among these compounds, specifics forms such as inositol hexakisphosphate (IHP) (Turner et al., 2002b;Vestergren et al., 2012;Vincent et al., 2013), glycerophosphate (GLY) [START_REF] Doolette | Spiking Improved Solution Phosphorus31 Nuclear Magnetic Resonance Identification of Soil Phosphorus Compounds[END_REF](Doolette et al., , 2011;;Newman and Tate, 1980), and glucose-6phosphate (G6P) [START_REF] Cui | Development of a glucose-6-phosphate biosensor based on coimmobilized p-hydroxybenzoate hydroxylase and glucose-6-phosphate dehydrogenase[END_REF][START_REF] Hogema | Catabolite repression by glucose 6-phosphate, gluconate and lactose in Escherichia coli[END_REF]Vincent et al., 2013) are generally considered major forms. In addition to these species, several other OP are potentially active but poorly characterized and remain somewhat puzzling (Richardson and Simpson, 2011). Each form differs from the others by its P content, and molecule size. These biochemical properties to which are added their adsorption, desorption and hydrolyzation processes control their fate and thus their availability to plants. The mobilization of each OP to plant is driven by soil microbes and root traits in the soil-plant continuum [START_REF] Bünemann | Phosphorus and sulphur cycling in terrestrial ecosystems[END_REF][START_REF] Lazali | Stratégies et mécanismes d'adaptation des légumineuses à la faible disponibilité des sols en phosphore[END_REF]. Indeed, soil microbes living freely in the complex plant-soil system (Richardson, 2005), can significantly control the status and turnover of OP and ultimately its availability in the soil [START_REF] Margenot | Biological P cycling is influenced by the form of P fertilizer in an Oxisol[END_REF]. Furthermore, in response to P deficiency, plants have developed numerous strategies that allow them to mobilize OP and assimilate IP with greater efficiency in soils. These are morphological, physiological, biochemical and molecular mechanisms [START_REF] Jain | Molecular mechanisms of plant adaptation to phosphate deficiency[END_REF][START_REF] Skene | Pattern Formation in Cluster Roots: Some Developmental and Evolutionary Considerations[END_REF]. These strategies consist of (i) increased root growth, (ii) the establishment of specialized organs, (iii) the expression of high-affinity IP transporters, (iv) the secretion of root exudates and specific enzymes [START_REF] Jones | Plant and mycorrhizal regulation of rhizodeposition[END_REF][START_REF] Lazali | Examples of belowground mechanisms enabling legumes to mitigate phosphorus deficiency[END_REF] and (v) symbiotic association with rhizosphere microbiome. It is therefore very likely that the potential of recycled P fertilizers to increase plant uptake depends not only on the forms and biochemical properties of the different OP, but also on the mobilization/acquisition process by microbes and strategies (e.g.

protons, carboxylates and phosphatase release...) used by plants to increase P availability. Thus, to predict the availability of P in cropping systems, it is very important to consider both the characteristics of the OP forms applied to soil and the mechanisms governing their mobilization/acquisition for crop plants.

The purpose of this review is to (1) highlight the main mechanisms involved in the potential mobilization of OP from organic inputs and soil in the soil-plant system and (2) to develop the emerging strategies in agroecology which can be adopted to improve the P availability in cropping systems.

Amount and characteristics of OP in soil and organic inputs

Phosphorus in soil comes from both pedogenic and anthropogenic sources, the majority of P being introduced as mineral fertilizers [START_REF] Fuentes | Chapter 16 Assessment of phosphorus bioavailability from organic wastes in soil[END_REF] or organic residues [START_REF] Scherer | Phosphorus fractions and phosphorus delivery potential of a luvisol derived from loess amended with organic materials[END_REF].

In addition to IP, soil OP are an important P pool (Monbet et al., 2009), especially in soils treated with organic inputs (Ruttenberg and Sulak, 2011). Studies which quantify OP in organic inputs and soils report different values about the amount of OP in soils, ranging from 20 to 90% of the total P pool in soils and sediments (Anderson, 1980;Anderson et al., 1974;[START_REF] Dalai | Soil Organic Phosphorus[END_REF]Hu et al., 2020;Turner et al., 2002a). A random-effects meta-analysis performed by Darch et al. (Darch et al., 2014) based on different studies showed that contribution of IP and OP to total P varied significantly in organic input or soil (Tables 5 ,6 , 7 and 8): in organic input, the contribution of IP was found to be 5200 mg.kg -1 against nearly 4000 mg.kg -1 for the OP pools. This revealed that OP is as important in amount as IP in soil and organic inputs. The amount of IHP the major forms of OP reaches 1325 mg.kg -1 in organic inputs, one order of magnitude higher than in soil (269 mg.kg -1 ). Moreover, the percentage contribution of IHP to total OP varied across the sample types, with soil (40%) > organic inputs (30%). This agrees with the idea that IHP is preferentially stabilized in soil compared with other OP forms due to its relative recalcitrance (Turner et al., 2002b), caused by its strong binding to the soil (Ganta et al., 2019). Further 31 P NMR studies have shown that the pool of labile monoester-P compounds was the largest pool of OP [START_REF] Granger | Towards a holistic classification of diffuse agricultural water pollution from intensively managed grasslands on heavy soils[END_REF][START_REF] Ignatiades | A review on toxic and harmful algae in Greek coastal waters (E. Mediterranean Sea)[END_REF][START_REF] Withers | Stewardship to tackle global phosphorus inefficiency: The case of Europe[END_REF] and that phosphonates were the weakest and generally less quantified group [START_REF] Jarosch | Characterisation of soil organic phosphorus in NaOH-EDTA extracts: A comparison of 31P NMR spectroscopy and enzyme addition assays[END_REF][START_REF] Zhu | Bioavailability and preservation of organic phosphorus in lake sediments: Insights from enzymatic hydrolysis and 31P nuclear magnetic resonance[END_REF]. Most individual studies that characterize OP in the environment show that total IP and OP vary with the characteristics of the organic inputs or soil types or properties, with IP being more important than OP, but remaining very close in some samples (Tables 5 and6). In soils, P forms and amounts vary with soil type (Turner et al., 2003), land use, and fertilizer history [START_REF] Guggenberger | Land-use and fertilization effects on P forms in two European soils: resin extraction and 31P-NMR analysis[END_REF]. Given these large pools of OP in soil and fertilizer and the range of values (20-90% of total P) generally carried over in soils and sediments (Anderson, 1980;Hu et al., 2020), it is pivotal to consider OP dynamics along with IP in order to improve P cycles in agroecosystems.

Current knowledge has revealed that OP is as equally important in amount as IP. However, most research on the fate of organic inputs applied to the soil has focused on the dynamics of IP, while the fate of OP has been neglected until now, and there remains a lack of knowledge on its contribution to plant nutrition. Thus, there is a need to define standard methods that can help guide OP research and a sustainable approach that could be taken to improve soil OP cycling. This can be achieved through a multi-pronged combination of sustainable farming systems, genetically-improved plants, beneficial biota (biofertilizers).

Organic phosphorus dynamics in rhizosphere

Rhizosphere microbiomes and roots traits involved in P acquisition are known to affect the dynamics of OP in the rhizosphere and, ultimately, its availability to the plant (Figure 6). Although studies showed that OP can be significantly depleted within the rhizosphere [START_REF] Chen | Effects of plant species on microbial biomass phosphorus and phosphatase activity in a range of grassland soils[END_REF][START_REF] Gahoonia | Root traits as tools for creating phosphorus efficient crop varieties[END_REF], the interaction between rhizosphere microbiomes in the rhizosphere, root traits, and their contribution to OP release to plants are not fully elucidated so far [START_REF] Jakobsen | Rhizosphere Microorganisms and Plant Phosphorus Uptake[END_REF]. Here we summarize and discuss the role of soil microbial processes, root mechanisms and their interactions in the fate of OP forms in the organic input-soil-plant system. (1) and (2) are the plants P mining and foraging strategies respectively (see Section 3.2 for more details); (3) P-mobilizing crop species improve OP utilization for non-P-mobilizing species, (4) refers to the microorganisms coming from organic input.

Indeed, organic inputs involve the addition of carbon sources and often even contain their own microbiota. System modified from [START_REF] Hinsinger | Impact of roots, microorganisms and microfauna on the fate of soil phosphorus in the rhizosphere[END_REF] and (Sulieman and Mühling, 2021).

Soil microbial processes involved in OP mobilization

In organic inputs-amended soils and P-depleted environments, there is generally a proliferation of free rhizosphere microbiome and symbiotic associations with mycorrhizal fungi which have the potential to mobilize and mineralize different forms of available and unavailable OP (Sulieman and Mühling, 2021;[START_REF] Tian | Roles of Phosphate Solubilizing Microorganisms from Managing Soil Phosphorus Deficiency to Mediating Biogeochemical P Cycle[END_REF] (Table 9). Phyla involved in OP mineralization include the dominant phyla Proteobacteria followed by Acidobacteria and Actinobacteria (Annaheim et al., 2010;[START_REF] Gaiero | Validating novel oligonucleotide primers targeting three classes of bacterial non-specific acid phosphatase genes in grassland soils[END_REF]. The order Xanthomonadales of Xanthomonadaceae family is known to contain several OP mineralizing genes. To obtain P from OP compounds, Streptomyces uses an extracellular alkaline phosphatase encoded by the phoA gene. Other alkaline phosphatase genes, phoD and the phoC, were initially described in the Streptomyces avermitilis and Streptomyces coelicolor genomes, respectively [START_REF] Tian | Roles of Phosphate Solubilizing Microorganisms from Managing Soil Phosphorus Deficiency to Mediating Biogeochemical P Cycle[END_REF]. Stenotrophomonas spp. has been shown to be an important contributors of OP solubilization. Controlled experiments using plant inoculated with rhizosphere microbiome provided further evidence for microbially mediated OP bioavailability to plants. Richardson et al.(Richardson et al., 2011) showed that both grasses and legumes exhibited an improved ability to utilize IHP-P when inoculated with bacteria isolates with high phytase activity. Bacillus spp. and Trichoderma spp. may be able to increase the use of IHP as P source by plants due to the production of organic anions and phytase (Garcia-Lopez et al., 2015;[START_REF] Garcia-Lopez | Effect of Bacillus subtilis on phosphorus uptake by cucumber as affected by iron oxides and the solubility of the phosphorus source[END_REF]. Nevertheless, there are little evidences on how these rhizosphere microbiomes may act in the presence of soil minerals that can immobilize both OP and hydrolytic enzymes. Soil minerals such as Fe, Al oxides, and clay minerals are known to considerably reduced the efficiency of applied P. It is assumed that adsorbed OP on Fe and Al oxides are protected from enzymatic hydrolysis leading to its accumulation in soil (Stutter et al., 2015) and its decreased use as P source by plants. However, García-López et al. (2020) recently showed that Bacillus subtilis improved hydrolytic activity of IHP even in the presence of high Fe oxide concentration. This led the conclusion that rhizosphere microbiome could contributes to an increased hydrolyzing capacity in soil with high OP sorption capacity (Table 9). Current work is insufficient to understand the extent to which rhizosphere microbiomes are actually able to access sorbed forms of P. Future work must be conducted by inoculating microorganisms with sorbed P complexes on major soil minerals such as goethite, gibssite, and major clays under laboratory conditions and even further in the field. Thus, as most of the legacy P is poorly available to plants, especially the important part corresponding to OP pools [START_REF] Stutter | Recovering Phosphorus from Soil: A Root Solution?[END_REF], the impact of rhizosphere microbiomes in mobilizing this legacy P is a crucial issue to reduce the dependence on mined P fertilizers (Giles et al., 2011). Moreover, it is important to keep in mind that hydrolysis of adsorbed OP depends to some extent on the release of organic anions or citrate by plant and rhizosphere microbiomes; this promotes the desorption and dissolution of OP making it available for hydrolysis [START_REF] Celi | Role of crystalline iron oxides on stabilization of inositol phosphates in soil[END_REF].

Different enzymes released by the rhizosphere microbiome that are involved in OP hydrolysis, such as phytases and alkaline and acid phosphatases, act specifically on particular OP substrates (Annaheim et al., 2010). Several studies using soil-specific enzyme additions have been published over the past decades (George et al., 2008;Turner et al., 2002b). Their results show that OP mineralization would be explained by the specificity of enzymatic activities on OP forms. For example, Scyllo-IHP was found to be most resistant to phytase activity [START_REF] Cosgrove | The chemical nature of soil organic phosphorus. I. Inositol phosphates[END_REF] while IHP hydrolysis has been reported for bacterial acid phosphomonoesterases [START_REF] Lung | Phytase activity in tobacco (Nicotiana tabacum) root exudates is exhibited by a purple acid phosphatase[END_REF]. Other phytases from Aspergillus spp. (EC 3.1.3.8) have also been reported to hydrolyze IHP, simple monoesters (G6P, GLY), and phosphoanhydrides, but their ability to hydrolyze diester bonds in nucleic acids [START_REF] George | Differential interaction of Aspergillus niger and Peniophora lycii phytases with soil particles affects the hydrolysis of inositol phosphates[END_REF]Turner et al., 2002b) is contradicted by to the result of various studies (Annaheim et al., 2013).

Monoesterase enzymes have been found to hydrolyze diester phosphates. However, the release of phosphates from DNA is generally very low. This could be because monoesterases hydrolyze only the 5' and 3' phosphate residues of DNA (Annaheim et al., 2010), while the other phosphate groups are not accessible [START_REF] George | Differential interaction of Aspergillus niger and Peniophora lycii phytases with soil particles affects the hydrolysis of inositol phosphates[END_REF]. It has previously been shown that acid and alkaline phosphatase and phytase are not active on nucleotide pyrophosphate that contains nucleotide pyrophosphate bonds, nor on RNA and DNA that contain phosphodiester bonds [START_REF] He | Enzymatic Characterization of Organic Phosphorus in Animal Manure[END_REF]. In organic input, nucleotide pyrophosphatase, which hydrolyzes nucleotide pyrophosphate to nicotinamide mononucleotide and AMP, and a P1 nuclease, which cleaves RNA and DNA to produce 5-phosphomonoesters, were used to access the presence of OP forms. The result showed that both enzymes (nucleotide pyrophosphatase and P1 nuclease) acted only on their own substrate (nucleotide pyrophosphate, RNA and DNA). Therefore, it has been suggested that these enzymes could be used to release specific forms of phosphorus when present in the soil [START_REF] He | Enzymatic Characterization of Organic Phosphorus in Animal Manure[END_REF].

Soil properties may influence the conversion of OP into IP by rhizosphere microbiome. Among the soil properties, soil pH is an especially important factor that affects the efficacy and biochemical availability of enzymes that hydrolyze the OP forms in the soil. For instance, at a pH of 7.5, Aspergillus niger phytases remained in solution, but at a pH of 5.5, it is unavailable [START_REF] George | Differential interaction of Aspergillus niger and Peniophora lycii phytases with soil particles affects the hydrolysis of inositol phosphates[END_REF]. But, optimal pH varies according to the soil microorganism specie and the associated plant. Fungal phytases have a pH between 4.5 and 6.5, such as Aspergillus fumigatus, where 80% of the activity takes place [START_REF] Wyss | Biochemical Characterization of Fungal Phytases (myo-Inositol Hexakisphosphate Phosphohydrolases): Catalytic Properties[END_REF]. Species such as Rhizoctonia sp. and Fusarium verticillioides can produce phytases at optimal pH of 4.0 and 5.0, respectively [START_REF] Marlida | Isolation, characterization and production of phytase from endophytic fungus its application for feed[END_REF], while in bacterial phytases the maximum activity was observed at an optimal pH of 6.0-8.0, as in Bacillus sp. [START_REF] Kim | Cloning of the thermostable phytase gene ( phy ) from Bacillus sp. DS11 and its overexpression in Escherichia coli[END_REF]. Most of the phytases are acidic and have an optimal pH between 4.5 and 6.0 [START_REF] Konietzny | Molecular and catalytic properties of phytate-degrading enzymes (phytases)[END_REF], whereas alkaline phytases in legume seeds [START_REF] Scott | Alkaline Phytase Activity in Nonionic Detergent Extracts of Legume Seeds[END_REF], lily pollen and cattail pollen have been reported to have an optimal pH of 8.0 [START_REF] Azeem | Microbial phytase activity and their role in organic P mineralization[END_REF]. For example, at pH 7.5, phytases from Aspergillus niger remain available in solution, but at pH 5.5 they are not available [START_REF] George | Differential interaction of Aspergillus niger and Peniophora lycii phytases with soil particles affects the hydrolysis of inositol phosphates[END_REF]. It is clear that phosphatases produced by rhizosphere microbiomes are more sensitive to pH. This pH dependence would even be superior to that of plant phosphatases. However, the optimal pH for OP mobilization varies among rhizosphere microbiome species. In addition, it is also important to understand how microorganisms could facilitate P mobilization from organic inputs or soil organic matter within a given pH range. Consequently, we conclude that the determination of the optimal pH for OP mobilization by microbes and root traits requires careful judgment in future research.

In addition to pH, soil temperature has a strong effect on OP availability even though studies showed divergent results on the influence of temperature on P solubilization by microbes. White et al. [START_REF] White | Microbial solubilization and immobilization of toxic metals: key biogeochemical processes for treatment of contamination[END_REF] found 20-25°C to be the optimal temperature for maximum microbial solubilization of P while 28°C was reported by [START_REF] Chauhan | Global Warming and Its Possible Impact on Agriculture in India[END_REF] and [START_REF] Alori | Microbial Phosphorus Solubilization and Its Potential for Use in Sustainable Agriculture[END_REF].

In addition, others recorded 30 °C as the best temperature for solubilization and mineralization of OP [START_REF] Fasim | Solubilization of zinc salts by a bacterium isolated from the air environment of a tannery[END_REF][START_REF] Kim | Cloning of the thermostable phytase gene ( phy ) from Bacillus sp. DS11 and its overexpression in Escherichia coli[END_REF]. [START_REF] Nautiyal | Stress induced phosphate solubilization in bacteria isolated from alkaline soils[END_REF] reported solubilization and hydrolysis of P at an extreme temperature of 45°C in desert soil while Johri et al. [START_REF] Johri | Fungal association and utilization of phosphate by plants: success, limitations, and future prospects[END_REF] reported a low temperature of 10 °C. The optimum temperature for phytate-degrading enzymes ranges from 35 to 77°C. In general, plant phytases, such as those from cereals, show maximum activity at lower temperatures than microbial phytases [START_REF] Konietzny | Molecular and catalytic properties of phytate-degrading enzymes (phytases)[END_REF]. The phytase from Fusarium verticillioides showed an optimal temperature of 50°C and stability up to 60°C [START_REF] Azeem | Microbial phytase activity and their role in organic P mineralization[END_REF].

The optimal temperature for phytase activity towards magnesium phytate (Mg-IHP) has been reported

to reach 40°C without and 50°C with 5 mM Ca 2+ [START_REF] Park | Degradation of Phytate Pentamagnesium Salt by Bacillus sp. T4 Phytase as a Potential Eco-friendly Feed Additive[END_REF]. Most plant phytases have an optimal temperature of 45-60°C, as reported by [START_REF] Johnson | Heterologous expression and functional characterization of a plant alkaline phytase in Pichia pastoris[END_REF]. The lowest temperature has been reported to be 10°C [START_REF] Johri | Fungal association and utilization of phosphate by plants: success, limitations, and future prospects[END_REF]. However, it is generally assumed that higher temperature (> 30°C) has a better effect on OP solubilization and availability as shown by the higher OP solubilization by Bacillus megaterium at 36°C than at 21°C. Like pH, phosphatases produced by rhizosphere microbiomes are thermostable. Therefore, changes in the interactions between microbes and root traits as a result of temperature variations and how this could affect OP mobilization processes must be considered in the soil-plant system. Furthermore, understanding the optimal activity of microorganisms as a function of soil temperature is an important challenge for improving biofertilizer management practices and their positive effects on OP hydrolysis and P availability. However, given the challenge of controlling soil temperature, it is nonetheless possible to identify the dates and seasons to apply the biofertilizer to maximize its effect. The effectiveness of microbial enzymatic activity is also influenced by different cations and other constituents in the soil solution. Model studies have shown that three classes of phytases, histidine acid phosphatases, β-propellant phytases, and purple acid phosphatases, would be unable to hydrolyze Al 3+ , Fe 2+ , Fe 3+ , Cu 2+ salts of IHP, but were able to hydrolyze Ca 2+ , Mg 2+ , and Mn 2+ salts (Lim et al., 2007;[START_REF] Tang | Hydrolysis of precipitated phytate by three distinct families of phytases[END_REF]. This implies that P mobilization will depend on the nature of the cation that precipitates OP. Thus, the accessibility of precipitated OP by enzymes and its mobilization for plants will be largely different depending on the nature and concentration of electrolytes in the soil.

In summary, the hydrolysis of OP and its release by enzymatic activity is generally affected by the biochemical nature of OP and its ability to interact with soil properties and rhizosphere microbiomes.

A wide variety of bacteria, fungi, and endophytes can therefore solubilize OP through the production of organic acids [START_REF] Adhya | Microbial mobilization of soil phosphorus and sustainable P management in agricultural soils[END_REF]. This solubilization is very important because most forms of OP are high molecular weight compounds that are generally resistant to chemical hydrolysis. However, the mechanisms associated with the transformation of OP to IP are poorly understood, and further work is needed, especially under field conditions. In most studies, the experimental conditions have suppressed interactions between system components. Therefore, these studies generally only indicate what is possible, but they do not necessarily indicate what is likely (Lung and Lim, 2006;[START_REF] Zimmermann | Engineering the root-soil interface via targeted expression of a synthetic phytase gene in trichoblasts[END_REF]. Indeed, knowledge of OP transformations must be a prerequisite for understanding the potential contribution of lesser-known forms of OP in the organic input-soil-plant system. In any case, it is clear that OP mineralization occurs in the rhizosphere and could contribute significantly to the requirements for plant growth. Factors affecting rhizosphere microbiome are likely to influence the lability and stability of their enzymes. Some enzymes become stable through interactions with soil minerals and humic substances, and retain some enzyme activity [START_REF] Allison | Changes in enzyme activities and soil microbial community composition along carbon and nutrient gradients at the Franz Josef chronosequence, New Zealand[END_REF]. In general, microbial activity is affected by biological (the amount and type of substrate, concentration of enzyme, ect.) and physicochemical processes (interactions with soil constituents pH, temperature, ect.). The former cause changes in enzyme production rates and microbial community composition, while the latter cause changes in adsorption/desorption reactions, substrate diffusion and enzyme degradation rates (Wallenstein et al., 2009). Critical factors affecting microbes and their enzyme activities include the amount and type of OP [START_REF] Fitriatin | The Influence of organic phosphorous substrate on phosphatase activity of soil microbes[END_REF], interactions with soil constituents, pH, temperature, and concentration of enzyme and product [START_REF] Sarapatka | Phosphatase activity of eutric cambisols (Uppland, Sweden) in relation to soil properties and farming systems[END_REF]. In addition, because OP adsorbs rapidly and strongly on-to soil particles, the binding processes involved also play a crucial role in the activity of rhizosphere microbiomes [START_REF] Fierer | Embracing the unknown: disentangling the complexities of the soil microbiome[END_REF][START_REF] Qu | Soil Enzyme Activity and Microbial Metabolic Function Diversity in Soda Saline-Alkali Rice Paddy Fields of Northeast China[END_REF]. To date, there are relatively few studies that explore the enzymatic hydrolysis of adsorbed OP. It has been reported that mineral surfaces protect the majority of adsorbed phosphate esters from enzymatic hydrolysis, but whether this is a general finding remains open [START_REF] Jones | Plant and mycorrhizal regulation of rhizodeposition[END_REF]. Furthermore, the mechanism of this process is largely unknown in the case where the enzyme is able to access the adsorbed OP forms. The results of Olsson et al. [START_REF] Olsson | Enzymatic Hydrolysis of Organic Phosphates Adsorbed on Mineral Surfaces[END_REF] on the hydrolysis of G1P on α-FeOOH surfaces showed the role of interactions at mineral surfaces with respect to the stabilization of OP molecules in soils [START_REF] Bian | Arsenic distribution and geological factors in the western Jilin province, China[END_REF]. These authors provided a mechanistic explanation of how P can be mobilized via enzymatic activity despite strong interactions with soil minerals. This sheds light on previous results showing that microbial stimulation and the resulting enzymatic activity can mobilize adsorbed OP from soil minerals [START_REF] Tang | Hydrolysis of precipitated phytate by three distinct families of phytases[END_REF].

However, a question is whether the enzyme acts only on the soluble fraction that is reconstituted by desorption of the substrate or whether the hydrolysis reaction occurs at the interface between the aqueous solution and solid particles. We therefore suggest future studies on these issues to understand better the effect of rhizosphere microbiomes on OP dynamics.

Apart of the rhizosphere microbiome, organic inputs-derived microorganisms also play a major role in the mobilization of OP. Organic inputs imply the addition of carbon sources and often even contain their own microbiota, like an inoculation of microbes and this is a very important issue that needs more study. Amendment of organic inputs generally increases the diversity of rhizosphere microbiomes and their enzymatic activities in the soil [START_REF] Francioli | Mineral vs. Organic Amendments: Microbial Community Structure, Activity and Abundance of Agriculturally Relevant Microbes Are Driven by Long-Term Fertilization Strategies[END_REF]. These positive reactions highlight the role of organic inputs-derived microorganisms in OP availability and on the other hand their high content of organic matter [START_REF] Li | Surface Speciation of Phosphate on Boehmite (γ-AlOOH) Determined from NMR Spectroscopy[END_REF] which is the main substrate of most microorganisms [START_REF] Li | Characterization of Phosphorus in Animal Manures Collected from Three (Dairy, Swine, and Broiler) Farms in China[END_REF]. However, complex questions remain about how the addition of organic inputs alters the soil microbial community and especially how this relates to soil OP mineralization. Then to successfully manage organic inputs, there is a need to develop a consistent procedure to quantitatively compare the potential of these different microorganisms to release orthophosphate from different sources of OP [START_REF] Li | Characterization of Phosphorus in Animal Manures Collected from Three (Dairy, Swine, and Broiler) Farms in China[END_REF]. As organic input-soil-plant continuum consists of various forms of OP with different chemical properties, their solubilization and hydrolysis rates would be strongly related to the diversity of soil microbial communities. Therefore, it is crucial to develop and utilize more advanced approaches to support the roles soil microbes especially the phosphate solubilizing microorganismsderived enzymes in releasing free IP from OP forms in the soil [START_REF] Alori | Microbial Phosphorus Solubilization and Its Potential for Use in Sustainable Agriculture[END_REF][START_REF] Liang | Novel phosphatesolubilizing bacteria enhance soil phosphorus cycling following ecological restoration of land degraded by mining[END_REF].

In sum, the main microbial processes involved in P dynamics that are synthesized and highlighted in this section, and the factors that influence them, greatly affect soil P mobilization processes. They could therefore, if well understood, contribute to increase the P use efficiency of organic wastes and those accumulated in agricultural soils. Furthermore, it is known that plant roots inoculated with commercial microorganisms can express synergistic effects to solubilize IP in the soil. In contrast, little is known about their effect on OP pools. Therefore, further research is needed to evaluate the application and efficacy of commercial microorganisms on various crops with contrasting root traits and fertilized with different P sources under field conditions.

Current cropping models often focus on understanding competition for light and the effects of N or P fertilization, but do not consider interactions with the rhizosphere microbiome and how it affects soil OP forms. Thus, the development of cropping models that consider more OP dynamics is needed to determine the efficiency of OP use in multi-species cropping systems and to manage P sustainably in the agroecosystem. Furthermore, it is important to note that current decision support tools do not consider OP sportion, its mineralization kinetics, and the effect of root trait and rhizosphere microbiome interactions on its dynamics. Therefore, for future research aimed at assisting farmers in organic input management, these parameters that govern OP dynamics, should be further studied and integrated into decision support tools. This will not only improve the decision support tools but also make them more focused on OP mobilization in the organic input-soil-plant system.

Another important factor is the effect of rhizosphere microbial populations on OP mineralization. Some studies have shown that soils taken from the rhizosphere slowed the sorption of phytate or phytase into the rhizosphere, suggesting that rhizosphere soils alter the adsorption of phytase and thus the release of orthophosphate from soils. This is an important observation because OP dynamics are altered in the rhizosphere, so it is possible that OP from organic inputs is more available around plant roots. Therefore, we strongly suggest that, along with the mobilization process by soil microbes, root mechanisms/traits can be exploited to facilitate soil OP mobilization at the field scale.

The hydrolysis of OP and its release by enzymatic activity is influenced by the biochemical nature of OP and its ability to interact with soil properties and rhizosphere microbiomes. However, current work is insufficient to understand the extent to which rhizosphere microbiomes are actually able to access sorbed forms of P from both soil constituents and organic matter. Furthermore, the potential of microbes to mobilize OP has been conducted on cultivable microbes, yet most root-associated rhizosphere microbiomes are not cultivable. We recommend future investigations to screen rhizosphere bacteria in the presence of different forms of OP and different soil properties, to identify those that are effective in OP mobilization.

Root mechanisms involved in the fate of OP forms

The contribution of plants to OP availability is known since many decades. Most plants have developed strategies to increase P acquisition in P-deficient soil or to specifically access different forms of OP and IP in the soil (Simpson et al., 2011). These strategies cover a wide range of morphological, architectural and physiological traits (Robles-Aguilar et al., 2019). In general, these traits could be categorized into three types of P acquisition strategies: foraging, mining and collective microbial-root strategy (Figure 6 and Table 9).

The plant P-foraging strategy is the acquisition of P in the soil solution through morphological and architectural traits by maximizing soil exploration. Through this strategy, plants can induce a diffusion gradient which in turn would favour the desorption process of the different adsorbed OP forms [START_REF] Fang | Impact of low-molecular weight organic acids on selenite immobilization by goethite: Understanding a competitive-synergistic coupling effect and speciation transformation[END_REF]White and Hammond, 2008). Phosphorus foraging strategy would also improve the efficiency of P uptake by slowing the rate at which OP moves from the free or moderately adsorbed form to the strongly adsorbed form on soil compounds (Simpson et al., 2011). Foraging strategy involves morphological traits such as specific root length, diameter and radius, and architectural traits including root length density, root biomass, root hairs, and the formation of clustered roots or arbuscular mycorrhizal symbioses that allow plants to increase their foraging capacity (Haling et al., 2018). These traits alter the C cost of soil exploration by regulating the extent of competition within and between root systems [START_REF] Ge | The importance of root gravitropism for inter-root competition and phosphorus acquisition efficiency: results from a geometric simulation model[END_REF]Rubio et al., 2003). Among morphological trait, root radius is considered important in the efficiency of P use. Plants with finer/thinner roots favoured the exploration and contact of a greater volume of soil per unit root area. Gahoonia et Nielsen [START_REF] Gahoonia | Root traits as tools for creating phosphorus efficient crop varieties[END_REF] reported that plant species with finer roots may be more effective in mobilizing OP and absorption of IP from the soil. Very recently, trade-offs between thicker and thinner roots have been observed by Honvault et al. (Honvault et al., 2020). Thicker roots are reported to have greater carboxylate release and phosphatase activity in the rhizosphere, which are involved in the desorption and mineralization of OP (Honvault et al., 2020). In contrast, the thinner exhibit the morphological traits (foraging) that favoured the exploration and contact of a larger volume of soil to permit P mobilization process (Hammond et al., 2009;Lynch, 2015). These observations are consistent with other results showing that species with finer fibrous roots express higher levels of morphological traits to access more OP in the soil (Haling et al., 2018;Lambers et al., 2006;Wen et al., 2019). However, since fine roots (root hairs, small root radius) tend to renew faster than large roots [START_REF] Ge | The importance of root gravitropism for inter-root competition and phosphorus acquisition efficiency: results from a geometric simulation model[END_REF], the cost of C to produce fine roots could be higher, since they would also need to be replaced more frequently (Rubio et al., 2003). In addition to root radus, the formation of root groups such as the proteoid and dauciform root groups commonly found in plant species belonging to the families Proteinaceae and Fabaceae (Lambers et al., 2006) and others is very strongly related to the dynamics of OP in soil. These roots cover a very dense mat of root hairs and also specialize in the efficient synthesis and secretion of citrate and malate (organic anions) and phosphatases, which help solubilize insoluble OP resources and hydrolyze OP for plant uptake [START_REF] Pearse | Triticum aestivum shows a greater biomass response to a supply of aluminium phosphate than Lupinus albus, despite releasing fewer carboxylates into the rhizosphere[END_REF]. Various effects of root growth and variation in root hair length on OP dynamics and contribution to P uptake have been reported in several species including maize, wheat, barley, beans, soybean and white clover [START_REF] Khare | XANES Determination of Adsorbed Phosphate Distribution between Ferrihydrite and Boehmite in Mixtures[END_REF]Zhu et al., 2005). Higher root length density in the upper soil layers was shown to be the most important root trait of wheat for OP mobilisation in response to organic input input (Lamont, 2003). Moreover, the variation in root growth angle and root hairs might have a significant impact on the total mobilisation of P in the soil [START_REF] Trachsel | Shovelomics: high throughput phenotyping of maize (Zea mays L.) root architecture in the field[END_REF]. In closely related maize genotypes, the effects of root growth and root hair length variation reportedly led to a 100% increase in total mobilized P and in other genotypes to as much as a 600% increase in P mobilization (Zhu et al., 2005). Such increases are due to the fact that root growth maximizes soil exploration and can induce a diffusion gradient and modify soil properties to promote P desorption. Root hairs are smaller in diameter than roots and grow perpendicular to the root axis and can form up to 77% of the root surface [START_REF] Fort | Plant ecological indicator values as predictors of fine-root trait variations[END_REF] of soil/field crops [START_REF] Parker | Genetic Interactions during Root Hair Morphogenesis in Arabidopsis[END_REF][START_REF] Raghothama | Phosphate Acquisition[END_REF].

The presence of root hairs can be very important for the effectiveness of OP mobilization through a considerable increase of root area in the soil. It has been reported that root hairs can contribute up to 70% of OP uptake [START_REF] Gahoonia | Root traits as tools for creating phosphorus efficient crop varieties[END_REF][START_REF] Smith | The phosphate uptake mechanism[END_REF]. Root hair length and density are highly controlled by P bioavailability. Geometric modeling indicates that root hair responses to P availability interact synergistically to enhance OP and IP acquisition (Ma et al., 2018). Root hairs also aid in the dispersal of root exudates such as organic acids into the rhizosphere, which improve OP bioavailability in many soils (Ryan et al., 2001). Root morphological traits reveal a much more significant influence on OP acquisition generally in winter wheat genotypes than at biochemical transformation by acid phosphatases (Nobile et al., 2019;[START_REF] Khare | XANES Determination of Adsorbed Phosphate Distribution between Ferrihydrite and Boehmite in Mixtures[END_REF]. These biochemical and morphological changes can vary considerably between and within plant species (Sulieman and Mühling, 2021;[START_REF] Zogli | Physiological and Molecular Mechanisms and Adaptation Strategies in Soybean (Glycine max) Under Phosphate Deficiency[END_REF]. Admittedly, the potential ability of plants root traits to utilize poorly available OP sources is greatly determined by its genetic makeup.

The plant P mining strategy, is the acquisition of P in the soil solution through physiological traits that are released into the soil from the roots, including carbohydrates, organic and amino acids, phenolic compounds, proteins, fatty acids, sterols, enzymes, polysaccharides and phospholipids (Guppy et al., 2005;Weisskopf et al., 2006). Among these compounds, carboxylic acids, PME activity, phenolic and mucilage compounds, and protons are the main physiological traits involved in P mining strategies for OP mobilization [START_REF] Carminati | Do roots mind the gap?[END_REF]. Through this strategy, plants increase the turnover of poorly available OP pools (Lambers et al., 2006;Richardson, 2005) by desorption, solubilization and mineralization process. Before any hydrolysis process by the enzymes, OP, if not free, must first be desorbed or dissociated from soil minerals or organic matter. The secretion of organic acids by Pmobilizing species improves the availability of OP forms by promoting their desorption from soil constituents to the soil solution in which they are subsequently mineralized by phosphatases (Li et al., 2004). Organic acids are generally expected to be strongly linked to OP mobilization in the soil-plant system (Neumann et al., 1999). Plant roots have the ability to produce organic acids, particularly shortchain organic acids such as lactate, acetate, oxalate, succinate, fumarate, malate, citrate, isocitrate, and aconitate which can mobilize both OP and IP (Damon et al., 2014). Among the organic acids, malic and citric acids are the most widespread and abundant detected in root exudates [START_REF] Aziz | Categorization of brassica cultivars for phosphorus acquisition from phosphate rock on basis of growth and ionic parameters[END_REF]. Given the highest affinities between OP forms and soil components, chelation between organic acids in root exudates and soil constituents would be the main mechanism for OP solubilization by organic acids in soil [START_REF] Oburger | Phosphorus saturation and pH differentially regulate the efficiency of organic acid anion-mediated P solubilization mechanisms in soil[END_REF]. Citrate has been shown to chelate Fe and Al oxyhydroxide and Mn and Cacarbonates, which could actively displace adsorbed OP towards free forms [START_REF] Ryan | Significance of Iron Oxides and Calcium Carbonate Particle Size in Phosphate Sorption by Calcareous Soils[END_REF]. Low molecular weight organic acids generally carry one or more negative charges. By complexolysis, negatively charged organic acids are able to release OP from insoluble forms of OP. These reactions lead to the solubilization of insoluble forms of OP such as Ca-OP, Na-OP etc. [START_REF] Courty | Temporal and functional pattern of secreted enzyme activities in an ectomycorrhizal community[END_REF]. The impact of direct chelation in the solubilization of OP by citrate exudation has for instance been demonstrated in rice [START_REF] Kirk | Phosphate solubilization by organic anion excretion from rice growing in aerobic soil: rates of excretion and decomposition, effects on rhizosphere pH and effects on phosphate solubility and uptake[END_REF]. In general, citrate and oxalate have a higher potential for mobilization of OP compared to other organic anions (Neumann et al., 1999;Ryan et al., 2001). After OP desobed from soil minerals by organic acids, the improvement of phosphatase and phytase activity released by roots can contribute to it efficiency use by plant (Hallama et al., 2019;[START_REF] Hayes | The Growth and Phosphorus Utilisation of Plants in Sterile Media When Supplied with Inositol Hexaphosphate, Glucose 1-Phosphate or Inorganic Phosphate[END_REF].

Chickpea, which appears to produce both phosphomonoesterases and diesterases, is thought to improve it P nutrition, probably through mining and mineralization of OP forms in soil (Darch et al., 2018;[START_REF] Pang | The carboxylate-releasing phosphorus-mobilizing strategy can be proxied by foliar manganese concentration in a large set of chickpea germplasm under low phosphorus supply[END_REF]. Various studies have demonstrated that plants have limited ability to access P in the form of IHP (the main form of OP) due to its low availability in soil solution and low level of extracellular phosphatase or phytase [START_REF] George | Differential interaction of Aspergillus niger and Peniophora lycii phytases with soil particles affects the hydrolysis of inositol phosphates[END_REF]Richardson and Simpson, 2011). It has also been shown that wheat and many other species are able to utilize P from G6P, GLY and phosphodiesters (DNA and RNA) due the mining capacity, but are limited to acquiring P directly from IHP, although it is an abundant in many soils (George et al., 2008). This suggests that the biological importance of the different forms of OP will be driven by their turnover rates. Therefore, it was considered that plants with optimal mining strategies for phytase release could potentially be used to improve the efficiency of inositol phosphate mobilization. The challenges are to understand the functioning of root-derived phytase activities on OP forms, and the chemical nature, soil properties, and root traits of crop species, to increase OP desorption and hydrolysis.

The collective microbial-root strategy refers to the investment of resources by plants to interact with the microbial community to access OP in soil. Many plants have developed a symbiotic association with vesicular arbuscular mycorrhizal fungi (AMF) that grow out from the root into the surrounding soil, extending the capacity of the root to mineralize OP and take up IP in soil solution [START_REF] Tinker | The role of microorganisms in mediating and facilitating the uptake of plant nutrients from soil[END_REF].

The association of roots with arbuscular mycorrhizae is thought to be much more related to the mobilization of total P than root hairs and root length activity [START_REF] Gashaw Deressa | Contribution of roots and hyphae to phosphorus uptake of mycorrhizal onion ( Allium cepa L.)-A mechanistic modeling approach[END_REF]. The symbiotic association of plant roots with mycorrhizae is reported to extend further from the roots than root hairs, and is also active in areas where P forms are adsorbed onto soil components [START_REF] Graham | Host genotype and the formation and function of VA mycorrhizae[END_REF][START_REF] Sattelmacher | Factors that contribute to genetic variation for nutrient efficiency of crop plants[END_REF]. A significant contribution of AMF to the uptake of P by plants has been reported, particularly in soils with high OP binding capacity. It is also accepted that AMF store OP in their vacuoles, which can be hydrolyzed and transported as IP in the host plant [START_REF] Smith | Physiological Interactions Between Symbionts in Vesicular-Arbuscular Mycorrhizal Plants[END_REF]. In addition, they also hydrolyze OP by releasing acid phosphatase in the soil. However, the relative contribution of root-derived extracellular phosphatases in the use of OP is still unclear, as the number and activity of bacteria and fungi are higher in the rhizosphere than in the soil in general (Richardson, 2005).

Overall, the traits of the P mining, foraging and collective microbial-root strategies are known and their indirect and sometimes even direct effects on OP dynamics/mobilization have been demonstrated (Ma et al., 2018;Nobile et al., 2019). The processes differ according to the nature of OP forms (phosphate mono or diester), the structure and function of soil microbial communities, and the physicochemical properties of the soil and climate. For instance, the availibility of IHP, G6P, GLY and phosphodiesters (DNA and RNA) as a direct effect of the P mining, foraging and collective microbialroot strategies remains unclear. Although the release of organic acids can make G6P, GLY and phosphodiesters (DNA and RNA) available to plants, it is less efficient to solubilize IHP (Gerke, 2015) probably due to it strong binding to soil. Interactions between plant traits in the mobilization of P have been studied but remain poorly understood and unconfirmed. To this end, when developing new crop varieties or cultivars, selection should be based on crops with high OP use efficiency to promote greater P availability. Thus, in future crop breeding programs, traits involved in OP use efficiency should be identified and recorded. Specifically, efficient cultivars with genes and traits that produce strong phosphatase/phytase activities should be identified for better mobilization of the major OP form (IHP).

There may also be trade-offs between physiological and morphological traits (Honvault et al., 2020;Lambers et al., 2006), These trade-offs have been examined very recently in different crop families and species (Honvault et al., 2020). Trade-offs between thicker and thinner roots were observed (Honvault et al., 2020), with thicker roots showing greater carboxylate release or phosphatase activity in the rhizosphere. Trade-offs and coordination between traits were strongly influenced by soil type. However, their effect on the availability of OP forms must still be elucidated (Wen et al., 2019). Thus, we suggest that these strategies can be exploited using combinations of species with contrasting strategies or using a single species to understand better their actual effects on OP forms in agroecosystems.

Both plant functional traits and organic input characteristics strongly interact to modulate OP dynamic. However, it is still unclear to what extent these contribute to the mobilization of sparinglyavailable OP forms. Challenges and perspectives should focus on understanding the relationships between plant functional traits, OP nature and organic input properties in order to characterize the dynamics of OP, model its fate in the soil-plant system and better understand its consequences on P availability. Further, crop models to estimate total soil OP reserves and at least its specific forms (IHP, G6P, GLY, etc.) in a multi-species cropping system can be developed based on plant traits (shoot and root morphological and chemical characteristics), including inter-and intraspecific trait variability and soil properties. This trait-based approach to modeling P mobilization can be developed and would therefore be potentially useful in different climates.

Approaches/strategies to improve OP-use efficiency 1.2.4.1 Understand and manage plant traits, root-associated microorganism and OP pool interactions to characterize P dynamics and P availability

In agroecosystems amended with organic inputs, it is pivotal to grow crops able to mobilize and release OP from both soil constituents and organic input. Several direct and innovative approaches have been identified to improve the mobilization of OP forms by plants (Table 10). These include the identification and selection of crop species/genotypes based on their functional traits (Faucon et al., 2015). This approach uses morphological, architectural [START_REF] Lynch | Root architecture and nutrient acquisition[END_REF]Nielsen et al., 1998) and physiological traits (Nielsen et al., 1998;Zhu et al., 2005;[START_REF] Zhu | The contribution of lateral rooting to phosphorus acquisition efficiency in maize (Zea mays) seedlings[END_REF], microorganisms or a combination of both to access sparingly available OP forms (Figure 6). Several plant species are presumed to be relatively efficient in OP utilization without assistance from rhizosphere microbiome. Some barley species with long root hairs (up to 1.0 mm) could easily access and mobilize twice as much OP as zita species (Prunus laurocerasus) in low P soil (Bates and Lynch, 2000). More importantly, allocating C to root hair growth would represent a minor metabolic cost to achieve greater P use efficiency (Bates and Lynch, 2000;[START_REF] Fang | Impact of low-molecular weight organic acids on selenite immobilization by goethite: Understanding a competitive-synergistic coupling effect and speciation transformation[END_REF]. Numerous plant species belonging to the family Fabaceae have been classified as efficient OP solubilizers (Schneider et al., 2019). For instance, legumes (72%) are more efficient than grain or oil crops (22%) in terms of extracellular acid phosphatase activity (Yadav andTarafdar, 2007, 2003). Compared with non-nodulated legumes, N2-fixing species possess a high level of functional plasticity to assist plants in facilitating OP mobilization [START_REF] Zogli | Physiological and Molecular Mechanisms and Adaptation Strategies in Soybean (Glycine max) Under Phosphate Deficiency[END_REF]. Since N2 fixation is highly expensive in terms of IP and energy expenditure, it is likely that this group of plants can promote OP bioavailability. A wide range of biochemical, physiological, and molecular mechanisms can give nodulating plants a superior dynamic capacity to utilize soil OP more effectively. Simultaneously, most legumes have a high potential capacity to establish double symbiosis with AMF and rhizobia [START_REF] Sulieman | Phosphorus homeostasis in legume nodules as an adaptive strategy to phosphorus deficiency[END_REF]. This tripartite symbiosis can provide an additional potential advantage that might assist in OP mobilization. Unfortunately, it is still unclear to what extent these symbiotic associations contribute to the mobilization of sparingly-available OP forms. Other approaches aim at stimulating rhizosphere microbiomes that would improve plant OP acquisition and thus meet the overall goal of reducing the amount of chemical fertilizer from non-renewable mineral rocks (Li et al., 2019;[START_REF] Strock | Reduction in Root Secondary Growth as a Strategy for Phosphorus Acquisition[END_REF]. It is therefore necessary to focus on these innovative approaches to optimise the management of organic input in the agricultural system.

Briefly, a better understanding of the impact of OP mobilization and acquisition strategies by plants, which are related to the multiple morphological and physiological traits and the interactions between them, is key in the management of OP availability. Compared to IP, the impact of these strategies in soil amended with various OP forms has received much less attention. Crop species trait might be used to increase OP mobilization, helping thereby rethink P fertilization, sustain production and recycle more OP in organic amended soil but this requires to elucidate the relationship among the various OP forms in organic inputs and root traits. In addition, understanding the trade-offs and effects of combining traits would allow us to unravel the complexity of the P form acquisition strategies and provide new knowledge for designing cultivated crop communities (i.e. multi-species crops) such as cover crops or intercrops to improve P acquisition and availability (Raven et al., 2018;Wen et al., 2019).

The strategies of P-acquisition by plants and the impact of root-associated microorganisms in P mobilization are quite well understood and are currently the focus of much research. However, it is still

unclear to what extent they may interact with organic input to mobilize the sparingly-available OP forms.

Several plant species belonging to the family Fabaceae are presumed to be relatively efficient in OP utilization without assistance from soil microorganisms. Therefore, future research should test these species under controlled conditions or at the field scale to identify specific plants that are strongly involved in to the mobilization of specific forms of OP.

Cover crops and OP availability

Cover crops offer the opportunity to improve OP recycling in agroecosystems by reducing P losses through runoff attenuation and improving P availability through P hydrolysis (Table 10), P release from crop residues, and decreased P sorption (Hallama et al., 2019;Honvault et al., 2020). As such, in soils amended with organic input with high levels of OP and/or superphosphate, several cover crop species have been effective in utilizing more of the OP and IP pool not only by promoting different root traits for soil exploration, but also developing mechanisms to release various OP species from organic input and soil [START_REF] Huang | Phosphate removal from wastewater using red mud[END_REF]Richardson et al., 2011). The use of ryegrass as a cover crop and P fertilizer applications resulted in a decrease in soil IHP stock [START_REF] Menezes-Blackburn | A Holistic Approach to Understanding the Desorption of Phosphorus in Soils[END_REF]. In addition, several cover crop species are thought to be able to significantly contribute to the desorption and redistribution of sorbed forms of P from the upper soil layer to the subsoil [START_REF] Franchini | Redistribution of phosphorus in soil through cover crop roots[END_REF].

Species such as common vetch (Vicia sativa) and radish (Raphanus sativus) are generally identified as effective for these desorption and redistribution mechanisms [START_REF] Pavinato | Organic compounds from plant extracts and their effect on soil phosphorus availability[END_REF]. For example, in a high P-fixing soil, the dynamics of various forms of P from different organic inputs were studied in the presence of five cover crop species: vetch, white lupin, forage radish, ryegrass, and black oat for 5 years in a no-till system. These species were able to mobilize labile and less labile OP and increase the proportion of IP in the soil solution. Considering the literature on cover crop species, white lupine is widely suggested to be the most efficient for extracting OP and IP forms and could be considered a Pmobilizing species, although this may depend on the characteristic of the organic input applied [START_REF] Calegari | Long-term effect of different soil management systems and winter crops on soil acidity and vertical distribution of nutrients in a Brazilian Oxisol[END_REF][START_REF] Soltangheisi | Cover Cropping May Alter Legacy Phosphorus Dynamics Under Long-Term Fertilizer Addition[END_REF]. Furthermore, though there is little information available in the literature, it is also pointed out that cover crops could specifically increase the dissolution of resistant OP associated with fulvic acid and highly resistant OP associated with humic acid [START_REF] Bowman | AN EXPLORATORY METHOD FOR FRACTIONATION OF ORGANIC PHOSPHORUS FROM GRASSLAND SOILS[END_REF][START_REF] Cui | The combined effects of cover crops and symbiotic microbes on phosphatase gene and organic phosphorus hydrolysis in subtropical orchard soils[END_REF]. Of the forms of soil OP, IHP can account for more than 70% of soil stoks because of its strong binding to soil minerals. For its more efficient mobilization, Gerke (2015), suggests that future research considering P acquisition from IHP should focus on its mobilization from the surface of soil components by root exudates of cover crop species, primarily di-and tricarboxylic acids, which can increase IHP solubility. In sum, cover crops can be an innovative technique to improve the mobilization of OP pools from the organic input-soil-plant system. However, their effects are mixed and depend on the concentration of P available in the soil and thus on the added P fertilizer [START_REF] Slazak | Soil organic phosphorus fraction in pine-oak forest stands in Northeastern Germany[END_REF]. The perspective is to examine the role of cover crops on desorption, mineralization of OP forms and consequences on P availability with a view to model their potential effect on P availability in soils amended with organic input. Studies on the impact of cover crops on OP availability are generally conducted over a short evaluation period. Thus, as observed by Calegari et al. [START_REF] Calegari | Long-term effect of different soil management systems and winter crops on soil acidity and vertical distribution of nutrients in a Brazilian Oxisol[END_REF], long-term studies are needed, as OP mobilization from applied organic input may depend on the cover crop species and their ability to desorb and redistribute fixed P. Most studies on the impact of cover crops on P dynamics are descriptive studies in which plant traits and OP forms are generally not characterized. Therefore, we suggest that future studies are needed to quantify species traits that may influence key forms of OP. This is to manage the relationship between cover crops and OP and more broadly between cover crops and organic input. The wide variability in potential contributions of OP pools in cover crop systems, their possible interactions with IP from crop residues for subsequent crop nutrition suggest a strong need to integrate soil OP dynamics into crop models in order to select cover crop traits that provide optimal utilization of OP from organic fertilization in cropping systems.

Cover crops have a wide range of P acquisition traits, and thus potentially different P acquisition strategies exploiting different P pools and probably OP pools. An outstanding question is whether P forms and soil type influence the expression of trade-offs and OP acquisition strategies in cover crops.

To answer this question, future research should measure morphological, architectural, and physiological traits of different cover crop species from various phylogenetic lineages in different contrasting agricultural soil types. This may help to characterize the relationships among traits involved in P acquisition to explore tradeoffs and the main P-acquisition strategies and their mediation by soil type.

Management of OP inputs in crop rotations

The ability of crop species to mobilize OP of organic inputs and soil constitutes an opportunity to define an OP management at the crop rotation scale (Table 10). Many Brassicaceae crop species (e.g. canola, cabbage, radish…) that produce more acid phosphatase than wheat, oats, maize, beans and chickpeas in response to P deficiency (Nobile et al., 2019;[START_REF] Wang | Phosphate and phytate adsorption and precipitation on ferrihydrite surfaces[END_REF], can benefit from the fertilization with organic inputs. Brassicaceae with different P acquisition strategies mineralize OP and improve P availability that would be beneficial to the next crop (Haling et al., 2018;Pang et al., 2010)(Figure 6).

The large differences in the efficiency of the P uptake strategy of canola, cabbage and radish on the one hand, and wheat, oats and barley on the other hand, can provide a tool to optimize the combination between the rotation crop and the organic input to be applied. In practice, since organic inputs slowly increase the soil P content available to plants after incorporation into the soil (Houben et al., 2019),

Brassicaceae crop species should be the first choice in the crop rotation to improve the P content of crops from poorly available forms of OP. For crop species such as wheat and barley that have high specific root length and relatively high carboxylate release, they could be more effective in releasing different forms of P adsorbed and/or precipitated on soil constituents, such as IHP which are very strongly adsorbed on soil. From an agronomic perspective, the most efficient system would be to apply organic input to the Brassicaceae species, while the following cereals will benefit from the residual OP.

But, this will require more investigation in the future. Another interesting effect of rotational crops for organic input management is the particular ability of legumes to affect soil P levels. Indeed, legumes significantly decrease soil IP/OP ratio values [START_REF] Lazali | Stratégies et mécanismes d'adaptation des légumineuses à la faible disponibilité des sols en phosphore[END_REF]. Thus, linking the efficiency of legumes to mobilize OP to the type of organic input is an essential step to know and optimize the combination of the crop species in relation to the P fertilizer type, thus allowing a more sustainable P fertilization.

It is now known that the application of organic input in rotations would affect soil OP reserves and their dynamics over time (Houben et al., 2019;[START_REF] Lazali | Stratégies et mécanismes d'adaptation des légumineuses à la faible disponibilité des sols en phosphore[END_REF][START_REF] Lemming | Plant availability of phosphorus from dewatered sewage sludge, untreated incineration ashes, and other products recovered from a wastewater treatment system[END_REF]. In general, as Glaesner et al. [START_REF] Glaesner | Phosphorus characterization and plant availability in soil profiles after long-term urban waste application[END_REF] point out, organic inputs, due to their OP content, have an impact on labile P in crop rotations system, which remains highly available to plants in the soil after long-term application. However, most of the studies do not generally consider how other forms of soil P (already available soil P) are affected in the rotation. In addition, the ability of rotational crops to mobilize OP from organic inputs remains poorly understood. Indeed, recent work suggests that P availability in rotations may change over time due to changes in the dynamics of soil-bound OP pools, which in turn are mediated by the type of crop in rotation (mobilization/acquisition strategies), concentrations, and forms of OP in organic input. Further studies are needed to determine the relative contribution of rotational crops with contrasting OP acquisition strategies on increasing labile P using isotope labeling techniques. As an innovative perspective to better manage short-or long-term OP inputs in agrosystems, fertilization management models need to evolve at the rotational scale by integrating plant traits, organic waste forms of OP, and soil properties to model microbial activities and their effects on available P.

Future Prospects

From the importance of OP mobilization processes by roots and rhizosphere microbiome, several suggestions and avenues of research can be deduced as well as promising approaches and innovative techniques that could improve the cycling of OP in the soil for use by plants. This includes a multipronged combination of beneficial biota, agronomic management practices and genetically-improved plants:

An important first direction for future research would be to focus on developing new cropping systems to recycle P from OP pools. To this end, understanding the impacts of cropping strategies, whether in rotation or intercropping systems, on mobilized OP could be promising for managing P availability for agroecological development. With this knowledge, crop species/genotypes (with specific morphological and physiological traits) which can enhance OP use efficiency could easily be identified and selected to improve plant P acquisition and thus reduce the amount of P fertilizer needed to maximize production.

For this purpose, we suggest that future researches studies could test plants with different P mobilization/acquisition traits in monospecific treatment or in multispecies treatment under different sources of OP. This would allow not only to evaluate the overall P uptake between these different treatments (multi-species and monospecific), but also to better determine their higher P use efficiency.

Inclusion of multi-species or single-species with different P-uptake strategies in P-uptake efficiency as cover crops or in crop rotation can help to develop new cropping system to recycle more OP and reduce the use of mineral P fertilizer. Other practices include better use of organic input as an alternative source of P by its better management in crop rotations, or of biofertilizers (microbial inoculants). The combination of these different practices deserves to be further explored and developed.

Since P availability depends on the interactions between OP and crop traits, the timing of application, the influence of both OP and the type of organic input and plants on microbial communities, it is necessary to start from the characterization of OP species in organic inputs and then study their relationship with soil properties and plant traits to really understand the P cycle and manage P availability. Furthermore, the direct contribution of OP to plant nutrition also needs to be well understood by quantifying the availability of readily available forms of OP to plants and by better understanding the dynamics of those adsorbed on soil minerals (sol-OP bonding complex). This knowledge will be useful to predict P availability as a function of the form that is applied and to better model P behavior as a function of soil properties and organic input characteristics.

At present, it is not known how the application of organic input can have an impact on the structure of the rhizosphere microbiome-root traits interaction on OP mobilization in the rhizosphere.

Furthermore, the pathways and thresholds of transformation of OP species in soils amended with organic inputs, and especially their interaction or competition with existing OP pools in soils, and all this in relation to mobilization processes by rhizosphere microbiomes and root traits, remain largely unknown.

Therefore, it is important for future research to highlight the role of OP forms from organic inputs in the changes of existing soil P forms over time by well characterizing the effect of rhizosphere microbiomes and root traits involved in their dynamics and how they relate to soil properties. The identification of these factors is a crucial step in fostering the utilization of soil OP by crop plants. Simultaneously, elucidating the plant uptake system to acquire OP can provide a strong complement to these efforts.

Apart from adding different OP species to the soil, the decomposition of organic inputs can activate exogenous microorganisms and organic acids that can influence OP dynamics (mobilization process), but these aspects are very poorly considered in the literature.

The N-P interactions play a major role in the C and P cycles (co-limiting or synergistic effects depending on their concentrations) and, accordingly, organic fertilization is jointly managed in the cropping system. Since organic inputs differ in terms of N concentration and organic carbon composition (e.g. cellulose, hemicellulose, lignin) which in turn impact microbiome-root trait interactions (protons, pH reduced, organic acid, phosphatase), one hypothesis is that forms of OP would have different response times to changes in nutrient status (C and N levels) in agricultural ecosystems. Thus, to confirm or refute the hypothesis, future research is needed to evaluate the actual effect of these compounds on OP mobilization in the organic input-soil-plant system.

Most research on the potential of microbes to mobilize OP has been conducted on culturable microbes. Because most rhizosphere microbiomes associated with plant roots are not culturable, further research on these microbes in the plant rhizosphere is needed, which will improve knowledge of the microbial community and microbe-plant roots traits interactions in OP mobilization. Furthermore, since the ability of rhizosphere microbiomes to mobilize OP varies with the forms of OP and their chemical properties, in order to better take advantage of these soil organisms or even select and introduce them, it is recommended that screening of these bacteria in the presence of different forms of OP and different soil properties be investigated, since in most studies, these bacteria have been screened under conditions where neither the forms of OP nor the soil properties are highlighted.

It is known that plant roots associated with rhizosphere microbiome can express synergistic effects to increase IP uptake by mobilizing more OP in the soil. Therefore, further research is needed to evaluate the actual effectiveness of beneficial rhizosphere microbiome associations whith various crops with contrasting root traits and fertilized with different P sources under field conditions, as well as how the mechanisms by which they mobilize OP, are hampered by competition with endemic microorganisms and soil properties (P sorption capacity, soil P status, pH, etc.).

Sustainable agricultural systems are expected to enhance the diversity of functional microorganisms in the soil, especially those actively involved in P mobilization from organic inputs or soil organic matter. However, given the lack of data about the link between sustainable agricultural systems and OP mobilization, it is important for future research to characterize both direct and indirect effect of such systems on OP mobilization in the organic input-soil-plant continuum.

Conclusion

Organic inputs and soil, can be used as a primary or supplementary source for plant P nutrition. This is because OP is as important in amount as IP in soil and organic inputs. However, the present review highlights that OP present in organic inputs and soil is in various chemical forms which differ in their ability to be mobilized and their availability to plants. These forms of OP tend to be scarcely available in agroecosystems because of their strong affinity for soil mineral surfaces. Rhizosphere microbiomes have the potential to mobilize and mineralize different forms of available and unavailable OP. Various controlled experiments using plants inoculated with the rhizosphere microbiome provide evidence for this. Rhizosphere microbiomes solubilize OP through the production of organic acids and then mineralize it via enzymes. However, the mechanisms associated with this mineralization are poorly understood, and in most studies, the experimental conditions suppress interactions between the components of the system. Furthermore, there is little evidence on how these rhizosphere microbiomes can act in the presence of soil minerals that can immobilize both OP and hydrolytic enzymes. Future work should be conducted by inoculating microorganisms with sorbed OP complexes on key soil minerals under laboratory conditions and even further in the field. Root traits may alter rhizosphere characteristics to enhance reactions of OP dissolution, desorption, chelation and mineralization. These traits are related to root P foraging strategy and may include alterations in root structure such as plasticity in low P stress responses and spatial arrangement of roots to induce a diffusion gradient that will in turn promote the process of OP desorption and thus P availability. Expansion of fine roots and longer, denser root hairs promotes OP acquisition by roots via increased root surface area. Physiological characteristics related to P mining strategy may alter pH and/or release carboxylates and phosphatases to increase turnover of sorbed OP pools. These rhizosphere microbiome and root traits processes are continuously interacting to modulate the stock of OP in agricultural soils. An alternative approach to P limitation would be to use crop species/genotypes with specific traits, inoculated naturally by rhizosphere microbiomes with suitable OP forms and soil properties, at crop and rotation scales, to increase OP mobilization from organic inputs. Thus, under conditions of P-deficient or soils amended with organic inputs, root traits and soil microbes will be effective in increasing plant growth especially by mobilizing highly-binding OP forms. The present work reinforces the need to develop future research to understand the trade-offs between root traits, their relationship to microbes, and their direct effect on OP mobilization and P availability. These mechanisms/processes could be integrated into models and decision support tools for estimating soil P availability and managing P fertility from organic waste.

PhD OBJECTIVES

This Ph.D. project aims to understand better the role of organic phosphorus forms (OP), soil minerals, nitrogen (N), and crop functional traits and their interactions on P availability and acquisition by plants for optimizing organic fertilizer management in agrosystems. To address this general objective four chapters were produced to examine the central and still pending questions involved (Figure 7).

Chapter 1 examined the sorption and desorption of OP on goethite, gibbsite, kaolinite, and montmorillonite. The goal of this chapter was to elucidate the adsorption and desorption dynamics of several forms of OP on several representative soil minerals. Specifically, the objective was to determine the factors underlying the adsorption and desorption of OPs onto and from soil minerals. It is assumed that the selected Fe, Al oxides, and clay minerals abundant in soils will exhibit various adsorption and desorption capacities due to their contrasting chemical properties.

Chapter 2 studied the role of soil minerals on organic phosphorus availability and P uptake by plants.

The objective was to elucidate the extent to which OP bound to Fe and Al oxyhydroxides and clay mineral complexes contributes to plant P acquisition. Specifically, we determined P availability to plants from several IHP, G6P, and GLY complexes that were adsorbed onto Fe and Al oxyhydroxides (goethite and gibbsite) and clay minerals (kaolinite and montmorillonite). The following three main hypotheses were discussed: (1) P from adsorbed OP compounds is available to ryegrass and varies with soil mineral properties;

(2) the relative P uptake of various OP-mineral complexes depends on their binding strength; and (3) adsorbed OP compounds are less available than adsorbed IP because it desorbs less and requires not only desorption but also enzymatic cleavage before being taken up by ryegrass. These aims could open up possibilities for utilization of renewable nutrient-rich organic amendments based on various soil mineral properties.

Chapter 3 aimed to understand better how N and soil mineralogy determine phosphorus limitation and plant P uptake from inorganic and organic forms of P. It focuses on assessing the independent and interactive effects of N and P forms and their interaction with soil minerals on P limitation in plants, to unravel biogeochemical processes involved in P limitation by characterization the role of N and P forms and their interaction with soil minerals in P availability and uptake by plants. The following assumptions were made: (1) addition of N in various specific forms would increase P limitation under conditions with low P availability, i.e. with OP forms and soil minerals, (2) plants shift from N limitation to P limitation would be due to the beneficial effect of N addition on rhizosphere processes involved in P mobilization/acquisition by plants, and (3) the degree of both P limitation and total plant P uptake would vary significantly by mineral type and P forms because of the contrasting physicochemical properties of the minerals used and the biochemical nature of the P sources. The results of this chapter are needed not only to enable ecosystem models to accurately predict plant N-P limitation and its impacts, but also to develop robust ecosystem models with fully coupled N-P or C-N-P interactions.

Chapter 4 aimed at estimating the role of phosphorus-acquisition strategies on organic P mobilization and acquisition. The objective of this chapter was to examine the response of P acquisition strategies toward P forms (IP and OP) in interactions with soil minerals and their consequences on OP availability and acquisition. The general hypothesis was that P-acquisition strategies (i.e. foraging and mining) differ in their responses to P sources, and this would promote greater OP availability and P acquisition from soil minerals. More specifically, (1) morphological traits involved in P-foraging strategy will increase P availability and uptake from OP. These traits would induce a diffusion gradient which, in turn, will favor the desorption process of the different forms of adsorbed OP, and thus the availability of P and (2) physiological traits involved in P-mining strategy will increase P availability and uptake by modifying the pH and/or release carboxylates and phosphatases allowing to increase the turnover of the pools of sorbed OP via desorption, solubilization and mineralization processes;

(3) the acquisition of P from OP will be more significant under strategies involving P-mining than under those involving P-foraging, because OPs will be hydrolyzed by the strong activities of phosphatase, and finally ( 4) regardless of the strategy, the acquisition of P from OPs will be lower than that of IPs due to their strong sorption on minerals. This chapter can offer insight into how phosphorus acquisition strategies could be utilized to increase OP mobilization, which would help rethink P fertilization, sustain production, and recycle more OP into soils amended with organic amendments.

Phd METHODS

Four complementary approaches were used to investigate the overall objective of this thesis. The first approach, addressing the objectives described in Chapter 1 (Figure 7), was to determine the factors underlying the adsorption and desorption of OPs onto and from soil minerals. After adsorption, both desorption and availability of OP forms to plants are still not elucidated. Therefore, the approach in Chapter 2 aims to investigate the extent to which OPs bound to Fe and Al oxyhydroxides and clay mineral complexes contribute to P acquisition by plants. Furthermore, since renewable P fertilizers differ in terms of nitrogen (N) concentration, which can impact the physicochemical and biological properties of the soil and thus the dynamics of OPs, the third approach, addressing the objectives described in Chapter 3, was to characterize the role of N and P forms and their interaction with soil minerals in the availability and uptake of P from OPs by plants. The fourth and final approach, addressing the objectives described in Chapter 4, examines the response of P acquisition strategies to OP forms interacting with soil minerals and their consequences on organic P availability and acquisition, before modeling the expected impacts on phosphorus uptake. In this step, plants with various P mobilization/acquisition characteristics were tested alone (single species treatment) (Figure 7).

Characterization of factors governing the dynamics of OP adsorption and desorption onto and from soil minerals

Moving toward more sustainable sources for managing P nutrition in agroecosystems, OP derived from organic inputs and soil is increasingly considered to complement mineral P fertilizer (Amadou et al., 2021;Sulieman and Mühling, 2021). However, enhancing OP cycling and availability in soils while reducing OP loss into the environment requires a better understanding of OP adsorption/desorption processes on soil minerals (Amadou et al., 2022;[START_REF] Wang | Phosphate and phytate adsorption and precipitation on ferrihydrite surfaces[END_REF]. Factors related to soil properties and OP molecular characteristics directly affect the reactions of OP and its release into the soil.

Extensive research has evaluated the adsorption of different individual sources of organic and inorganic P to soils or to individual soil minerals (Amadou et al., 2022). However, no study has evaluated and compared P desorption from the main OP compounds that were adsorbed onto the main soil minerals.

Deciphering the interactions between soil minerals and the predominant forms of OP in soils could provide new insights for the sustainable management of P in agroecosystems.

Triplicate batch experiments were conducted to understand the interactions between OP forms and soils minerals at different P concentrations. We used standard P adsorption procedure proposed by Nair et al. (1984). Three organic P (OP) compounds, IHP, GLY, G6P and one IP (KH2PO4) were selected based on their predominance in organic wastes and soils and their contrasted properties (type of P bonds, different molecular sizes). The individual soil minerals were selected to be representative of the predominant soil minerals involved in P adsorption in soils. Four individual soil minerals were used.

Goethite [FeO(OH)] and gibbsite [Al (OH)3] were chosen as representative of Fe and Al oxides; kaolinite and montmorillonite were selected as clay minerals, particularly 1:1 phyllosilicate and 2:1 phyllosilicate respectively. The minerals used have different specific surface areas (SSA) and points of zero charge (PZC). The SSA of the minerals used are as follows: goethite (46 m 2 g -1 ), gibbsite (120-364 m 2 g -1 ), kaolinite (19 m 2 g -1 ) and K-montmorillonite (83 m 2 g -1 ) and their PZCs were: goethite (7.04), gibbsite (9.3), kaolinite (4.5) and montmorillonite (2.5), as previously reported by other authors (He et al., 1994;He and Zhu, 1997;Ruttenberg and Sulak, 2011;Shang et al., 1990;Yan et al., 2014). Inorganic P was determined colorometrically (Ohno and Zibilske, 1991). Organic P compound samples was hydrolyzed to IP form before colorimetric determination by using the persulfate oxidation method (Peters and Van Slyke, 1932). The quantity of P adsorbed was calculated as the difference between the initial amount of P added and the remaining P amount in solution at the end of the adsorption experiment.

Total P concentration in a subsample of each P-loaded was also determined using the procedure by Ostrofsky (2012) and showed very similar values compared to the ones determined as the difference between the initial and the final P amount in the supernatant (differences were in the range of 3-5.5%

for the organic mineral-P complexes and 1.5-5% for the inorganic mineral-P complexes). Adsorption maxima, capacity and other adsorption parameters were determined by fitting data to the non-linear form of the Langmuir (1) and Freundlich (2) isothermal model (Crini et al., 2007;Langmuir, 1918).

Desorption maxima and rate were determined by fitting data to the non-linear form of the Elovich kinetic model (Bulut et al., 2008) (3). More specific details are described in the methodology section of Chapter 1.

Assessment of P availability to plants from several mineral-

OP complexes

Organic phosphorus (OP) represents a significant fraction of the total P pool in soils. With the increasing use of organic resources to substitute mineral P fertilizers and the need to recover P from the soil, it is pivotal to gain insight into the interactions between various OP forms and soil minerals and their consequences on P availability. Overall, our understanding of the dynamics of the major OP pools in the soil-plant system is very limited. Most research has focused on the dynamics of IP forms (Sulieman and Mühling, 2021), suggesting that soil characteristics control their availability to plants (Gómez-Suárez et al., 2020). However, OP forms may strongly differ from each other's and have therefore different biogeochemical processes controlling their availability and uptake by plants [START_REF] Anderson | Biochar induced soil microbial community change: Implications for biogeochemical cycling of carbon, nitrogen and phosphorus[END_REF]. To date, it is not known how the chemical forms of OPs, and their interactions with soil minerals, influence the uptake of OPs by plants in ecosystems. The paucity of research significantly limits our ability to understand the overall dynamics of P cycling in ecosystems and to optimize the use of renewable P fertilizers which often contain various forms of OP (Kelessidis and Stasinakis, 2012;Mininni et al., 2015).

After gaining more insight into the sorption and desorption dynamics of OPs in Chapter 1, this chapter aims to determine the extent to which adsorbed OPs are available to plants. Four soil minerals were loaded with the three OP compounds or inorganic P to serve as a P source for ryegrass (Chapter 2). The four minerals were selected to be representative of the predominant minerals in soils: Goethite [Fe (OH)O] and gibbsite [Al(OH)3] were chosen as representative of Fe and Al oxyhydroxides; kaolinite and montmorillonite were selected as clay minerals, particularly 1:1 phyllosilicate and 2:1 phyllosilicate respectively. The three OP compounds, include myo-inositol hexakisphosphate (IHP), glycerophosphate (GLY) and glucose-6-phosphate (G6P), and one inorganic P (KH2PO4). Organic P compounds were initially selected based on their predominance in organic inputs and soils, the types of P bonds and their different molecular sizes. The inorganic P form was chosen for comparison with organic P compounds.

We used the RHIZOtest device (MetRHIZlab, France) (Figure 8) designed by [START_REF] Bravin | RHIZOtest: A plant-based biotest to account for rhizosphere processes when assessing copper bioavailability[END_REF] which consists in separating plant roots from soil with a 30-mm polyamide mesh to facilitate the collection of roots and rhizosphere [START_REF] Houben | Impact of biochar and root-induced changes on metal dynamics in the rhizosphere of Agrostis capillaris and Lupinus albus[END_REF]. Prior to the experiment, the substrates were sterilized by autoclaving at 121 °C for 2 h (Gómez-Suárez et al., 2020) to eliminate potential microorganisms, allowing therefore to attribute the results to the only effect of root activity. To avoid any P limitation for plants during the experiment, we supplied a total amount of P which was previously found to sufficiently meet the plant requirement in such RHIZOtest devices (Gómez-Suárez et al., 2020). The RHIZOtest devices were placed in controlled conditions (phytotron) under a photoperiod of 12h, constant temperature (25 °C), and relative humidity (80%). Unplanted control treatments, in which the quartzmineral-P complex had been incubated in similar devices without plants (hereafter called the bulk substrate), were also conducted. In total, 128 such devices were implemented: 4 P compounds (IHP, GLY, G6P, and IP) x 4 soils minerals (goethite, gibbsite, kaolinite and montmorillonite) x 2 crop conditions (ryegrass and bulk soil) x 4 replicates. The concentration of P in shoots and roots was determined colorimetrically (Ohno and Zibilske, 1991) after mineralization by 65% HNO3 digestion directly in a microwave Teflon vessel (Lange et al., 2014). The amount of P taken up by shoot and root from the P-mineral complexes was calculated as the difference between the amount of P in plant parts at the end of the experiment minus the average amount of P in plants at the end of the preculture period.

Total plant P uptake from P-minerals was calculated by summing P uptake from P-minerals by roots (i.e., root P concentration multiplied by root dry mass) and P uptake from P-minerals by shoot (i.e., shoot P concentration multiplied by shoot dry mass). The percentage of P recovered by ryegrass was determined. To assess the factors that determine OP availability to the plant, desorption dynamics, rhizosphere and bulk soil P availability and Phosphomonoesterase activities were evaluated. and P forms and their interaction with soil minerals

Ecosystem N and P cycling consists of multiple pools and biogeochemical processes that are interrelated and interdependent, jointly controlling soil P availability, plant P uptake and its limitation [START_REF] Zhang | En outre, différentes stratégies de mobilisation et d'acquisition des OP dans les espèces et cultivars de cultures ont été démontrées, mais leur efficacité dans l'acquisition de P à partir des différentes formes d'OP et d'IP reste peu étudiée[END_REF]. To date, it remains unclear how N forms, P chemical forms, and their interactions with soil minerals influence both P limitation and P uptake by plants within ecosystems. The paucity of research on the effect of these important biogeochemical processes (N-P-soil minerals), severely limits our ability to understand ecological processes underlying the alteration of ecosystem P cycling with N additions.

More importantly, it limits our ability to incorporate the actual impact of P limitation into ecosystem models used to analyze the effects of potential future climate change on overall ecosystem productivity (Deng et al., 2017;Goll et al., 2012).

In Chapter 2, the availability of OPs was strongly determined by OP forms and mineral types. However, to date, it remains unclear how N forms contained in organic fertilizers and their interactions with soil minerals influence OP dynamics, i.e., OP availability, P limitation, and P uptake by plants in ecosystems.

To attempt to answer this question in this chapter, two minerals (goethite and kaolinite) were loaded with the three compounds P (IHP, GLY, and IP) to serve as a source of P for ryegrass. The two minerals were chosen on the basis of their contrasting characteristics, as shown in Chapter 1. The procedure for preparing the mineral-OP complexes was similar to that described in Chapter 2. The two forms of nitrogen used were ammonium (NH4-N) provided as (NH4)2SO4 and nitrate (NO3-N) provided as Ca (NO3)2. We used a device whose principle is very similar to the RHIZOtest except that here, the roots of the plants are not separated from the soil but remain separated from the nutrient solution (Figure 9).

Non-planted control treatments, in which the quartz-mineral-P complex was incubated without plants (hereafter called bulk substrate), were also performed. A total of 96 such devices were implemented: 3 P compounds (IHP, GLY and IP) x 2 soil minerals (goethite and kaolinite) x 2 forms of nitrogen (NO3-N and NH4-N) x 2 cropping conditions (ryegrass and bulk soil) x 4 replicates. The concentration of P in shoots and roots was determined calorimetrically (Ohno and Zibilske, 1991) after mineralization by 65%

HNO3 digestion directly in a microwave Teflon vessel (Lange et al., 2014). In addition to P analysis, the N elemental concentrations were determined. We calculated N:P ratios by dividing leaf N concentration by leaf P concentration (both as percentage nutrient in the sample) within each plant tissue sample. Total plant P uptake was calculated by summing P uptake by roots. After defrosting some samples, acid phosphomonoesterase activity in the rhizosheath (PME) was measured with a modified buffer at pH 6.5 [START_REF] Tabatabai | Use of p-nitrophenyl phosphate for assay of soil phosphatase activity[END_REF]. The plant P acquisition traits are known and their indirect and sometimes even direct effects on P acquisition/mobilization have been demonstrated (Ma et al., 2018;Nobile et al., 2019). The processes differ according to the nature of IP or OP forms (phosphate mono or diester) and the physicochemical properties of the soil. For instance, the availability of the different OP forms (IHP, G6P, GLY, DNA and RNA) as a direct effect of P acquisition strategies (P mining and foraging) remains unclear.

Although the release of carboxylates can make some OP (G6P, GLY) available to plants, it is less efficient to solubilize IHP (Gerke, 2015) probably due to its strong binding to soil. Interactions between plant functional traits in the mobilization/acquisition of both OP and IP have been studied but remain poorly understood and unconfirmed. Thus, it has been suggested that plant strategies can be exploited using combinations of species with contrasting strategies or using a single species to understand better their actual effects on OP mobilization and acquisition in agroecosystems. A better understanding of the impact of P-acquisition strategies on OP mobilization and acquisition by plants, which are related to the multiple morphological and physiological traits and the interactions between them, is key in the management of OP availability.

In order to examine the response of P acquisition strategies toward P forms (IP and OP) in interactions with soil minerals and their consequences on OP availability and acquisition, a wide range of traits were measured for their recognized role in phosphorus acquisition [START_REF] Lynch | Root architecture and nutrient acquisition[END_REF]. Measured traits included morphological and architectural traits (root length density, root surface area, specific root length, finer root percentage) involved in plant phosphorus foraging capacity (Haling et al., 2018)and physiological traits or indicator thereof (phosphomonoesterase activity in the rhizosheath, change in rhizosheath pH, carboxylate exudation rate) involved in plant phosphorus mobilizing capacity [START_REF] Sun | Influence of intercropping and intercropping plus rhizobial inoculation on microbial activity and community composition in rhizosphere of alfalfa (Medicago sativa L.) and Siberian wild rye (Elymus sibiricus L.)[END_REF]. Two OP compounds, including inositol hexakisphosphate/phytate (IHP) and glycerophosphate (GLY), as well as inorganic P (KH2PO4), were selected for the experiments. Organic P compounds were initially selected because of their ubiquity in organic inputs and soils, the nature of phosphorus bonds, and their variable molecular sizes. Inorganic P forms were selected for comparison with organic P compounds. Two minerals were chosen because of their contrasting properties and as Hydrophyllaceae: Phacelia tanacetifolia Benth.) were selected for their diverse morphologies, P-acquisition traits and relevance for the local context. Species selection is central in order to observe enough diversity in trait attributes to produce generalisable results [START_REF] Duarte | Comparative functional plant ecology: rationale and potentials[END_REF]. Species from different phylogenetic families (Poaceae, Fabaceae and Hydrophyllaceae) were selected in order to ensure we would observe varied trait values and phosphorus acquisition strategies. Fabaceae have been observed to have high phosphorus mining capacity (Maltais-Landry, 2015) and often incorporated in cover crops for their ability to fix atmospheric N. Poaceae species were selected due their phosphorusforaging strategy. Finally, Hydrophyllaceae were selected for their capacity to mine phosphorus and capacity to forage large soil volumes respectively. To construct the experimental mesocosms, we filled 120×120 mm square polymer Petri dishes with sterilized coarse quartz sand (Figure 10), which is extremely poor in soil nutrients. The various P-mineral complexes prepared were then added to each square Petri dish and mixed with acid-washed quartz. Prior to the experiment, the substrates were sterilized by autoclaving at 121 °C for 2 h (Gómez-Suárez et al., 2020)to eliminate potential microorganisms, thus allowing the results to be attributed to the effect of root activity alone. The procedure for preparing the mineral-OP complexes was similar to that described in Chapter 2 and 3. To avoid any P limitation for the plants during the experiment, we provided a total amount of P that was found to be sufficient to meet the plants' needs (Gómez-Suárez et al., 2020). A total of 480 such devices were implemented: 8 species x 3 P compounds (IHP, GLY and IP) x 2 soil minerals (goethite and kaolinite) x 2 cropping conditions (ryegrass and bulk soil) x 5 replicates. A multivariate clustering approach was employed to identify plant phosphorus acquisition strategies based on the array of phosphorus acquisition trait measured.

Highlights

• Mineral properties and organic P (OP) characteristics affected OP (de)sorption

• Myo-inositol hexakisphosphate had higher adsorption than the other OP forms

• Organic P showed contrasted adsorption capacities relative to inorganic P forms (IP)

• Fe and Al oxides exhibited highest adsorption capacity compared to clay minerals

• Organic P was more desorbed from clays minerals than from Fe and Al oxides Graphical abstract

Introduction

Phosphorus (P) is one of the essential nutrients required for plant growth and an important driver of agroecosystem productivity (Hu et al., 2020a;Ruttenberg and Sulak, 2011). Due to its low solubility and high affinity for mineral surfaces [START_REF] Roy | Soil phosphorus sorption capacity after three decades of intensive fertilization in Mato Grosso, Brazil[END_REF][START_REF] Tisdale | Soil Fertility and Fertilizers[END_REF], P availability is limited in agricultural soils and rarely sufficient for optimum growth and development of crops. On the other hand, accumulation of P in the soil increases the risk of P leaching and runoff, consequently leading to eutrophication of surface waters [START_REF] Hansen | The fate and transport of phosphorus in agricultural systems[END_REF]. Therefore, with the increasing use of organic resources as P fertilizers (Amadou et al., 2021), a sustainable and efficient use of organic P (OP)

fertilizers is of utmost importance to secure future crop production and reduce environmental hazard (Faucon et al., 2015). However, most of the research investigating the fate of P applied to the soil has focused on inorganic P (IP) so far, showing that most of it was adsorbed onto iron (Fe) and aluminum (Al)-oxides and clays minerals (Celi et al., 2000(Celi et al., , 1999) ) or precipitated with Ca (Houben et al., 2011;[START_REF] Urrutia | Theoretical chemical characterization of phosphate-metal-humic complexes and relationships with their effects on both phosphorus soil fixation and phosphorus availability for plants[END_REF]. In contrast, the fate of OP has been disregarded so far even though it is now clear that these forms of P can be at least as available as IP (Amadou et al., 2021;Kahiluoto et al., 2015).

Organic P can be mineralized along with plant uptake and/or be protected by organic substances from adsorption, even in the long term [START_REF] Huang | Hydrolysis of glucose-6-phosphate in aged, acid-forced hydrolysed nanomolar inorganic iron solutions-an inorganic biocatalyst?[END_REF]. However, the adsorption mechanisms of OP and the factors that affect sorbing processes remain poorly understood (Yan et al., 2014) and there is still a lack of knowledge about their contribution to plant nutrition (Faucon et al., 2015).

Organic P in soil-plant-system comes from both soil and organic waste sources (e.g. manure, compost, sludge, biochar, …) (Fuentes et al., 2006). The major OP compounds from soil and organic wastes include IHP [START_REF] Turner | Inositol phosphates in the environment[END_REF]Vincent et al., 2013), GLY (Doolette et al., 2011;Newman and Tate, 1980) and G6P (Deiss et al., 2018;Giles et al., 2011). Each form differs from the others by its P content, P bond type and molecular size. They may constitute large fractions of the total P in soils (Monbet et al., 2009), especially in organic waste-amended soils [START_REF] Khare | XANES Determination of Adsorbed Phosphate Distribution between Ferrihydrite and Boehmite in Mixtures[END_REF]. It has been shown

that adsorption of OP compounds increases with the number of P groups. Therefore, with six phosphate groups, IHP has a high charge density and would undergo a strong interaction with the soil (Anderson and Arlidge, 1962;Celi et al., 1999). This higher accumulation of IHP through adsorption limits P acquisition by plants from this source. The size and molecular structure of OP forms generally affect their adsorption capacity. The G6P adsorption density and rate is higher than IHP and adenosine triphosphate (ATP) as a result of its lower molar mass (Giaveno et al., 2008). However, Goebel et al., (2017) reported that G6P is potentially more available than IHP and ATP.

After adsorption, the ability of soil minerals to release P in soil solution determines P availability for plants but also loss of P in both surface runoff and subsurface flow [START_REF] Sharpley | Phosphorus loss from land to water: integrating agricultural and environmental management[END_REF]. Several authors have suggested that P from mineral-P complexes is not available to plants because of their very limited desorption [START_REF] Barrow | Reaction of Anions and Cations with Variable-Charge Soils[END_REF]Bollyn et al., 2017;Guzman et al., 1994;Lagos et al., 2016). For instance, Bollyn et al., (2017) showed that after several cycles of desorption, less than 5% P desorbed from IHP-goethite complexes. Similar results by Lagos et al., (2016) showed limited desorption of IHP (<3% P) from gibbsite. On the other hand, there is also experimental evidence that P can desorb significantly from minerals to be available to plants and runoff (Andrino et al., 2019;Parfitt, 1979).

However, in all of these studies cited above, the form of P used was exclusively IP with very limited consideration for important OP pools such as IHP, GLY or G6P. Furthermore, the soil minerals used were in most cases Fe oxides (namely goethite) while Al oxides and clay minerals were much less investigated. To our knowledge, no study has evaluated and compared P desorption from the main OP compounds (IHP, GLY, and G6P) that were adsorbed onto the main soil minerals (Fe and Al oxides, and clay minerals). There is a need to bridge this gap of knowledge to identify the properties that govern OP adsorption and desorption processes and gaining insight into the behavior of OP compounds at the surface of soil minerals.

In sum, extensive research has evaluated the adsorption of different individual sources of organic and inorganic P to soils or to individual soil minerals. However, no study has evaluated and compared P desorption from the main OP compounds that were adsorbed onto the main soil minerals.

The aim of our study was to elucidate the dynamics of adsorption and desorption of several forms of OP on several representative soil minerals. More specifically, we aimed at determining the drivers of adsorption and desorption of OP on soil minerals. For this purpose, we studied the adsorption of three OP compounds, myo-inositol hexakisphosphate (IHP), glycerophosphate (GLY) and glucose-6phosphate (G6P) and one inorganic compound (KH2PO4, IP) on Fe and Al oxides (goethite and gibbsite, respectively) and on clay minerals (kaolinite and montmorillonite). Organic P sources were chosen based on their predominance in both soils and organic inputs and their contrasted chemical properties.

We assume that the selected Fe, Al oxides and clay minerals, abundant in the soils, will present different capacities of adsorption and desorption due to their chemical properties.

Materials and methods

Organic P forms and individual soil minerals

Three organic P (OP) compounds, IHP, GLY, G6P and one IP (KH2PO4) (Figure 11) were selected based on their predominance in organic wastes and soils and their contrasted properties (type of P bonds, different molecular sizes). The individual soil minerals were selected to be representative of the predominant soil minerals involved in P adsorption in soils. Four individual soil minerals were used.

Goethite [FeO(OH)] and gibbsite [Al (OH)3] were chosen as representative of Fe and Al oxides;

kaolinite and montmorillonite were selected as clay minerals, particularly 1:1 phyllosilicate and 2:1 phyllosilicate respectively. The minerals used have different specific surface areas (SSA) and points of zero charge (PZC). The SSA of the minerals used are as follows: goethite (46 m 2 g -1 ), gibbsite (120-364 m 2 g -1 ), kaolinite (19 m 2 g -1 ) and K-montmorillonite (83 m 2 g -1 ) and their PZCs were: goethite (7.04), gibbsite (9.3), kaolinite (4.5) and montmorillonite (2.5), as previously reported by other authors (He et al., 1994;He and Zhu, 1997;Ruttenberg and Sulak, 2011;Shang et al., 1990;Yan et al., 2014). All minerals were obtained from Sigma-Aldrich Chemie S.a.r.l. and VWR (France) for experimentation (see supplementary data references in supplementary data (Appendix A, Table S1) for mineral references).

Adsorption Experiments

Triplicate batch experiments were conducted to understand the interactions between OP forms and soils minerals at different P concentrations. We used standard P adsorption procedure proposed by Nair et al., (1984). Prior to adsorption, 80mg of each soil mineral were weighed and transferred to 50 mL polypropylene centrifuge tubes. Then, 20 ml of 0.1 M KCl were added and the tubes were shaken for 24 hours at 25°C to sufficiently hydrate the adsorption sites on the minerals. The pH was maintained at 5.5 ± 0.05 by adding 0.1 M HCl or NaOH solution. Six P concentrations (0, 4, 8, 16, 40, 75 and 100 mg L - 1 ) were used for each P forms. Phosphorus stock solutions of each OP were prepared under the same conditions of 0.1 M KCl at pH 5.5. KCl was used as electrolyte to mimic the environmental condition and adjust ionic strength of the solution. To start the adsorption, 20 ml of solution containing each concentration of P were pipetted into tubes containing the soil particles. The control experiment was the same but without P. The final volume was 40 mL and the concentration of particles in this final volume was 2 g L -1 . In each tube, some drops of hexanol were added to suppress microbial activities. The final samples were shaken on a mechanical shaker for 24 hours at 25°C and then centrifuged (3000 g for 15 minutes). After centrifugation, samples were immediately filtered through a 0.22-μm membrane syringe filter. The filtrates were stored in a cold room until the P content was analyzed. Inorganic P was determined colorometrically (Ohno and Zibilske, 1991). Organic P compound samples was hydrolyzed to IP form before colorimetric determination by using the persulfate oxidation method (Peters and Van Slyke, 1932). The quantity of P adsorbed was calculated as the difference between the initial amount of P added and the remaining P amount in solution at the end of the adsorption experiment. Adsorption maxima, capacity and other adsorption parameters were determined by fitting data to the non-linear form of the Langmuir (1) and Freundlich (2) isothermal model (Crini et al., 2007;Langmuir, 1918):

Qads = Qm KL [Ce/ (1+ KL Ce)] (1) ;
where Ce is the concentration of P in the equilibrium solution (mg L -1 ), Qads is the total amount of P adsorbed, KL is the affinity constant or binding energy (L mg -1 ), and Qm is the P adsorption maxima (µg g -1 ). The ability of soil minerals to resist a change in solution P concentration was measured as the maximum adsorption buffer capacity: MBC = KL × (Qm); where KL and Qm are the binding-energy related constant and maximum adsorption, respectively, in the Langmuir equation.

Qads = KF Ce 1/nF (2);
where Qads (µg g -1 ) is the total amount of P adsorbed, Ce is the adsorbate equilibrium concentration in solution, KF (µmol L -1 ) is adsorption capacity, and nF (mmol L -1 ) is Freundlich exponent.

Desorption kinetics experiments

Prior to desorption, the four soil minerals were loaded with the three OP compounds or IP. Solutions containing 1 g P L -1 in 0.1 M KCl at pH 5.5 were prepared using the different P compounds. Goethite, gibbsite, kaolinite and montmorillonite was weighed in portions of 100 g into 1L bottles containing.

Then, 200 ml of 0.1 M KCl were added and the bottles were shaken for 24 hours at 25°C to sufficiently hydrate the adsorption sites on the minerals. The pH was maintained at 5.5 ± 0.05 by adding 0.1 M HCl or NaOH solution. To start the complex formations, each of the 1L bottles containing the soil minerals was filled with 800 ml of P solutions. This was done in order to obtain all the mineral-P complexes, for example for goethite we will have: goethite-IP, goethite-IHP, goethite-G6P and goethite-GLY and similarly for the other minerals. In each 1L bottles containing both the soil minerals and P compounds, some drops of hexanol were added to suppress microbial activities. The final samples containing in the bottles were shaken on a mechanical shaker for 24 hours at 25°C and then centrifuged (3000 g for 15 minutes). The 1L bottles were distributed into several small 250-mL bottles, centrifuged, and the supernatants were collected. Centrifugation was repeated until the maximum volume of supernatants was removed. The produced P-loaded minerals was agitated in deionized water and frozen at -20•C. The amounts of adsorbed P were determined using the same procedure as described in Section 4.3. The amounts of adsorbed P (µgP g -1 ) were similar to the Qm values (Table 11) of the adsorption data (Section 2.2) that were predicted by the Langmuir model.

Desorption kinetics experiments were initiated by adding 40 ml of 0.1 M KCl adjusted to pH 5.5 to 0.5g of the different minerals-P complex. Samples were shaken on a mechanical shaker at 25°C at regular intervals (24h, 48h, 72h, 96h). After the first cycle (24h), the entire suspension was removed and immediately filtered through a 0.22-μm membrane filter. A fresh 40 ml solution of 0.1 M KCl was added to start the second cycle (48h). The same process was applied for the remaining cycles. The P concentration in the supernatant was determined as described above. Desorption maxima and rate were determined by fitting data to the non-linear form of the Elovich kinetic model (Bulut et al., 2008) (3):

Q = A + B * Lnt (3);
where q is the amount of P desorbed at time t, and A and B are the constants with 𝐴 = in the Elovich equation is the amount of P desorbed in the first day of desorption (q = A +B*ln t, A = q when t = 1) and that B (mgP day -1 ) is positively related with the P desorption rate as demonstrated in the studies of (He and al. 1994). A and B values have been used to compare P release rate in different soils (He and Zhu, 1997). The maximum desorption amount (Dm) was calculated as total amount P desorbed.

Statistical analysis

All the Langmuir, Freundlich and Elovich model's parameters were evaluated by non-linear regression method using function nls from Package 'nlstools' in R software. Nonlinear parameter estimates can be obtained using different methods [START_REF] Archontoulis | Nonlinear Regression Models and Applications in Agricultural Research[END_REF][START_REF] Bates | Nonlinear Regression Analysis and Its Applications[END_REF]; the most common is ordinary least squares, which minimizes the sum of squared error between observations and predictions [START_REF] Brown | A step-by-step guide to non-linear regression analysis of experimental data using a Microsoft Excel spreadsheet[END_REF]. The determination coefficient (R 2 ) for each parameter was used to measure the goodness-of-fit. Apart from R 2 , standard errors (S.E.) were also used to determine the best-fitting isotherm to the experimental data. The conceptual framework was performed using correlate and network plot function in the latest development version of the corr package (Ahmed et al., 2021). This generates a network graph of a correlation data frame in which variables that are more highly correlated appear closer together and are connected by stronger paths. The proximity of points is determined using multidimensional clustering.

Results

Dynamics of Organic Phosphorus Adsorption

Effect of OP forms on adsorption dynamics

Organic P adsorption differed for each specific OP compounds (Table 11). The strongest differences in OP adsorbed among the different isotherms occurred with the greatest initial OP concentrations (Figure 12). In addition, the magnitude of OP adsorption increased rapidly when the initial OP concentration was low (< 25 mg L -1 ), but became relatively slow with increasing concentration (up to 40 mg L -1 ). Each OP compound had different adsorption characteristics onto the various soil minerals. The Qm, i.e.

maximum OP adsorption capacity from the Langmuir equation (Table 11) ranged from 1045 µg g -1 to 56697µg g -1 , indicating marked variations in the amount of OP adsorbed. Among the OP compounds, IHP was the most adsorbed form (3742-56697 µg g -1 ) followed by G6P and then GLY (1045-6237 µg g -1 ) (Figure 12 and Table 11). The adsorption maxima of OP increased with increasing molar mass in this order: GLY (172 g mol -1 ) < G6P (260 g mol -1 ) < IHP (660 g mol -1 ), which showed that the size of the molecule would have favored the adsorption of OP compounds.

Compared to IP, a contrasted adsorption behavior of OP compounds was observed. The adsorption dynamics followed the trend IHP > IP > G6P > GLY, showing that IHP was more adsorbed than IP, which in turn was more adsorbed than the G6P and GLY forms (Figure 12 and Table 11). The KL value, i.e. the binding energy between OP and minerals surfaces were highly variable. With the exception of montmorillonite, GLY or G6P showed higher or equal binding strength compared IHP (Table 11). Our results showed that the adsorption dynamics of OP was strongly controlled by their biogeochemical properties in the soil. The IHP, GLY and G6P form showed a different adsorption process from each other as well as from the IP form. In general, IHP was found to be the most adsorbed P form and GLY the least adsorbed form. S2).

Adsorption dynamics as affected by soil minerals

Isotherms of OP adsorption for the four tested minerals demonstrated that OP adsorption patterns of the Fe and Al oxides (goethite and gibbsite, respectively) were very similar but quite different from that of clays minerals (montmorillonite and kaolinite) (Figure 12). Fe and Al oxides rapidly adsorbed OP and their adsorption maximum was reached at a lower initial concentration than for clays. All tested minerals fitted the Langmuir and Freundlich equation (Table 11). Adsorption capacity (KF) of OP by soil minerals followed the trend kaolinite < montmorillonite < goethite << Gibbsite (Table 11), showing a marked variability between the adsorption capacities of the tested soil minerals. The Fe and especially Al oxides exhibited the highest maximum adsorption capacity for all OP forms. The specific surface area (SSA) of soil minerals may differently affect their ability to sorb OP compounds. Our result showed that the larger the SSA of soil minerals, the greater their ability to sorb IP forms. However, this was not consistent for the OP compounds. For instance, kaolinite showed greater IHP adsorption than goethite and montmorillonite despite its smaller specific surface area.

The KL value, i.e. the binding-energy-related constant obtained from the Langmuir equation varied in the following order clays << Fe and Al oxides (Table 11). The highest binding energy for adsorbed OP was observed with goethite and the lowest with kaolinite. In addition, the maximum buffering capacity of adsorption (MBC) of the Fe and Al oxides was much larger than for the clay mineral (Table 11). Compared to IP, goethite and montmorillonite are more strongly bonded to OP; however, the opposite was found on gibbsite and kaolinite, which bond IP more strongly than OP.

Therefore, despite the highest OP adsorption capacity of gibbsite, its interaction with OP would be less

Dynamics of Organic Phosphorus Desorption

Role of OP compounds in desorption dynamics

In general, OP desorption by KCl was well fitted with Elovich equation, with determination coefficient from 0.91 to 0.99 (Table 12). In this study, KCl was found to desorb a variable portion of adsorbed OP from the tested OP-mineral complexes. The portion of OP desorbed from all soil minerals was lower than the initially adsorbed OP (Figure 13 and Table 12) which indicates that the adsorption was not fully reversible, as a large amount remained adsorbed. Overall, P desorption was high on the first day (up to 30%) and then slowed down from the second to the fourth day (Figure 13 and Table 12).

The Dm values refer to the predicted maximum desorption capacity of OP obtained from the Elovich model (Table 12). Organic P compounds showed different Dm trends by mineral type. Both G6P and GLY showed higher Dm values (13%-56%) than IHP (3%-14.44%) on Fe and Al oxides. On clay minerals, the pattern was rather opposite, with IHP desorption being higher than other OP forms (Table 12). The desorption maxima of all of the OP compounds were 4%-56%, lower than those of IP which were between 13 % to 70% (Table 12 and Figure 13), showing a general lower desorption of OP relative to IP. However, there were some exceptions with G6P and/or GLY which showed higher desorption than IP on Fe and Al oxides. The amount of OP desorbed could be related to the strength with which it was bound to soil minerals (adsorption parameter KL). The Figure 16 showed negative correlations between Dm and KL, indicating that the amount of OP desorbed tends to decrease with increasing OP binding energy to the soil minerals.

The rate of OP desorbed per day (A) predicted by the Elovich model varied widely for each OPmineral complex (Table 12). Most of OP-minerals complexes showed lower desorption rates per day than IP-minerals. In addition, the different OP-mineral complexes can be classified according to desorption rates into three categories (Figure 14): low desorption rate complexes (<5% per day) which include all the OP desorbed from gibbsite and kaolinite; medium desorption rate complexes (10-20% per day) including IHP and G6P from montmorillonite and high desorption rate complexes (20% > per day) which include only G6P from goethite (Figure 14). Dm: maximum P desorption capacity, A: P desorption rate, B: amount of P desorbed in the first day of desorption in this study (q = A + B * Lnt, B = q when t = 1), R 2 : model fitting degree.

Role of soil minerals in desorption dynamics

There was a large difference between Fe and Al oxides minerals and clays mineral with respect to desorption properties (Table 2 and Figure 13). Phosphate desorption from Fe and Al oxides was very rapid, and equilibrium was attained within 2 days. Except for G6P on goethite, OP desorption from soil minerals at the end of the experiment could be ranked as gibbsite (3-14%) < goethite (13-14%) < kaolinite (5-39%) << montmorillonite (23-45%) (Table 2, Figure 13). Organic P desorption from clays minerals was thus much higher than from Fe and especially Al oxides. This large difference in the capacity of soil minerals to release OP would be related to the physicochemical properties of the soil and the OP. Indeed, our results showed strong negative correlation between the desorption capacity (Dm) and the properties of the soil minerals (PZC and SSA), and the correlation appears to be stronger with PZC (Figure 16).

Successive desorption (Figure 15) using KCl showed that more than 25% of the adsorbed OP (IHP, G6P, GLY) on montmorillonite was desorbed in the first cycle and there was no desorption after 4 cycles. Compared to the clays-IHP complex, P desorbed from Fe, A1 oxide-IHP was lower but declined more slowly with increasing number of cycles (Figure 15). The same trends were observed with the Fe andA1 oxide-GLY complexes. For instance, at the first cycle, more IHP and GLY was and GLY desorbed from the clay minerals was lower or equal to that from Fe and A1 oxides. This suggests that the clays-IHP and GLY complex supplied P rapidly but over a short period whereas the Fe and A1 oxide-IHP and GLY complex supplied P slowly but over a long period. With slight differences, the soil mineral-G6P complexes appeared to show the same trend as mineral-IHP or GLY. As mentioned above for the results of the adsorption mechanisms of montmorillonite, the desorption properties (kinetics, amount and rate of desorption) are also only valid for K-saturated montmorillonite. The linkage is based on the relationships between different variables. The color of each line refers to the degree of relationship between the variables. R² > 0.5

Discussion

Influence of organic phosphorus properties on adsorption and desorption dynamics

Adsorption dynamics of OP compounds play an important role in the potential reactivity of OP in soils amended with organic input. Our results showed the positive relationship between OP adsorption dynamics and the number of phosphate groups of the organic molecule. The higher phosphate group number, the higher the adsorption. Thus, IHP, which has six orthophosphates per C moiety, was adsorbed in larger quantities than the orthophosphate monoesters (G6P and GLY) because it can coordinate with more hydroxyl (OH) groups on the surface of soil minerals [START_REF] Mckercher | Characterization of the inositol penta-and hexaphosphate fractions of a number of Canadian and Scottish soils[END_REF]. The sizes of the C moiety, may be also responsible for the difference in adsorption amount of each OP compounds. Our results about molecular mass effects on OP adsorption dynamics were in disagreement with most studies that found decreases in OP adsorption with increasing molecular mass due to steric hindrance effects (Lü et al., 2017;Ruttenberg and Sulak, 2011). They specifically disagree with those of Lü et al., (2017) who observed that the adsorption maxima of OPs on goethite and hematite were classified as follows: IP > Adenosine monophosphate (AMP) = G6P > ATP, showing a decreasing trend in sorption levels with increasing molecular mass of the different forms of OP. Our results also contrast with those of Yan et al., (2014) where the maximum sorption densities of three Al (oxyhydr)oxides (amorphous Al(OH)3, boehmite and α-Al2O3) increased with decreasing molecular massas follows IHP < ATP < G6P < GLY < IP. However, the results obtained agree with the work of [START_REF] Berg | Sorption Dynamics of Organic and Inorganic Phosphorus Compounds in Soil[END_REF], which showed a trend of increasing rather than decreasing sorption levels with increasing molecular mass of different forms of OP (IHP > G6P > ATP > IP). Similarly, recent work by Ganta et al., (2020) and Ahmed et al., (2021) also supported our results. They demonstrated that the organic fraction of the OP may not influence the interaction of individual phosphate groups with the soil and thus the effect of molecular mass steric hindrance may be insignificant.

After adsorption, the ability of OP compounds to desorb depends not only on their chemical properties but also on the degree of energy with which they are adsorbed onto soil minerals (Ganta et al., 2021(Ganta et al., , 2019)). A general weaker or equal binding strength of IHP compared to GLY or G6P was found. This disagrees with recent results that reported total interaction energies (in absolute value) measured for goethite-IHP complexes (-72 to -85 kcal mol -1 ) higher than those for GLY (-38 to -48 kcal mol -1 ) (Ganta et al., 2019;Kubicki et al., 2012;Rakovan et al., 1999). In addition, this finding also contradicts the extensive literature that associates the large amount of IHP adsorbed with its strong binding to minerals (Celi et al., 2000;Giaveno et al., 2008;Guan et al., 2006;Johnson et al., 2012;Xu et al., 2017). However, this indicates that the higher adsorption of IHP relative to other OP compounds did not necessarily imply that its binding capacity is always strong and stable under all environmental conditions. Thus, we suggest that despite the higher accumulation of IHP reported in most soils (Amadou et al., 2021;Gerke, 2015), its desorption may be easier than that of the GLY or G6P forms, although this depends greatly on the soil minerals and experimental conditions . Furthermore, our results indicated that if both GLY and G6P species compete with IHP for the same active sites on soil minerals, the binding energy of GLY or G6P would be higher than that of IHP. Therefore, one could expect easier desorption of IHP from soil compared to GLY and G6P even though this would be highly dependent on soil minerals.

Influence of soil mineral characteristics on adsorption and desorption dynamics

The tested soil minerals presented a different capacity to sorb OP compounds due to their contrasting physicochemical properties. Fe and Al oxides showed very different OP adsorption mechanisms compared to clays, as the adsorption capacity ranked as follows: kaolinite < montmorillonite < goethite <<< gibbsite. This can be explained by their contrasting types of surface charge. At pH 5.5 (pH used for this study), kaolinite has a small net negative charge, goethite has a small net positive charge and gibbsite is positively charged while montmorillonite is negatively charged according to their PZC values (He et al., 1994;He and Zhu, 1997). Gibbsite exhibited the greatest adsorption maximum, which was probably related to the combined effect of its high surface positive charge and greater SSA (120-364 m 2 g -1 ), as well as the abundance of active adsorption sites, as noted by Shang et al., (1990) and Yan et al., (2014). Manning and Goldberg, (1996) found that gibbsite and goethite adsorbed roughly 23 times more P than kaolinite and up to 53.5 times more IP than montmorillonite and illite. However, despite the highest OP adsorption capacity of gibbsite, its interaction energy with OP would be less strong than IP. The order of the KL value, i.e., binding energy (clays << Fe and Al oxides), suggests a much higher binding energy between OP and Fe and Al oxides than between OP and clays. These results suggest that the mechanism of OP adsorption on Fe and Al oxides is quite different from that on clay minerals. In sum, soil minerals had diverse adsorption mechanisms, specifically Fe and Al oxides compared to clay minerals. The changes in their adsorption and binding capacity to OP compounds were the result of their contrasting physicochemical properties. This may result in different behavior in the desorption of adsorbed OP.

However, since it is well known that the number of positive charges of variably charged minerals (especially Fe and Al oxyhydroxides and kaolinite) decreases with increasing pH, we speculate that their adsorption may decrease at higher pH than that of our study (i.e. pH> 5.5) (Hu et al., 2020b). In addition, it is also known that cations in solution can affect the P sorption potential of certain minerals, e.g., Al

or Ca saturated clay minerals [START_REF] Ellis | Phosphate fixation by montmorillonite[END_REF][START_REF] Peters | Influence of cation saturation on phosphorus adsorption by selected clay minerals[END_REF][START_REF] Prietzel | Reference spectra of important adsorbed organic and inorganic phosphate binding forms for soil P speciation using synchrotron-based K -edge XANES spectroscopy[END_REF]. The next challenge will be therefore to elucidate the role various cations on OP retention by minerals. This could also allow to feed surface complexation models to gain in robustness on the understanding of the adsorption and desorption mechanisms while better predicting P behavior in soils.

The desorption dynamics of the adsorbed OP was markedly affected by both OP and soil minerals characteristics. OP was more desorbed from clays minerals (montmorillonite and kaolinite) than from Fe and Al oxides. Since clays have also been shown to have a lower OP retention capacity, it can be expected that OP will be more available when organic inputs are applied to soils dominated by phyllosilicates, e.g. subtropical and temperate soils (Bortoluzzi et al., 2015;He et al., 1994).

Furthermore, with time, OP desorption kinetics and rate differed between soil minerals. Our findings showed that clays-OP complex released P rapidly but over a short period whereas the Fe and A1 oxide-OP complex released slowly but over a longer period. In the clay-OP complexes, the binding energy would be unstable and its distribution would have varied remarkably with time, probably from looselybound fraction to tightly-bound fraction. In contrasts, Fe and Al oxide-OP complexes were stable with time. These results indicated that each complex would have presented a different binding mechanism, e.g. the inner sphere versus the outer sphere complex with different types of bonds e.g. bidentate versus monodentate (Ganta et al., 2019). Our results highlighted the central role of OPs and their interactions with soil minerals on P availability and potential P loss to water. Better knowledge of these interactions constitutes an important challenge to model OP dynamics and predict P release to plants and waters in soil amended with OP fertilizers. Despite the overall low desorption of OP from Fe and Al complexes, G6P and GLY were however more desorbed from goethite and gibbsite than IP. This weaker retention of these OP forms by Fe and Al oxides suggests that both G6P and GLY could be used in Fe/Al oxide-rich soils to improve P nutrition of plants. This has therefore great implication for P fertilization in highly weathered soils of tropical regions in which Fe and/or Al oxides are dominant. Taken together, our results indicate that both Fe and Al oxides and clay minerals in soil could be either OP sinks or OP sources, depending on their properties, binding energy and adsorption saturation.

It must be noted, however, that soils may contain a much wider variety of Fe and Al oxides than those used in this study, namely goethite and gibbsite respectively. For example, many soils contain significant amounts of ferrihydrite, which was reported to have a higher P sorption than goethite [START_REF] Prietzel | Reference spectra of important adsorbed organic and inorganic phosphate binding forms for soil P speciation using synchrotron-based K -edge XANES spectroscopy[END_REF]Ruttenberg and Sulak, 2011;[START_REF] Prietzel | Phosphorus K -edge XANES spectroscopy has probably often underestimated iron oxyhydroxide-bound P in soils[END_REF]. As an outlook, we strongly suggest studies to understand better the involvement of a wide range of iron oxides in the dynamics of OP forms. More generally, though our results provide a mechanistic understanding of the sorption processes of various OP forms on selected soil minerals, the role of other soil minerals alone or in combination needs still to be investigated to generate a better overview of OP dynamics in real complex soil systems. In addition, it is also important to point out that our results regarding the comparison between the P (de)sorption properties of montmorillonite and other soil minerals are only valid for the K-saturated montmorillonite used here. For Al-or Ca-saturated montmorillonite, a much stronger P sorption or less pronounced P desorption would be expected compared to K-saturated montmorillonite. Furthermore, in agroecosystems, with the exception of periods immediately following heavy K fertilization, K-saturated montmorillonite, which was used here as the montmorillonite type, is rare in most soils. Thus, the results must be considered in light of the type of clay used (K-saturated montmorillonite in this study).

Adsorption and desorption dynamics of OP relative to IP

Compared to IP, IHP was generally more strongly adsorbed whereas the opposite was observed for G6P

and GLY. This result showed that specific forms of OP, depending on their characteristics, had contrasting adsorption dynamics with respect to IP. Therefore, the weaker retention of OP compared to IP which is generally suggested in the literature (Anderson et al., 1974;[START_REF] Condron | Chemistry and Dynamics of Soil Organic Phosphorus[END_REF]Condron et al., , 2005) ) did not apply to all organic P compounds as higher inositol phosphate esters can be strongly retained in soil. [START_REF] Berg | Sorption Dynamics of Organic and Inorganic Phosphorus Compounds in Soil[END_REF] found that soils pretreated with IHP or having combinations of IHP and IP in solution had reduced IP adsorption by successfully competing for binding sites, indicating that there was a preference in the adsorption of IHP over IP. This preference may either lead to the release of already adsorbed IP or prevent further adsorption of IP, leading to an increase in both available IP for plants and soluble IP for runoff [START_REF] Leytem | Sorption of organic phosphorus compounds in atlantic coastal plain soils[END_REF]. Furthermore, in the presence of different OP forms in soils, the preferential adsorption of IHP or IP over both G6P and GLY may increase G6P and GLY availability and promote their mineralization. Thus, this contrasting adsorption dynamics of OP versus IP have important implications for P management from organic input in soils because IHP, GLY and G6P can comprise up to 80% of total P in some organic input (Amadou et al., 2021;Darch et al., 2014;George et al., 2018), and many animal manures, notably those from monogastrics (pigs, poultry), contain substantial quantities of inositol phosphates (Hu et al., 2020a;Peperzak et al., 1959). Application of these manures to agricultural land could, therefore, promote the solubilization of IP and/or reduce the adsorption of G6P and GLY which would then be available for uptake by plants but also released into runoff water [START_REF] Reid | Components of phosphorus loss from agricultural landscapes, and how to incorporate them into risk assessment tools[END_REF]. On most soil minerals, the amount of desorbed OP and the desorbed rate of OP were generally lower than those of IP. After several desorption cycles, [START_REF] Roy | Soil phosphorus sorption capacity after three decades of intensive fertilization in Mato Grosso, Brazil[END_REF] found that 20% of IP desorbed from goethite while it only accounted for less than 5% for OP. Similar findings were reported by [START_REF] Ruyter-Hooley | The effect of humic acid on the sorption and desorption of myo-inositol hexaphosphate to gibbsite and kaolinite: Humic acid affects phytic acid sorption[END_REF] with limited desorption of OP (<3% of total amount) on gibbsite, even in the presence of humic acids as competing ligands for sorption sites. [START_REF] Huang | Hydrolysis of glucose-6-phosphate in aged, acid-forced hydrolysed nanomolar inorganic iron solutions-an inorganic biocatalyst?[END_REF] showed that OP compounds added by organic input may desorb slowly and mineralized in step with plant uptake, even in the long term. However, our results showed that this did not apply to all OP compounds.

Concluding remarks

Moving toward more sustainable sources for managing P nutrition in agroecosystems, OP derived from organic inputs and soil is increasingly considered to complement mineral P fertilizer. However, enhancing OP cycling and availability in soils while reducing OP loss into the environment requires a better understanding of OP adsorption/desorption processes on soil minerals. Factors related to soil properties and OP molecular characteristics directly affect the reactions of OP and its release into the soil. The IHP, GLY and G6P form showed different adsorption processes from each other as well as from the IP form. Our results demonstrated contrasted adsorption capacities between IHP and the other organic P forms (G6P and GLY) relative to IP form, with IHP exhibiting the greatest adsorption capacities. The adsorption capacity of each OP compounds is determined by the number of orthophosphate groups associated with the C moiety in each compound and its size. The general idea of a lower adsorption of OP relative to IP suggested by the literature does not match for all OP compounds since, even though IHP was more strongly retained relative to IP, G6P and GLY were more weakly retained. In general, OP compounds showed less desorption and slower desorption rate per day than IP forms. Fe and Al oxides showed very different OP adsorption mechanisms compared to clays regarding their binding energy and adsorption amount, which were related to different in properties (SSA and PZC). The Fe and especially Al oxides (gibbsite) exhibited the highest maximum adsorption capacity for all OP forms.

The desorption dynamics of the adsorbed OP was markedly affected by both OP and soil minerals characteristics. Montmorillonite showed the highest desorption for OP suggesting higher OP release when organic inputs are applied soils dominated by 2:1 phyllosilicate. However, the results are very dependent on the specific type of montmorillonite used in this study. In fact, the results related to the comparison between the P (de)sorption properties of montmorillonite and other soil minerals are

Role of soil minerals on organic phosphorus availability and phosphorus uptake by plants

Issifou Amadou, Michel-Pierre Faucon and David Houben

Published in Geoderma (September 2022). https://doi.org/10.1016/j.geoderma.2022.116125

Highlights

• Organic P (OP) availability is strongly driven by OP forms and mineral types

• Ryegrass was able to take up about 3-18% of OP adsorbed to soil minerals

• Adsorbed glycerophosphate was more available than the other OP forms

• Montmorillonite-OP showed the highest P uptake and kaolinite-OP the lowest one

• The binding strength of OPs to the mineral surface did not explain P availability

Abstract

Organic phosphorus (OP) represents a significant fraction of the total P pool in soils. With the increasing use of organic resources to substitute mineral P fertilizers and the need to recover P from the soil, it is pivotal to gain insight into the interactions between various OP forms and soil minerals and their consequences on P availability. Here, we aim at elucidating the extent to which OP compounds adsorbed onto major soil minerals may be available to plants. Ryegrass (Lolium multiflorum) plants were grown in RHIZOtest devices in the presence of OP including myo-inositol hexakisphosphate (IHP), glycerophosphate (GLY), and glucose-6-phosphate (G6P) and inorganic P (IP) compounds that were previously adsorbed onto Fe and Al oxyhydroxides (goethite and gibbsite, respectively) and clay minerals (montmorillonite and kaolinite). Phosphorus availability and P uptake were then determined through rhizosphere and plant characterization. Irrespective of the type of mineral, ryegrass was able to take up about 3-18% of adsorbed OP compounds. The magnitude of availability and uptake depended on the OP compounds and the type of soil minerals. The potential availability of OP adsorbed by different minerals was strongly mediated by mineral-OP interaction types and properties. The P uptake increased in the following order: kaolinite-OP << gibbsite-OP ≤ goethite OP << montmorillonite-OP.

Phosphorus uptake from adsorbed OP compounds showed contrasting patterns compared to adsorbed IP and depended more on available P concentration in the rhizosphere rather than on the binding strength of OPs to the mineral surface.

Keywords: Adsorption; desorption; organic phosphorus; phosphorus availability; phosphorus acquisition

Introduction

Phosphorus (P) is a limiting nutrient in both natural and agricultural ecosystems due to its strong sorption with soil particles which limits its availability for plants [START_REF] Fan | Understanding phosphate sorption characteristics of mineral amendments in relation to stabilising high legacy P calcareous soil[END_REF]Hou et al., 2020). The depletion of the world's phosphate rock reserves used to produce mineral fertilizers threatens food security (Filippelli, 2008;[START_REF] Reijnders | Phosphorus resources, their depletion and conservation, a review[END_REF][START_REF] Yu | Sustainable phosphorus supply by phosphorus recovery from steelmaking slag: a critical review[END_REF]. Recycling P from organic input becomes thus a necessity for sustainable P management in agroecosystems (Elser and Bennett, 2011;Houben et al., 2017;[START_REF] Mcgrail | Enhancing agroecosystem phosphorus management: root phenotyping and decomposition for improved phosphorus cycling[END_REF]. However, P contained in organic input and soil occur under various inorganic and organic forms that differ in their availability to plants (Faucon et al., 2015;Kahiluoto et al., 2015).

The predominant organic P (OP) forms in organic input include myo-inositol hexakisphosphate (IHP), glycerophosphate (GLY) and, glucose-6-phosphate (G6P) (Giles et al., 2011;Vincent et al., 2013). Each compound differs from the others in its P content, type of P bond, and size of the molecule (Amadou et al., 2021;[START_REF] Xu | Competitive sorption and accumulation of organic phosphorus in phosphate-rich soils and sediments[END_REF]. These biochemical properties are likely to impact the availability of OP forms to plants as they govern their interactions with the solid phases. Most research on the fate of P applied to soil has focused on inorganic P (IP) compounds, showing that most of it is adsorbed at the surface of soil particles, which in turn influences its availability to plants (Grenon et al., 2021;Hinsinger, 2001;Houben et al., 2011). In contrast, the dynamics of OP forms and their availability have been understudied to date and the contribution of these compounds to plant nutrition is poorly known (Faucon et al., 2015;Haygarth et al., 2018;[START_REF] Mezeli | Soil 'Organic' Phosphorus: An Untapped Resource for Crop Production?[END_REF].

Soil minerals such as iron (Fe) and aluminum (Al) oxyhydroxides (e.g. goethite and gibbsite, respectively) and clay minerals (e.g., kaolinite, montmorillonite) are major components of soils [START_REF] Xu | Competitive sorption and accumulation of organic phosphorus in phosphate-rich soils and sediments[END_REF]. They have received considerable attention due to their high P adsorption capacity (Bortoluzzi et al., 2015;Ryan et al., 2001;[START_REF] Xu | Solution 31P NMR Investigation of Inositol Hexakisphosphate Surface Complexes at the Amorphous Aluminum Oxyhydroxide-Water Interface[END_REF] which may cause an OP utilization efficiency in soils as low as 5-10% (He et al., 1994). This leads to poor utilization of OP sources in agroecosystems (Amadou et al., 2021;Sulieman and Mühling, 2021). Organic P compounds adsorbed on minerals were found to be the most stable P forms in different soil types (Martin et al., 2002;[START_REF] Montalvo | Natural Colloidal P and Its Contribution to Plant P Uptake[END_REF].

This has been attributed to their specific binding mechanism. Indeed, it was found that the number of the phosphate groups in a certain OP compound determines the stability of its complex with the mineral surface (Anderson and Arlidge, 1962;[START_REF] Li | Fate of low-molecular-weight organic phosphorus compounds in the P-rich and P-poor paddy soils[END_REF]. For instance, IHP with its six phosphate groups generally exhibits a strong binding and high stability as compared with other OP or IP compounds which have a smaller number of phosphate groups (Gerke, 2015). Ognalaga et al. (1994) showed that up to four phosphate groups of IHP interact with the goethite surface, leading to the formation of inner-sphere complexes between the IHP phosphate groups and the goethite surface. A similar mechanism has been suggested for other P-mineral complexes. Desorption of P from mineral surfaces would be more limited for OP compounds compared to IP (Bai et al., 2021;Gerke, 2015;Ruttenberg and Sulak, 2011).

However, the extent to which OP compounds adsorbed to soil minerals can desorb remains poorly known and their availability to plants is still debated.

Several authors have suggested that the mineral-OP bridging compounds are not available to plants because these complexes are formed during the slow reaction phase with soil minerals [START_REF] Hingston | ANION ADSORPTION BY GOETHITE AND GIBBSITE: II. DESORPTION OF ANIONS FROM HYDROUS OXIDE SURFACES[END_REF]Barrow and Shaw, 1975). This process has been hypothesized to be a major cause of plant growth limitation (Javaid, 2009). After several desorption cycles, Martin et al. (2002) found that 20% of IP desorbed from goethite while it only accounted for less than 5% for IHP. Similar findings were reported by Ruyter-Hooley et al. ( 2015) with limited desorption of IHP (<3% of total amount) on gibbsite, even in the presence of humic acids as competing ligands for sorption sites. In addition, Gerke (2015) proposed that the presence of Ca in soil solution further reduces IHP solubility and availability due to the formation of Ca-IHP precipitates. These studies suggest that the availability of OP is probably mainly limited by its solubility and not by enzymatic activity (Gerke, 2015;Lung and Lim, 2006). This is corroborated by plant growth tests in the presence of synthetic goethite (Martin et al., 2002) and in Pfixing soils [START_REF] Adams | Availability of organic and inorganic forms of phosphorus to lupins (Lupinus spp.)[END_REF] where sorption and/or precipitation also lowered both IHP solubility and availability. In any case, there was a greater affinity of the OP compounds for soil minerals than that of the IP compounds, indicating the formation of a very stable complex of OPs with mineral surfaces. Thus, it can be expected that desorption and plant availability of mineral-OP complexes are lower than those of IP compounds. However, the very few studies on OP do not adequately quantify their potential contribution to P availability in the organic fertilizer-soil-plant system (Amadou et al., 2021;Klotzbücher et al., 2020;Sulieman and Mühling, 2021). For example, although some studies consider IHP as a source of available P, its availability in the presence of the major soil minerals remains poorly understood (Garcia-Lopez et al., 2015;Martin et al., 2002). Moreover, these studies did not consider other important P pools such as GLY or G6P which, together with IHP, nevertheless represent an important part of the total P in the soil (Darch et al., 2014;[START_REF] Gérard | Clay minerals, iron/aluminum oxides, and their contribution to phosphate sorption in soils -A myth revisited[END_REF]. Furthermore, the soil minerals used were in most cases goethite while Al oxyhydroxides and clays were much less considered (Amadou et al., 2022;[START_REF] Gérard | Clay minerals, iron/aluminum oxides, and their contribution to phosphate sorption in soils -A myth revisited[END_REF]. To our knowledge, there are no study that evaluates and compares the availability of P to plants from the major OP compounds (IHP, GLY, and G6P) that were adsorbed onto the major soil minerals (Fe and Al oxyhydroxides and clay minerals). It is therefore crucial to understand the complex mechanisms that control the dynamics of important compounds of OP in major soils fertilized with organic inputs and the efficiency of the OP-minerals interaction in supplying P to crops.

Overall, our understanding of the dynamics of the major OP pools in the soil-plant system is very limited. Most research has focused on the dynamics of IP forms (Sulieman and Mühling, 2021), suggesting that soil characteristics control their availability to plants (Gómez-Suárez et al., 2020).

However, OP forms may strongly differ from each others and have therefore different biogeochemical processes controlling their availability and uptake by plants (Amadou et al., 2021;Condron et al., 2005).

To date, it is not known how the chemical forms of OPs, and their interactions with soil minerals, influence the uptake of OPs by plants in ecosystems. The paucity of research significantly limits our ability to understand the overall dynamics of P cycling in ecosystems and to optimize the use of renewable P fertilizers which often contain various forms of OP (Kelessidis and Stasinakis, 2012;Mininni et al., 2015). The goal of this study was to elucidate the extent to which OP bound to Fe and Al oxyhydroxides and clay minerals complexes contributes to plant P acquisition. This could open up possibilities for the use of renewable nutrient-rich organic amendments according to different soil mineral properties. Specifically, we determined the plant P availability from several complexes of IHP, G6P, and GLY that were adsorbed onto Fe and Al oxyhydroxides (goethite and gibbsite) and clay minerals (kaolinite and montmorillonite). Mineral-IP complexes with KH2PO4 were also carried out for comparison. The P uptake for each compound was determined using ryegrass grown in an RHIZOtest device. The three main following hypotheses were addressed: (1) P from adsorbed OP compounds is available to ryegrass and varies with soil mineral properties; (2) the relative P uptake of the different complexes OP-minerals are dependent on their binding strength and (3) adsorbed OP compounds are less available than adsorbed IP because it desorbs less and requires not only desorption but also enzymatic cleavage before being taken up by ryegrass.

MATERIALS AND METHODS

Organic P compounds and individual soil minerals

Three OP compounds, including myo-inositol hexakisphosphate (IHP), glycerophosphate (GLY) and glucose-6-phosphate (G6P), and one inorganic P (KH2PO4) were selected for experiments. Organic P compounds were initially selected based on their predominance in organic inputs and soils, the types of P bonds and their different molecular sizes. The inorganic P form was chosen for comparison with organic P compounds. Four minerals were selected to be representative of the predominant minerals in soils: Goethite [Fe (OH)O] and gibbsite [Al(OH)3] were chosen as representative of Fe and Al oxyhydroxides; kaolinite and montmorillonite were selected as clay minerals, particularly 1:1 phyllosilicate and 2:1 phyllosilicate respectively. All mineral powders were obtained from Sigma-Aldrich Chemie and VWR (France) for experimentation.

Preparation of minerals-P Adsorption Complexes

The four soil minerals were loaded with the three OP compounds or inorganic P to serve as a P source for ryegrass. Solutions containing 1 g P L -1 in 0.1 M KCl at pH 5.5 were prepared using the different P compounds. Goethite, gibbsite, kaolinite, and montmorillonite was weighed in portions of 100 g into 1-L bottles. Then, 200 mL of 0.1 M KCl were added and the bottles were shaken for 24 hours at 25 °C to sufficiently hydrate the adsorption sites on the minerals. The pH was maintained at 5.5 ± 0.05 by adding 0.1 M HCl or NaOH solution. To start the formation of OP-mineral complexes, each of the 1 L bottles containing the soil minerals was filled with 800 mL of each P solution. In each bottle containing both the soil minerals and P compounds, some drops of hexanol were added to suppress microbial activities.

Bottles were shaken on a mechanical shaker for 24 hours at 25 °C and then centrifuged (3000 G for 15 minutes). The 1 L bottles were distributed into several 250-mL bottles, centrifuged, and the supernatants were collected and removed. The produced P-loaded minerals were agitated in deionized water and frozen at -20 °C. To determine the amounts of adsorbed P, a certain volume of supernatants was immediately filtered through a 0.22-μm membrane syringe filter for P analysis. The concentration of P in the supernatants was determined colorimetrically (Ohno and Zibilske, 1991) after hydrolyzing OP to IP using the persulfate oxidation method (Peters and Van Slyke, 1932). The quantity of P adsorbed was calculated as the difference between the initial amount of P added and the remaining P amount in the supernatant at the end of the experiment. Total P concentration in a subsample of each P-loaded was also determined using the procedure by Ostrofsky (2012) and showed very similar values compared to the ones determined as the difference between the initial and the final P amount in the supernatant (differences were in the range of 3-5.5% for the organic mineral-P complexes and 1.5-5% for the inorganic mineral-P complexes). The P loadings of the mineral-P complexes produced are shown in Table 13. All minerals were loaded to reach their adsorption maxima. Go: goethite; Gib: gibbsite; K: kaolinite; M: montmorillonite; IP: inorganic P; IHP: Myo-inositol hexakisphosphate, GLY:

glycerophosphate and G6P: glucose-6-phosphate.

Characterization of OP desorption

The desorption ability of various P compounds from soil minerals was characterized using a 0.1 M KCl extraction. Briefly, 40 mL of 0.1 M KCl adjusted to pH 5 were added to 0.5g minerals-P complex.

Samples were then shaken on a mechanical shaker at 25 °C for 24h. After centrifugation for 10 minutes, 5 mL of the supernatant was taken for the measurement of desorbed P concentration by colorimetry (Ohno and Zibilske, 1991). In addition, we carried out two additional desorption steps by successively desorbing P at 48h and 72h using the same extractant to further characterize the desorption dynamics of the P forms.

Experimental Setup and Plant growth

We used the RHIZOtest device (MetRHIZlab, France) (Figure 17) designed by [START_REF] Bravin | RHIZOtest: A plant-based biotest to account for rhizosphere processes when assessing copper bioavailability[END_REF] which consists in separating plant roots from soil with a 30-mm polyamide mesh to facilitate the collection of roots and rhizosphere [START_REF] Houben | Impact of biochar and root-induced changes on metal dynamics in the rhizosphere of Agrostis capillaris and Lupinus albus[END_REF]. As described by Gómez-Suárez et al.

(2020), in a first step (preculture period), 0.20 g of ryegrass (Lolium multiflorum) seeds were grown for 14 days in hydroponics in a cylinder closed at the bottom with a 30 µm polyamide mesh allowing the development of a dense, planar root mat with a nutrient solution: Ca(NO3)2 (2 mmol L -1 ), MgSO4 (0.5 mmol L -1 ), K2SO4 (0.7 mmol L -1 ), KCl (0.1 mmol L -1 ), KH2PO4 (0.1 mmol L -1 ), MnSO4 (0.5 µmol L -1 ), CuSO4 (0.5 µmol L -1 ), ZnSO4 (0.5 µmol L -1 ), (NH4)6Mo7O24 (0.01 µmol L -1 ) and Fe-EDTA (100 µmol L -1 ). After this preculture period, 15 plants were removed from the experiment and the roots and shoots were kept for analysis to determine the amount of P in plants before the cultivation period.

In a second phase (cultivation period), the two-week-old seedlings, showing a dense root mat, were transferred to a thin layer of substrate made of different mineral-P complexes previously prepared and acid-washed quartz. Prior to the experiment, the substrates were sterilized by autoclaving at 121 °C for 2 h (Gómez-Suárez et al., 2020) to eliminate potential microorganisms, allowing therefore to attribute the results to the only effect of root activity. To avoid any P limitation for plants during the experiment, we supplied a total amount of P which was previously found to sufficiently meet the plant requirement in such RHIZOtest devices (Gómez-Suárez et al., 2020). Thus, the amount of mineral-P complex added to the mixture was calculated to supply 40 mg of P in each treatment while the amount of quartz was calculated to reach a final mass of 10 g, which corresponded to a 1.5-mm thick soil layer. The soil layer was then connected to a 500 mL nutrient solution with a filter paper wick. The composition of this nutrient solution was the same as that used for the preculture period except that P was not added. The RHIZOtest devices were placed in controlled conditions (phytotron) under a photoperiod of 12h, constant temperature (25 °C), and relative humidity (80%). Unplanted control treatments, in which the quartz -mineral-P complex had been incubated in similar devices without plants (hereafter called the bulk substrate), were also conducted. In total, 128 such devices were implemented: 4 P compounds (IHP, GLY, G6P, and IP) x 4 soils minerals (goethite, gibbsite, kaolinite and montmorillonite) x 2 crop conditions (ryegrass and bulk soil) x 4 replicates.

Plant sampling and analysis

The plants were harvested after 15 days of contact with mineral-OP complexes. At harvest, shoots and roots were separated and roots were gently rinsed with deionized water. Shoots and roots were then dried at 60 °C for 72 h, weighed, and crushed before analysis. The concentration of P in shoots and roots was determined colorimetrically (Ohno and Zibilske, 1991) after mineralization by 65% HNO3 digestion directly in a microwave Teflon vessel (Lange et al., 2014). The amount of P taken up by shoot and root from the P-mineral complexes was calculated as the difference between the amount of P in plant parts at the end of the experiment minus the average amount of P in plants at the end of the preculture period.

Total plant P uptake from P-minerals was calculated by summing P uptake from P-minerals by roots (i.e., root P concentration multiplied by root dry mass) and P uptake from P-minerals by shoot (i.e., shoot P concentration multiplied by shoot dry mass). The percentage of P recovered by ryegrass was determined by the following equation:

P recovered (%) = Amount of P uptake per pot (mg P) 40 (Amount of P supplied per pot, mg P ) * 100

Rhizosphere and bulk soil analyses

The availability of P in the rhizosphere and the bulk soil collected at the end of the RHIZOtest experiment was assessed by anion exchange membrane (Nobile et al., 2019). Briefly, 0.5 g (mineral-P + quartz) of the collected mineral-P complexes were added to 50 ml bottles with 30 mL deionized water and two strips of anion exchange membrane. The whole set was mixed and stirred for 16 h. The membranes were then removed and rinsed in deionized water and the P recovered by shaking for 1 h in 20 mL of 0.5M HCl. Phosphorus concentrations were analyzed by colorimetry using a spectrophotometer (610 nm). Just after the harvest, alkaline phosphatase activity in the rhizosphere was determined by measuring the amount of p-nitrophenol (PNP) released from the addition of 5 mM pnitrophenyl phosphate according to [START_REF] Tabatabai | Use of p-nitrophenyl phosphate for assay of soil phosphatase activity[END_REF].

Data processing and analysis

Data were statistically analyzed with R software (R version 4.1.3). The impact of factors (P compounds, soil minerals, and their combined effect) on P availability and uptake was modeled by generalized linear models (GLM) using the "FactomineR" package. The GLM model was used to avoid mathematical transformation of the variables and to get rid of the strict assumption that "the residuals will follow a conditionally normal distribution" [START_REF] Mccullagh | Generalized linear models[END_REF][START_REF] Warton | Three points to consider when choosing a LM or GLM test for count data[END_REF] and allow the use of a variety of other distributions of the exponential family for the residuals [START_REF] Cohen | Applied multiple regression/correlation analysis for the behavioral sciences[END_REF]. All factors were tested individually and the models were compared based on second-order Aikake information (AICc), with the lowest relative value being considered the best fit. The ANOVA of the best-fit GLM model with a chi-square test generated the deviance analysis table that gave the significance level of all factors. Statistical analyses to compare the average results of percent P recovered, enzyme activities, and biomass were performed using a one-way analysis of variance (ANOVA) followed by Tukey's honest significant difference (HSD) test (p < 0.05).

RESULTS

Biomass Production

Total biomass varied slightly between treatments (Table 14). Although there was a significant difference between goethite and gibbsite for IHP forms, total biomass did not vary significantly between treatments. Some weak differences were observed between soil mineral types. The lowest biomass was observed with the Gib-OP complex and the highest with the K-OP complex. In general, except on gibbsite, the mineral-OP complexes produced equal or slightly more total biomass than the mineral-IP complexes.

Combined effects of organic P and soil minerals on P uptake

The impact of P compounds, soil minerals, and their combined effect on total P uptake by ryegrass was modeled by GLM (Table 15). Variations in P uptake by ryegrass were significantly affected by P compounds and their interaction with soil minerals. As shown by the lower AIC values (Table 15), the variation was more dependent on the interaction between minerals and P compounds. During the growing season, P recovered by ryegrass was 21-28% from adsorbed IP, 0-5% from adsorbed IHP, 4-18% from adsorbed GLY, and 2-9% from adsorbed G6P, depending on the mineral type (Table 16). glucose-6-phosphate, and IP: KH2PO4); Dashes (-) identify mineral-phosphorus complexes produced by adsorption of forms of P onto soil minerals. The example Go-IHP refers to goethite and myo-inositol hexakisphosphate complexes.

Effect of OP compounds on P uptake by ryegrass

Except for kaolinite, P uptake by ryegrass varied significantly between the adsorbed OP compounds (Table 17; Figure 18). Differences in total P uptake between OP compounds decreased in the order GLY >> G6P > IHP (Table 16; Figure 18). Phosphorus concentrations in roots and shoots were higher in the presence of adsorbed GLY compound compared to the other OP compounds (Table 16; Figure 18). Of all OP compounds, adsorbed IHP was the lowest supplier of P to ryegrass. Compared to IP, P uptake from adsorbed OP compounds was highly contrasted and dependent on the specific compounds of OP.

Phosphorus uptake from adsorbed IHP and G6P was significantly lower than that from adsorbed IP, with the order being: IP >> G6P > IHP (Table 16; Figure 18). However, the trend was different for the adsorbed GLY compound, which, depending on the minerals, was in this order IP = GLY (goethite and montmorillonite) or in this order GLY >> IP (gibbsite). Thus, P uptake from GLY adsorbed on goethite and montmorillonite was similar to the adsorbed IP compound while P uptake from GLY adsorbed on gibbsite was significantly higher than IP. Moreover, P uptake was highly variable and strongly dependent on the characteristics of the OP compounds. Successive desorption of the different mineral-P complexes with KCl (see supplementary data Appendix B Figure S1) also indicated that, in general, the percentage of OP desorption at all cycles was in the order GLY >> G6P > IHP, which was similar to the trend observed for OP availability and uptake by the plant (Figure 18). In addition, the forms of P significantly impacted phosphatase activity in the rhizosphere (Figure 19). Irrespective of the soil minerals, treatments might be ranked according to their phosphatase activity as follows: GLY >> G6P > IHP (Figure 19). In sum, OP adsorbed on soil minerals was available to ryegrass since the plant was able to take up a certain amount of it even if it was relatively low from certain mineral-OP complexes, e.g., mineral-IHP complexes. The effect of P compounds, soil minerals, and their combined effect on total P uptake was significant (P < 0.0001) according to GLM model results testing the impact of factors (P compounds, soil minerals, and their combined effect) on total P uptake.

Relationships between P uptake, soil minerals-OP interaction and P availability

The P uptake was influenced by the soil mineral-OP interactions. Phosphorus uptake from OP adsorbed onto the four tested minerals increased in the following order: kaolinite-OP << gibbsite-OP ≤ goethite OP << montmorillonite-OP. A large difference was observed among kaolinite, Fe and Al oxyhydroxides and montmorillonite in their ability to release P for plant uptake (Figure 18). The amount of P taken up from montmorillonite-OP complexes was the highest. On the other hand, P uptake from goethite-OP, gibbsite-OP, and kaolinite-OP (especially gib-IHP or G6P) was low. Overall, less than 4% of the initial adsorbed P was desorbed and mineralized for plant uptake (Table 16).

Phosphorus uptake by ryegrass from mineral complexes was positively correlated with ΔP resin (R = 0.73, p < 0.01) (Figure 20). However, no correlation was found between P uptake, resin-extracted P concentration in the rhizosphere (Resin P), and KCl-extractable P concentration. In addition, the ΔP resin values of the majority of the mineral-OP were generally negative (Figure 21) even though some complexes, e.g., GLY-mineral complexes, showed almost nil ΔP resin values, i.e., no variation between resin P concentration in bulk soil and resin P concentration in the rhizosphere (Figure 21).

DISCUSSION

Phosphorus from adsorbed OP compounds is available to plants

Our first hypothesis that P from adsorbed OP compounds is available to ryegrass and varies with soil mineral properties was confirmed in our experiment. The two main findings supporting the hypothesis are: (i) the ryegrass was able to take up about 3-18% of OP adsorbed to soil minerals; (ii) OP compounds as well as their interactions with soil minerals significantly affected P uptake for ryegrass.

The amount of P recovered by ryegrass reached 5% from adsorbed IHP, 9% from G6P and 18% from adsorbed GLY (Table 16). In general, P uptake decreased in the order GLY >> G6P > IHP. Taken together, these results indicate that, irrespective of the soil mineral, adsorbed OP was at least partially available to plants. The magnitude of this availability depended on the OP compounds and the types of soil minerals. By comparing several of the main soil mineral-OP complexes, our work indicates that al., 2020; [START_REF] Montalvo | Natural Colloidal P and Its Contribution to Plant P Uptake[END_REF]. Even under conditions where the root-associated microbiomes that can help mobilize P are limited, OP-mineral complexes still have potential for supplying P to plants.

Montmorillonite-OP complexes, in particular, montmorillonite-GLY or G6P were found to serve as sources of P in soils more than the other complexes. Organic P adsorbed on kaolinite released the lowest amount of P to the plants. Overall, there was a marked difference in P uptake between the tested minerals. Montmorillonite-OP complexes would provide more P due to the negative charges of montmorillonite (He et al., 1994) causing its weak binding to OP, resulting in the formation of unstable OP-montmorillonite complexes (He and Zhu, 1998;He et al., 1994;[START_REF] Hingston | ANION ADSORPTION BY GOETHITE AND GIBBSITE: II. DESORPTION OF ANIONS FROM HYDROUS OXIDE SURFACES[END_REF][START_REF] Lang | Soil phosphorus supply controls P nutrition strategies of beech forest ecosystems in Central Europe[END_REF]. The low P uptake from kaolinite-OP agrees with previous observations showing that kaolinite-P is an inner-sphere surface and bidentate complex below pH 6 (Hu et al., 2020;Ruyter-Hooley et al., 2015), and the adsorbed P on kaolinite is difficult to desorb (Kafkafi et al., 1988;Manning and Goldberg, 1996;Xiong et al., 2022). Hence, our result emphasized that Fe and Al oxyhydroxides were less responsible for limiting OP availability than kaolinite despite their general higher adsorption capacity in soil. Apart from the nature of the OP compounds, the characteristic of the minerals are an important factor responsible for the difference in P uptake between the tested OP-mineral complexes. Thus, it is important to further quantify the interaction of OP with soil minerals in order to characterize and subsequently model P availability.

No correlation was found between P uptake and resin-extracted P (Figure 20). In addition, rhizosheath resin P concentration for most mineral-OP complexes was higher than that of the bulk soil.

These results suggest that plants have induced additional desorption of OP. According to Le Chatelier's principle (Law of Mass Action), the sink effect of roots caused an OP depletion in the solution, which in turn induced further OP desorption dissolution to replenish the solution [START_REF] Houben | Zinc mineral weathering as affected by plant roots[END_REF][START_REF] Penn | A Critical Review on Soil Chemical Processes that Control How Soil pH Affects Phosphorus Availability to Plants[END_REF]. In addition, mobilization of OP by ryegrass roots might also have contributed to OP depletion. As shown by Martin et al. (2002), high efficiency of ryegrass in displacing strongly bounded P may be due to the fact that the plant can react to P deficiency by extending the root surface and utilizing more than one mechanism of extraction at the same time. Thus, the effect of plant uptake may result in additional mobilization of OP forms from soil minerals.

It is generally accepted that P extraction with KCl is negatively correlated with the binding energy of the P compounds to soils. Thus, the more P can be extracted with KCl to become available to plants, the lower its binding energy (Martin et al., 2004;Yan et al., 2014). However, our results showed no correlation between P uptake and P extracted with KCl. The lack of correlation in our case may imply that the P taken up by plants did not depend on the strength or energy with which OP compounds are bounded to soil minerals. Nevertheless, this lack of correlation between P taken up by plants and P extracted by KCl could also mean that OP compounds may have been released from the soil minerals but remained in organic form without being mineralized for uptake by plants. Therefore, we hypothesize that although OP was desorbed from some minerals, it may not have been absorbed because it was not readily hydrolyzable by the enzyme released by plant roots. This supports our earlier explanation of the compared to GLY, suggesting that the hydrolysis of IHP to an available IP form was very limited (Figure 19). Finally, we found that the adsorbed GLY compound, depending on the minerals, was almost equivalent or more available than the IP compound. This high availability of GLY could be attributed to its low affinity for soil minerals and especially to its high desorption in soil. Soil amendment with organic inputs with high concentration of GLY would allow the efficient P fertilization from organic waste. This improving of knowledge on OP adsorption by soil minerals therefore reinforces the applications of OP for sustainable alternative to mineral P fertilizer. More importantly, we showed that on Al oxyhydroxides, GLY was significantly more available than IP. Thus, based on comparisons of different P compounds, our results showed that in soil, unlike IHP, another major compound of OP such as GLY can be equal or superior to IP in terms of plant availability.

Conclusion

Our results demonstrate that adsorbed OP compounds may be a source of P for plants irrespective of the type of mineral and its sorption capacity. Higher use efficiency of OP adsorbed on montmorillonite than on other minerals indicates that soils rich in 2:1 phyllosilicate might have greater P availability than soils rich in Fe and Al oxyhydroxides or 1:1 mineral. In addition, GLY would be less affected by Al oxyhydroxides that limit P availability in highly weathered soils in tropical regions. The binding strength of OPs to the mineral surface does not necessarily affect P availability to plants and plant uptake may result in additional P mobilization in the rhizosphere. Finally, the wide range of P uptake and availability in the presence of different mineral-OP complexes emphasized the importance of considering the chemical nature of OP and its ability to interact with soil minerals when attempting to improve soil OP cycling for plant use. As a further step, the role of OP-soil minerals interactions on P availability should be unraveled according to the main plant P acquisition strategies (e.g. mining, foraging and intermediates strategies) to design sustainable P cropping system.

Statements & Declarations

Funding: No received external funding Author Contributions: A. I. prepared and wrote the manuscript; D. H and M. P. defined the outline, main highlights, revisions and suggestions of the manuscript, tables and figures. All authors have read and agreed to the published version of the manuscript.

Declaration of Competing Interest:

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Introduction

Phosphorus (P) limitation and its co-limitation with nitrogen (N) represent a main ecological driver of ecosystem functioning (Hou et al., 2020;Vitousek et al., 2010). The interactions of P with N is a key factor in managing plant P acquisition and agroecosystem productivity. These interactions determine whether plants are limited by P, or N and P together (Long et al., 2016), which in turn influences ecosystem productivity and functioning (Achat et al., 2016;[START_REF] Peñuelas | Human-induced nitrogenphosphorus imbalances alter natural and managed ecosystems across the globe[END_REF]. Worldwide, 32% of the cropland and 43% of the pasture are estimated to be P deficient and require increased P availability and fertilization to improve yields and ensure global food security [START_REF] Lun | Global and regional phosphorus budgets in agricultural systems and their implications for phosphorus-use efficiency[END_REF]. As a result, the increasing global demand for P in a world where soils are enriched with N is creating an N: P imbalance that can lead to significant changes in ecosystems and limit the development of natural ecosystems and agricultural production in the future. According to the theory of ecological stoichiometry, plant growth rate is determined by a specific ratio of RNA to protein which is reflected by the plant N:P ratio (Elser et al., 2010). This ratio is usually recognized as an indicator of P or N (co-)limitation (Vitousek et al., 2010). For instance, extensive researches have shown that P limitation occurring under N addition is reflected by an increased plant N:P ratio which is due to the enhanced production of N-rich protein compared to P-rich ribosomal RNA (Peng et al., 2019). Nevertheless, multiple mechanisms depending on soil properties [START_REF] Craine | Plant nitrogen and phosphorus limitation in 98 North American grassland soils[END_REF], N and P chemical forms, their availability and uptake by plants can mediate the N-induced P limitation. Nitrogen addition affect P uptake by plants directly by promoting plant growth and the production protein [START_REF] Sardans | Changes in nutrient concentrations of leaves and roots in response to global change factors[END_REF][START_REF] Yue | Effects of three global change drivers on terrestrial C:N:P stoichiometry: a global synthesis[END_REF], but also indirectly by interacting with P pools in soil (Long et al., 2016;Schleuss et al., 2020). In particular, it is well known that depending on its inorganic form in the soil solution (i.e. NH4-N or NO3-N), N may increase or decrease P solubility, resulting in changes in P limitation and availability [START_REF] Lü | Convergent responses of nitrogen and phosphorus resorption to nitrogen inputs in a semiarid grassland[END_REF]Peng et al., 2019). For instance, plant-induced decrease in soil pH caused by NH4-N nutrition increases the solubility of poorly soluble P pools in alkaline soils, resulting in greater P availability compared to the supply of NO3-N (Gómez-Suárez et al., 2020;Wang et al., 2012) while the opposite occurs in acidic soils (Hinsinger, 2001). Overall, it has been stated that plants could trade N for P by adjusting N and P acquisition rates from the soil, potentially explaining the synergistic growth responses to N and P addition (Long et al., 2016;Peng et al., 2019;Schleuss et al., 2020). Furthermore, depending on P availability, the effect of N may be more or less pronounced, resulting in differential P limitation between IP and OP forms.

Benefits of N addition on P cycling are highly dependent on characteristics of the minerals involved (Deng et al., 2017;Hou et al., 2020;Vitousek et al., 2010). For example, it is shown that in Luvisols and Calcosol (soil rich in calcium, with neutral or basic pH), P mobilization increases with NH4-induced pH decrease, whereas NO3-induced pH increase had no effect. In contrast, in Oxisols (soil rich in Fe and Al oxides, with acidic pH ), a similar decrease in pH caused by NH4-N nutrition had no effect, whereas the increase in pH caused by NO3-N markedly increased soil P mobilization [START_REF] Gahoonia | Mobilization of phosphate in different soils by ryegrass supplied with ammonium or nitrate[END_REF] clay mineral, specifically the 1:1 phyllosilicate. All minerals were obtained from Sigma-Aldrich Chemie S.a.r.l. and VWR (France) for the experiment. The two forms of nitrogen used were ammonium (NH4-N) provided as (NH4)2SO4 and nitrate (NO3-N) provided as Ca (NO3)2.

Preparation of Goethite-P and Kaolinite-P Adsorption Complexes

The minerals (goethite and kaolinite) were loaded with the three compounds (IHP, GLY, and IP) to serve as a source of P for ryegrass. Solutions containing 1g L -1 P in 0.1 M KCl at pH 5.5 were prepared using the individual P compounds. The minerals were weighed in 100g portions into 1-liter bottles.

Then, 200 ml of 0.1 M KCl was added and the bottles were shaken for 24 hours at 25°C to sufficiently hydrate the adsorption sites. The pH was maintained at 5.5 ± 0.05 by adding 0.1 M HCl or NaOH solution. To begin the formation of P-mineral complexes, each of the 1-L bottles containing the soil minerals was filled with 800 mL of each P solution. Then, a few drops of hexanol were added to suppress microbial activities. The bottles were shaken on a mechanical shaker for 24 hours at 25°C and then centrifuged (3000 G for 15 minutes). The 1-L bottles were divided into several 250-mL bottles, centrifuged, and the supernatants were collected and disposed of. The P-laden minerals produced were shaken in deionized water and frozen at -20•C. To determine the amounts of adsorbed P, a certain volume of supernatants was immediately filtered through a 0.22-μm membrane syringe filter for P analysis. The concentration of P in the supernatants was determined by colorimetry (Ohno and Zibilske, 1991) after hydrolysis of IHP and GLY to IP by the persulfate oxidation method (Peters and Van Slyke, 1932). The amount of P adsorbed was calculated as the difference between the initial amount of P added and the amount of P remaining in the supernatant at the end of the experiment. The P loadings of the mineral-P complexes produced are shown in Table 18. All minerals were loaded to reach their adsorption maxima.

Table 18 : P adsorption capacity of the produced minerals-P adsorption complexes

Go: goethite; K: kaolinite; IP: inorganic P; IHP: myo-inositol hexakisphosphate, GLY: glycerophosphate and G6P: glucose-6phosphate.

Mineral-P complexes Quantity of P adsorbed (µg g -1 )

Go-IP 2810

Go-IHP 3742

Go-GLY 1398 K-IP 1736 K-IHP 6082 K-GLY 1222

Experimental Setup and Plant growth

We used a device whose principle is very similar to the RHIZOtest (Figure 22) except that here, the roots of the plants are not separated from the soil but remain separated from the nutrient solution. In a first step (preculture period), 0.20 g of ryegrass (Lolium multiflorum) seeds were grown for 14 days in hydroponics in a cylinder closed at the bottom by a screen allowing the development of the roots with a nutrient solution: Ca (NO3)2 (2 mmol L -1 ), MgSO4 (0.5 mmol L -1 ), K2SO4 (0.7 mmol L -1 ), KCl (0.1 mmol L -1 ), KH2PO4 (0.1 mmol L-1), MnSO4 (0.5 µmol L -1 ), CuSO4 (0.5 µmol L -1 ), ZnSO4 (0.5 µmol L -1 ), (NH4)6Mo7O24 (0.01 µmol L -1 ) and Fe-EDTA (100 µmol L -1 ). In a second phase (culture period), the two-week-old seedlings were transplanted into polystyrene cylinder pots (125 ml volume) containing the growth media. The growing media consisted of a mixture of the previously prepared P-mineral complexes mixed with acid-washed quartz. Before the experiment, the quartz was sterilized by autoclaving (Gómez-Suárez et al., 2020) at 121 °C for 2 h in order to eliminate potential microorganisms, thus allowing the results to be attributed to the effect of root activity alone. In addition, to avoid any P limitation for the plants during the experiment, we provided a total amount of P that was previously found to be sufficient to meet the plants' needs (Gómez-Suárez et al., 2020). Thus, the amount of mineral-P complex added to the growing medium was calculated to provide 10 mg of P in each treatment while the amount of quartz was calculated to reach a final mass of 100 g in each pot. Then the pots containing the plants and growing medium were nested into other 250 ml cylinder pots containing a nutrient solution with a filter paper wick. The composition of this nutrient solution was the same as that used for the preculture period, except that P was not added and N was added as Ca (NO3)2 (4 mmol L -1 ) or (NH4)2SO4 (4 mmol L-1). To make the amounts of Ca equal between the NO3-N and NH4-N treatments, CaCl2 was added to the NH4-N treatment. The devices were placed under controlled conditions (phytotron) under a 12h photoperiod, constant temperature (25 °C) and relative humidity (80%). Non-planted control treatments, in which the quartz-mineral-P complex was incubated without plants (hereafter called bulk substrate), were also performed. A total of 96 such devices were implemented: 3 P compounds (IHP, GLY and IP) x 2 soil minerals (goethite and kaolinite) x 2 forms of nitrogen (NO3-N and NH4-N) x 2 cropping conditions (ryegrass and bulk soil) x 4 replicates.

Plant sampling and analysis

The plants were harvested after 20 days of contact with mineral-P complexes. At harvest, shoots and roots were separated and roots were gently rinsed with deionized water. Shoots and roots were then dried at 60 °C for 72 h, weighed and crushed prior to N and P analysis. The concentration of P in shoots and roots was determined calorimetrically (Ohno and Zibilske, 1991) after mineralization by 65% HNO3 digestion directly in a microwave Teflon vessel (Lange et al., 2014). In addition to P analysis, the N elemental concentrations were determined. We calculated N:P ratios by dividing leaf N concentration by leaf P concentration (both as percentage nutrient in the sample) within each plant tissue sample. Total plant P uptake was calculated by summing P uptake by roots (i.e., root P concentration multiplied by root dry mass) and P uptake by shoot (i.e., shoot P concentration multiplied by shoot dry mass).

Soil Analyses

At the completion of the experiment, cropped soil (i. e., rhizosphere) and the uncropped soil (i. e., bulk soil) were collected and dried at ambient temperature. In accordance with the scheme proposed by DeLuca et al. (2015), each soil sample was subjected to CaCl2 extraction (0.01 mol L -1 ), which extracts soluble and weakly adsorbed inorganic P and emulates accessible P by interception and root diffusion.

One g of soil was transferred to a polypropylene centrifuge tube to which 20 mL of 0.01 mol L -1 CaCl2

was added and shaken for 3 h in a reciprocal shaker at 200 rpm at 20 •C. After shaking, the pH (pH-CaCl2) was measured in the suspension and the extract was separated from the solid residue by centrifugation at 3000g for 15 min. In the extract, P concentrations were analyzed colorimetrically [START_REF] Murphy | Phosphorus speciation in temperate basaltic grassland soils by solution 31P NMR spectroscopy[END_REF] using a spectrophotometer (610 nm). ΔpH between rhizosheath and bulk soil from unplanted pots postgrowth was then calculated.

After defrosting some samples, acid phosphomonoesterase activity in the rhizosheath (PME)

was measured with a modified buffer at pH 6.5 [START_REF] Tabatabai | Use of p-nitrophenyl phosphate for assay of soil phosphatase activity[END_REF]. Briefly, phosphatase activity was assessed via production of pnitrophenol from sodium p-nitrophenyl phosphate during a 1 h incubation at 37 °C with 0.5 g dry soil, 0.2 mL toluene, 4 mL modified buffer and 1 mL substrate.

pNitrophenol release was determined spectrophotometrically at 410 nm after stopping the reaction with 4 mL 0.5 M NaOH and 1 mL 0.5 M CaCl2 and filtering.

Data processing and analysis

All statistical analyses were performed using R software version 3.5.0 and the package Rcmdr. The impact of factors (soil minerals, P compounds, N forms, and their combined effect) on P availability and uptake was modeled by generalized linear models (GLM) using the "FactomineR" package. The GLM model was used to avoid mathematical transformation of the variables and to get rid of the strict assumption that "the residuals will follow a conditionally normal distribution" [START_REF] Mccullagh | Generalized linear models[END_REF][START_REF] Warton | Three points to consider when choosing a LM or GLM test for count data[END_REF] and allow the use of a variety of other distributions of the exponential family for the residuals [START_REF] Cohen | Applied multiple regression/correlation analysis for the behavioral sciences[END_REF]. All factors were tested individually and the models were compared on the basis of second-order Aikake information (AIC), with the lowest relative value being considered the best fit. The anova of the best-fit GLM model with a chi-square test generates the deviance analysis table that gives the significance level of all factors. Statistical analyses to compare the average results of N:P mass ratio, P uptake, enzyme activities, and biomass were performed using a one-way analysis of variance (ANOVA) followed by Tukey's honest significant difference (HSD) test (p < 0.05). As recommended by Schabenberger and Pierce, ( 2001), the results of ANOVA were presented by showing the degree of freedom (Df), F-ratio (F, i.e., the between-group variance divided by the within-group variance) and p-value (i.e., the lowest probability level at which the means are considered significant).

Results

The best model fit that most affected N:P ratio, total P concentrations, and total ryegrass biomass were obtained with the interaction of all factors, i.e., N x minerals x P forms, rather than their separate effects (Table 19, highest LR Chisq of 20.9 for N:P and lowest AICc values of -35 and -172 for P uptake and total biomass, respectively).

Total biomass increased with N addition to an extent dependent on the mineral-P complexes (Figure 23). The N:P ratio values varied markedly among treatments, ranging from a minimum value of 2.5 ± 0.42 to a maximum value of 32.31 ± 2.00 (Figure 24). Except for K-Gly, the N:P ratio was below 12 without N addition, reflecting N limitation (Figure 24). With N addition, the N:P ratio increased irrespective of the mineral-P complex. It shifted from N limitation to N and P co-limitation in the presence of mineral-IP complexes (N:P = 14.8-15.8) and to P limitation in the presence of mineral-OP complexes (N:P = 19.12-32.2). The addition of both N forms increased the N:P ratio in a similar way except in the Go-IHP treatment where NO3-N significantly increased the N:P ratio compared to NH4-N (Figure 24). Between minerals, the N-induced increase in N:P ratio was significantly higher on goethite than on kaolinite (Figure 24 and Table 19). Similar to N:P, total P uptake differed markedly between mineral-P complexes (Figure 25 and Table 20). With N addition, more P was absorbed by the plant and P in mineral-IP complexes was significantly more available than mineral-OP sources (Table 20). This was evidenced by the discrepancy between the percentage of P recovered without N (≤ 12%) and with N (≤ 25%). In the presence of mineral-IP complexes, the addition of NO3-N significantly increased P uptake compared to NH4-N (Figure 25); however, no significant difference was found between the two N forms for mineral-OP complexes (except on Go-GLY). The mineral type had little influence on Ninduced P uptake, except for K-GLY which showed significantly higher P uptake than Go-GLY. In general, P uptake from mineral-P complexes after N addition showed the following trend: mineral-IP >>> mineral-IHP > mineral-GLY (Figure 25 and Table 20). Furthermore, we found that foliar N (Figure 26a) and P (Figure 26b) increased significantly with the N addition, and varied with the mineral-P complexes.

Rhizosphere properties were affected by N forms and their interactions with mineral-P complexes. Rhizosphere pH showed a significant increase with NO3-N but decreased significantly with NH4-N (Figure 26c). The addition of N significantly increased soil phosphatase activities, the highest activities being detected in the presence of mineral-OP complexes (Figure 27). However, the available P pool in the rhizosphere was significantly decreased with N addition (Figure 26d). Plant N:P ratio showed a positive correlation with soil phosphatase activities and foliar N and a negative correlation with soil available P concentration (Table 21). Total P uptake was positively related to available P concentration, phosphatase activity, and foliar N. Foliar P was also positively correlated with foliar N.

Overall, no parameter was correlated with rhizosphere pH (Table 21). The interaction effect of N, P compounds, soil minerals on N:P ratios was significant (P < 0.001) according to GLM model results testing the impact of factors (N forms, P compounds, soil minerals, and their combined effect). Means with different letters were significantly different according to Tukey's HSD test at P < 0.05. Error bars indicate standard error. N forms (NO3-N: nitrate and NH4-N: Ammonium); Soils minerals (Go: goethite and K: kaolinite); Phosphorus compounds (IHP: myo-inositol hexakisphosphate, GLY: glycerophosphate and IP: KH2PO4); The dashes (-) identify the mineral-phosphorus complexes produced by the adsorption of P forms onto soil minerals. Example Go-IHP refers to goethite and myo-inositol hexakisphosphate complexes. The N:P ratio has been used to indicate plant N or P limitation conditions i.e., N limitation when N:P < 12, P limitation when N:P > 16 or 20 and NP co-limitation between 12 and 16 or 20 [START_REF] He | Leaf nitrogen and phosphorus of temperate desert plants in response to climate and soil nutrient availability[END_REF][START_REF] Koerselman | The Vegetation N:P Ratio: a New Tool to Detect the Nature of Nutrient Limitation[END_REF][START_REF] Zheng | Altered leaf functional traits by nitrogen addition in a nutrient-poor pine plantation: A consequence of decreased phosphorus availability[END_REF]. The interaction effect of N, P compounds, soil minerals on total P uptake by ryegrass was significant (P < 0.001) according to There is evidence from literature that N addition may increase plant P demand which, in turn, promotes soil P mobilization (Schleuss et al., 2020;[START_REF] Yue | Effects of three global change drivers on terrestrial C:N:P stoichiometry: a global synthesis[END_REF][START_REF] Zhan | Nitrogen enrichment alters plant N: P stoichiometry and intensifies phosphorus limitation in a steppe ecosystem[END_REF]. This highlights the ecological importance of the beneficial effect of N on P use efficiency by plants (Vitousek et al., 2010).

Our results suggest that N addition increased plant P limitation in all treatments (Figure 24), as well as a further increase in plant P uptake (Figure 25) via altered rhizosphere chemistry (Figure 26c,d). The addition of NH4-N or NO3-N resulted in a decrease or increase in pH, respectively (Figure 26c).

Accordingly, the shift of plants from N limitation to N and P co-limitation or P limitation (and the associated increase in P uptake) would result from the impact of N addition in stimulating rhizosphere processes involved in P mobilization/acquisition (Schleuss et al., 2020;[START_REF] Zhan | Nitrogen enrichment alters plant N: P stoichiometry and intensifies phosphorus limitation in a steppe ecosystem[END_REF],, which is consistent with our second hypothesis.

Our results regarding the trend of N:P ratio without N (mineral-IHP < mineral-GLY) and with N (mineral-IHP > mineral-GLY) suggest that the addition of N would promote the mobilization of IHP (main forms of OPs) and make it less plant-limiting compared to other forms of OPs, highlighting the pivotal role of the interaction between N, P, and minerals on the OP cycle [START_REF] Craine | Plant nitrogen and phosphorus limitation in 98 North American grassland soils[END_REF]Hou et al., 2021). In addition, these results highlight a new mechanism by which N inputs could accelerate the cycling of OPs, particularly by increasing the availability of IHP (the most accumulated OP in the soil), and thus delay the onset of P limitation of this form for plant growth. In conclusion, the benefits of N addition on P limitation depend strongly on its interaction with P forms and the characteristics of the minerals involved. With the addition of N, more P can be recycled from the clay minerals (kaolinite) and thus delay P limitation as compared to iron and aluminum oxides (goethite).

The magnitude of P limitation resulting from the interaction of N with OP forms relative to that with IP forms provides insight into the consequences of organic fertilization on P cycling dynamics in some OPrich tropical soils and in N-fertilized agroecosystems. The increase in plant P uptake with the addition of N, particularly with the NO3-N forms (Figure 25), highlights the synergistic effects of N and P and their interactions with minerals on P dynamics, i.e., P availability and limitation. High phosphatase activity (Figure 27) , and the availability of P in the rhizosphere (Figure 26d) with N addition likely contributed to plant P uptake, as both increase the possibility that a phosphatase enzyme meets an OP compound and catalyzes its hydrolysis from the minerals [START_REF] Craine | Plant nitrogen and phosphorus limitation in 98 North American grassland soils[END_REF]Long et al., 2016).

Consistently, correlations indicated that total P uptake was positively related to available P and phosphatase activity (Table 21). Most likely, the addition of N allowed plants to synthesize N-costly phosphatases (Schleuss et al., 2020), which then made OP available for plant uptake [START_REF] Helfenstein | Estimates of mean residence times of phosphorus in commonly-considered inorganic soil phosphorus pools[END_REF]. Thus, it seems likely that with the addition of N, P is more intensively recycled from the IP and OP pools, irrespective of the soil minerals (Widdig et al., 2019). However, the lower P uptake found in the presence of mineral OP complexes in spite of the addition of N, (Figure 25) could be a result of their low desorption rate relative to IP (Amadou et al., 2021;Amadou et al., 2022 ) (Figure 26d) and because once desorbed, OPs require enzymatic cleavage before being taken up by the plant (Klotzbücher et al., 2020). The correlations between plant N and P nutrition, available P and phosphatase activity (Table 21) indicated that increases in N:P ratio and P uptake may be accounted for by the significant changes in soil properties. In this study, N addition increase phosphatase activity (Figure 27) and decreased available P (Figure 26d) and, both were significantly related to plant N:P ratio and P uptake (Table 21),

suggesting that in OP sources, available P and phosphatase activity influences plant P uptake and P limitation. The decrease in available P with N addition in the rhizosphere (Figure 26c) may result from greater P uptake and probably lower replenishment of the available P pool from the mineral-P complexes [START_REF] Lund | Effects of N and P fertilization on the greenhouse gas exchange in two northern peatlands with contrasting N deposition rates[END_REF][START_REF] Sardans | The Role of Plants in the Effects of Global Change on Nutrient Availability and Stoichiometry in the Plant-Soil System[END_REF]. Recent studies also showed that the addition of N has influence on rhizosphere properties [START_REF] Marklein | Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems[END_REF][START_REF] Zheng | Altered leaf functional traits by nitrogen addition in a nutrient-poor pine plantation: A consequence of decreased phosphorus availability[END_REF], and in low P ecosystems, the available P could decrease leading to more P limitation for plant primary productivity [START_REF] Lü | Convergent responses of nitrogen and phosphorus resorption to nitrogen inputs in a semiarid grassland[END_REF]. Thus, our results suggest that N supply to plants has the potential to increase P uptake from both mineral-IP and OP complexes, thereby altering plant P limitation. We found that supplying the NO3-N form to plants increased plant P uptake and availability and, to some extent, greater P limitation compared to supplying NH4-N (Figure 24 and 25). This suggests that it was not through alterations in rhizosphere pH that the form of N affected P uptake by the plant.

Key role of soil minerals in P limitation under different N forms additions

Our results showed no significant variation in the N:P ratio of plants between the two N forms, i.e. NO3-N and NH4-N, although NO3-N seems to induce a greater P limitation on some complexes (Figure 24).

In the presence goethite-P complexes, the plant was significantly more P-limited (higher N:P ratio) than in kaolinite-P mineral complexes (Figure 24). These results agree with our third hypothesis that the degree of P limitation would vary significantly between mineral types and P forms due to the contrasting physicochemical properties of the minerals used (Bai et al., 2021;Yan et al., 2014) and the biochemical nature of the P sources (Amadou et al., 2021;Anderson, 1980;Condron et al., 2005). In agreement with the literature, we found in a recent study that, compared to kaolinite, goethite had very low P desorption dynamics (Amadou et al., 2022). Similarly, other studies found greater P limitation in the presence of iron and Al oxides than in the clay minerals (Bortoluzzi et al., 2015;Celi et al., 1999).

Conclusions

In this study, we tried to unravel the biogeochemical processes involved in P limitation by characterizing the role of N and P forms and their interaction with soil minerals on P availability. Interactions between N forms, P forms, and soil minerals strongly altered P dynamics, as compared to individual effects.

These interactions increased plant P limitation and P uptake via modification of rhizosphere chemistry.

The extent of P limitation was strongly dependent on the degree of availability of P sources. Therefore, we found that the interaction of N with IP forms led to greater P uptake and a marked reduction in P limitation compared with the interaction of N with OP. Thus, we inferred that in addition to the degree of P availability, the characteristics and biochemical nature of the P sources determine the degree of P limitation in plants. Furthermore, we found with the addition of N, more P was recycled from clay minerals and P limitation was delayed compared to iron oxides.

Our results highlight the ecological importance of the benefit of N and its interaction with soil minerals on P use efficiency by plants. This study, therefore, provides important information on ecosystem P cycling under N addition and the biogeochemical properties involved, which will allow ecosystem models to accurately predict plant N-P limitation and its impacts, and will also help build robust ecosystem models with fully coupled N-P or C-N-P interactions. Future perspectives will be to understand the effects of N-P-mineral interactions on P limitation in other plant species with contrasting P acquisition strategies (Fabaceae, Brassicaceae...). Then, the scale could be extended to plant communities and ecosystems based on the trait approach of plants and minerals, and N and P chemical forms.

Role of phosphorus-acquisition strategies on organic P mobilization and acquisition

Issifou Amadou, David Houben and Michel-Pierre Faucon

Abstract

Plant P acquisition strategies (i.e., foraging and mining) are generally considered to have access to legacy P pools in the soil. However, compared to inorganic P, the impact of these strategies in soil amended with various forms of organic P (OP) has received much less attention. The purpose of this study was to examine the response of P acquisition strategies toward forms of P (IP and OP) in interactions with soil minerals and their consequences for OP availability and P acquisition. We characterized P acquisition strategies in eight plant species from diverse phylogenetic lineages known with contrasting P acquisition traits that were cultivated under several complexes of IP and OP (IHP, and GLY) adsorbed on Fe oxyhydroxides (goethite) and clay minerals (kaolinite). Results showed an important plasticity of root traits in response to IP and OP forms. P acquisition traits of the species changed between application of the OP forms and application of the IP form. A difference in trait responses was also observed between the specific OP forms, i.e. IHP and GLY. Phosphorus-acquisition traits were generally more prominent on the OP forms than on the IP form. The positive response of P acquisition strategies to OP sources resulted in greater availability and acquisition of P from OPs.

Species were found to have contrasting responses between P forms. Vicia faba and Pisum sativum had significantly higher P acquisition from the OP forms, while Lolium perenne had a higher overall P uptake on the IP form. On the other hand, Lens culinaris, Hordeum vulgare and Trifolium alexandrinum had an overall equivalent P acquisition between P forms. Compared to strategies involving P foraging, those involving P mining resulted in greater P acquisition from OPs. Crops employing intermediate strategies (involving both P acquisition strategies) also showed important P acquisition. Nevertheless, modeling results showed that phosphorus uptake was better predicted by root morphological traits than root physiological traits. This study showed that the positive response of P acquisition strategies to OP forms led to P acquisition from OPs, thus potentially improving the use of renewable OP resources via optimization of crop combinations and the type of P fertilizer applied.

Introduction

Soil phosphorus (P) deficiency limits the productivity of many agroecosystems (Filippelli, 2008;Jarvie et al., 2019). Modern agricultural practices depend heavily on mineral fertilizer derived from mined phosphate rock, a finite and steadily declining resource (Sulieman and Mühling, 2021). To meet plant P requirements and sustain the growing population and food needs, new strategies that can provide available P for plants while limiting the use of mineral P fertilizers are urgently needed (Faucon et al., 2015;Houben et al., 2019). One solution is to recycle P from P-rich organic wastes (Amadou et al., 2021;Sulieman and Mühling, 2021). However, P in organic wastes is a mixture of organic and inorganic P forms, in various proportions depending on their characteristics. Major organic (OP) compounds found in soil and organic waste include inositol hexakisphosphate, IHP [START_REF] Turner | Genetic variability for root hair traits as related to phosphorus status in soybean[END_REF]Vincent et al., 2013), glycerophosphate, GLY (Doolette et al., 2011;Newman and Tate, 1980), and glucose-6phosphate, G6P (Deiss et al., 2018). Inorganic forms of P (IP) include calcium phosphates and amorphous P bound to aluminum or iron. These forms have been found to be unavailable to plants due to their strong adsorption to soil minerals (Amadou et al., 2022;[START_REF] Barrow | A mechanistic model for describing the sorption and desorption of phosphate by soil[END_REF], which is considered one of the main causes of P limitation for plants (Javaid, 2009). However, these poorly available forms of P in soil or organic wastes can be mobilized by some plants in P-deficient soils (Amadou et al., 2021;Honvault et al., 2020).

Several direct and innovative approaches have been identified to improve the mobilization and acquisition of OP forms by plants. These include the identification and selection of crop species/genotypes based on their functional traits (Faucon et al., 2015;Nobile et al., 2019). This approach uses morphological, architectural (Lynch, 2015;Nielsen et al., 1998) and physiological traits (Richardson et al., 2009;[START_REF] Yadav | Adsorptive removal of phosphate from aqueous solution using rice husk and fruit juice residue[END_REF]Zhu et al., 2005), microorganisms or a combination of both to access sparingly available OP forms. In general, these traits could be categorized into three types of P acquisition strategies: foraging, mining and collective microbial-root strategy (Amadou et al., 2021).

The plant P-foraging strategy is the acquisition of P in the soil solution through morphological and architectural traits by maximizing soil exploration. Through these strategies, plants can induce a diffusion gradient which in turn would favor the desorption process of the different adsorbed OP forms [START_REF] Fang | Phosphorus adsorption onto clay minerals and iron oxide with consideration of heterogeneous particle morphology[END_REF]White and Hammond, 2008). Foraging strategy involves morphological traits such as specific root length, fine root percentage and root surface area, and architectural traits including root length density, root biomass, and the formation of clustered roots or arbuscular mycorrhizal symbioses that allow plants to increase their foraging capacity (Haling et al., 2018). The plant P mining strategy, is the acquisition of P in the soil solution through physiological traits that are released into the soil from the roots, including carbohydrates, organic and amino acids, phenolic compounds, proteins, fatty acids, sterols, enzymes, polysaccharides, and phospholipids (Guppy et al., 2005;Weisskopf et al., 2006). The collective microbial-root strategy refers to the investment of resources by plants to interact with the microbial community to access OP in soil.

Different P-mobilization and -acquisition strategies in crop species and cultivars have been highlighted, but their efficiency to acquire P from different OP and IP forms remains poorly studied [START_REF] Lambers | Plant nutrient-acquisition strategies change with soil age[END_REF]Turner, 2008). A recent study of [START_REF] Ceulemans | Phosphorus resource partitioning shapes phosphorus acquisition and plant species abundance in grasslands[END_REF] showed that some grassland species had preferential P acquisition from a P source over another, either OP or IP, while others showed equal P acquisition of both P sources. These authors also showed that P acquisition of some grassland species was more efficient when multiple P sources were added to the soil, the addition of both OP and IP to the soil inducing a higher shoot P content than the addition of one form only. There may also be trade-offs between physiological and morphological traits (Lambers et al., 2006), These trade-offs have been examined very recently in different crop families and species (Honvault et al., 2020). Trade-offs between thicker and thinner roots were observed (Honvault et al., 2020), with thicker roots showing greater carboxylate release or phosphatase activity in the rhizosphere. Trade-offs and coordination between traits were strongly influenced by soil type. However, their effect on the availability of OP forms must still be elucidated (Honvault et al., 2020;Wen et al., 2019).

Several plant species are presumed to be relatively efficient in OP utilization without assistance from rhizosphere microbiome. Some barley species with different root traits could easily access and mobilize twice as much OP as Prunus laurocerasus in low P soil (Bates and Lynch, 2000). Numerous plant species belonging to the family Fabaceae have been classified as efficient P solubilizers (Schneider et al., 2019). Chickpea, which appears to produce both phosphomonoesterases and diesterases, is thought to improve it P nutrition, probably through mining and mineralization of OP forms in soil (Darch et al., 2018;Pang et al., 2010). Various studies have demonstrated that plants have limited ability to access OP in the form of IHP (the main form of OP) due to its low availability in soil solution and low level of extracellular phosphatase or phytase [START_REF]Differential interaction of Aspergillus niger and Peniophora lycii phytases with soil particles affects the hydrolysis of inositol phosphates[END_REF]Richardson et al., 2009). It has also been shown that wheat and many other species are able to utilize P from G6P, GLY and phosphodiesters (DNA and RNA) due the mining capacity, but are limited to acquiring P directly from IHP, although it is an abundant in many soils (George et al., 2008). This suggests that the biological importance of the different forms of IP and OP will be driven by their turnover rates. The challenges of OP mobilization and acquisition are to understand the response of plant functional traits depending on OP forms and soil properties to improve P acquisition and mobilization of crop species.

Overall, the plant P acquisition traits are known and their indirect and sometimes even direct effects on P acquisition/mobilization have been demonstrated (Ma et al., 2018;Nobile et al., 2019). The processes differ according to the nature of IP or OP forms (phosphate mono or diester) and the physicochemical properties of the soil. For instance, the availability of the different OP forms (IHP, G6P, GLY, DNA and RNA) as a direct effect of P acquisition strategies (P mining and foraging) remains unclear. Although the release of carboxylates can make some OP (G6P, GLY) available to plants, it is less efficient to solubilize IHP (Gerke, 2015) probably due to its strong binding to soil. Interactions between plant functional traits in the mobilization/acquisition of both OP and IP have been studied but remain poorly understood and unconfirmed. Thus, it has been suggested that plant strategies can be exploited using combinations of species with contrasting strategies or using a single species to understand better their actual effects on OP mobilization and acquisition in agroecosystems. Briefly, a better understanding of the impact of P-acquisition strategies on OP mobilization and acquisition by plants, which are related to the multiple morphological and physiological traits and the interactions between them, is key in the management of OP availability. Compared to IP, the response of P acquisition strategies to OP compounds and their impact on P acquisition from soils amended with various forms of OP have received much less attention. Crop species traits could be used to increase OP mobilization, helping to rethink P fertilization, sustain production, and recycle more OP in soils amended with organic amendments, but this requires a better understanding of the response of Pacquisition strategies to P sources, and their effect on OP mobilization and acquisition from soil minerals. In addition, understanding the trade-offs and effects of combining traits would allow us to unravel the complexity of the P form acquisition strategies and provide new knowledge for designing cultivated crop communities (i.e. multi-species crops) such as cover crops or intercrops to improve P acquisition and availability (Raven et al., 2018;Wen et al., 2019).

The aim of this study was to examine the response of P acquisition strategies toward P forms (IP and OP) in interactions with soil minerals and their consequences on OP availability and acquisition.

We measured P-acquisition strategies in eight major plant species from various phylogenetic lineages grown on several complexes of IP and OP (IHP, and GLY) adsorbed on Fe oxyhydroxides (goethite)

and clay minerals (kaolinite). We hypothesized that P-acquisition strategies (i.e. foraging and mining) differ in their responses to P sources, and this would promote greater OP availability and P acquisition from soil minerals. More specifically:

(i) morphological traits involved in P-foraging strategy will increase P availability and uptake from OP. These traits would induce a diffusion gradient which, in turn, will favor the desorption process of the different forms of adsorbed OP and thus the availability of P and, (ii) physiological traits involved in P-mining strategy will increase P availability and uptake by modifying the pH and/or release carboxylates and phosphatases allowing to increase the turnover of the pools of sorbed OP via desorption, solubilization and mineralization processes;

(iii) the acquisition of P from OP will be more significant under strategies involving P-mining than under those involving P-foraging, because OPs will be hydrolyzed by the strong activities of PME, and finally (iv) regardless of the strategy, the acquisition of P from OPs will be lower than that of IPs due to their strong sorption on minerals.

Materials and methods

Crop species, organic P compounds, and individual soil minerals

Two OP compounds, including inositol hexakisphosphate/phytate (IHP) and glycerophosphate (GLY), as well as inorganic P (KH2PO4), were selected for the experiments. Organic P compounds were initially selected because of their ubiquity in organic inputs and soils, the nature of phosphorus bonds, and their variable molecular sizes. Inorganic P forms were selected for comparison with organic P compounds.

Two minerals were chosen because of their contrasting properties and as representatives of the major Phacelia tanacetifolia Benth.) were selected for their diverse morphologies, P-acquisition traits and relevance for the local context.

Preparation of minerals-OP Adsorption Complexes

The two soil minerals were loaded with the two OP compounds or inorganic P to serve as a P source for the different species. Solutions containing 1 g P L -1 in 0.1 M KCl at pH 5.5 were prepared using the different P compounds. Goethite, and kaolinite was weighed in portions of 100 g into 1-L bottles. Then, 200 mL of 0.1 M KCl were added and the bottles were shaken for 24 hours at 25 °C to sufficiently hydrate the adsorption sites on the minerals. The pH was maintained at 5.5 ± 0.05 by adding 0.1 M HCl or NaOH solution. To start the formation of OP-mineral complexes, each of the 1 L bottles containing the soil minerals was filled with 800 mL of each P solution. In each bottle containing both the soil minerals and P compounds, some drops of hexanol were added to suppress microbial activities. Bottles were shaken on a mechanical shaker for 24 hours at 25 °C and then centrifuged (3000 G for 15 minutes).

The 1 L bottles were distributed into several 250-mL bottles, centrifuged, and the supernatants were collected and removed. The produced P-loaded minerals were agitated in deionized water and frozen at -20 °C. To determine the amounts of adsorbed P, a certain volume of supernatants was immediately filtered through a 0.22-μm membrane syringe filter for P analysis. The concentration of P in the supernatants was determined colorimetrically (Ohno and Zibilske, 1991) after hydrolyzing OP to IP using the persulfate oxidation method (Peters and Van Slyke, 1932). The quantity of P adsorbed was calculated as the difference between the initial amount of P added and the remaining P amount in the supernatant at the end of the experiment. Total P concentration in a subsample of each P-loaded was also determined using the procedure by Ostrofsky (2012) and showed very similar values compared to the ones determined as the difference between the initial and the final P amount in the supernatant (differences were in the range of 3-5.5% for the organic mineral-P complexes and 1.5-5% for the inorganic mineral-P complexes). The P loadings of the mineral-P complexes produced are shown in table 22. All minerals were loaded to reach their adsorption maxima.

Experimental Setup and Plant growth

To construct the experimental mesocosms, we filled 120×120 mm square polymer Petri dishes with sterilized coarse quartz sand, which is extremely poor in soil nutrients (Figure 28). The various Pmineral complexes prepared previously were then added to each square Petri dish and mixed with acidwashed quartz. Prior to the experiment, the substrates were sterilized by autoclaving at 121 °C for 2 h (Gómez-Suárez et al., 2020) to eliminate potential microorganisms, thus allowing the results to be attributed to the effect of root activity alone. To avoid any P limitation for the plants during the experiment, we provided a total amount of P that was found to be sufficient to meet the plants' needs (Gómez-Suárez et al., 2020). Thus, the amount of mineral-P complex added to the mixture was calculated to provide 40 mg of P in each treatment while the amount of quartz filled was approximately 100 g. The eight species were seeded one individual per square Petri dish per species and watered four times per week with water and a mixture of solution without P: Ca (NO3)2 (2 mmol L-1), MgSO4 (0. 5 mmol L-1), K2SO4 (0.7 mmol L-1), KCl (0.1 mmol L-1), MnSO4 (0.5 µmol L-1), CuSO4 (0.5 µmol L-1), ZnSO4 (0.5 µmol L-1), (NH4)6Mo7O24 (0.01 µmol L-1) and Fe-EDTA (100 µmol L-1). The devices were placed under controlled conditions (phytotron) with a 12h photoperiod, constant temperature (25 °C) and relative humidity (80%). Non-planted control treatments, in which the quartz-mineral-P complex had been incubated in similar devices without plants (hereafter referred to as the bulk substrate), were also performed. A total of 480 such devices were implemented: 8 species x 3 P compounds (IHP, GLY and IP) x 2 soil minerals (goethite and kaolinite) x 2 cropping conditions (ryegrass and bulk soil) x 5 replicates.

Morphological traits

Aboveground biomass and roots were separated by cutting the stem 1 cm above the first visible root.

Roots were then scanned while being immersed in deionised water using an Epson Scanner perfection V800 (Regent Instruments Inc., Québec, Qc, Canada) to produce a 600-dpi image. The image was analysed using WinRHIZO Regular software V.2016a (Regent Instruments Inc., Québec, Qc, Canada)

to determine root traits including root surface area (RSA), the percentage of fine root (FR), defined here as length of roots with a diameter < 0.5 mm, and root length density (RLD). After 48 h drying at 55 °C, scanned roots were weighed to calculate specific root length (SRL).

Nutrient uptake

Shoots and roots were then dried at 60 °C for 72 h, weighed, and crushed before analysis. The concentration of P in shoots and roots was determined colorimetrically (Ohno and Zibilske, 1991) after mineralization by 65% HNO3 digestion directly in a microwave Teflon vessel (Lange et al., 2014). The P concentrations in the seeds of the different species were also measured. The amount of P in seeds and plants (mg) was then calculated as the concentrations multiplied by their biomasses, respectively.

Finally, the amount of P taken up by plants (mg) was calculated after deducting the amount of P supplied by seeds (mg).

Rhizosphere and bulk soil analyses

After defrosting, acid phosphomonoesterase activity in the rhizosheath (PME) was measured with a modified buffer at pH 6.5 [START_REF] Tabatabai | Use of p-nitrophenyl phosphate for assay of soil phosphatase activity[END_REF]. Briefly, phosphatase activity was assessed via production of pnitrophenol from sodium p-nitrophenyl phosphate during a 1 h incubation at 37 °C with 0.5 g dry soil, 0.2 mL toluene, 4 mL modified buffer and 1 mL substrate. pNitrophenol release was determined spectrophotometrically at 410 nm after stopping the reaction with 4 mL 0.5 M NaOH and 1 mL 0.5 M CaCl2 and filtering. Rhizosheath pH was measured on 2 g equivalent dry soil with a 1:10 soil to solution ratio. ΔpH between rhizosheath and bulk soil from unplanted pots postgrowth was then calculated.

Data analysis

Data were statistically analyzed with R software (R version 4.1.3). The impact of factors (Species, P compounds, soil minerals, and their combined effect) on all measured morphological/architectural and physiological traits as well as P uptake and total biomass production was modeled by generalized linear models (GLM) using the "FactomineR" package. The GLM model was used to avoid mathematical RSA: root surface area; SRL: specific root area; TCE: total carboxylate release rate.

Influence of species, P forms and soil minerals f and their interactions on P acquisition traits

All measured morphological/architectural and physiological traits as well as P acquisition and total biomass production were significantly affected by species (P < 0.0001) and their interaction with P forms (P < 0.01) (Table 24). Mineral-species interactions had a significant effect on all measured traits (P < 0.001) except for fine roots percentage and total carboxylate release. Interactions between all factors (Species x Minerals x P forms) also affected the majority of plant traits (P < 0.0001).

Response of P acquisition traits and strategies to P forms

The P acquisition traits of species within the P acquisition strategy groups varied among P forms, with significant responses for some traits (Tables 25 and26). In Lolium perenne (group C4) and Phacelia tanacetifolia (C4), only total carboxylate release and fine roots percent differed significantly among P forms, and their values were significantly greater under OP forms. Total carboxylate release was found to be significant with Lolium perenne, and fine root percentage with Phacelia tanacetifolia in both OP forms. PME activity and other traits were also significant under OP forms but not significant from IP forms. Traits were significantly higher in the IHP form than in the GLY form. Pisum sativum (C1) and

Hordeum vulgare (C2) species showed significant variation of rhizosheath pH and total carboxylate release as well as SRL and fine root percentage in response to P forms. However, unlike the previous species, these traits were significantly higher on IP form than on OP forms. Finally, the remaining species, Lupinus albus (C1), Vicia faba(C1), Lens culinaris (C3), and Trifolium alexandrinum (C4)

showed different physiological (Rhizosheath pH change, total carboxylate release and PME activity)

and morphological (SRL, fine root percentage, RLD) traits between the IP and OP forms. Rhizosheath pH change was significantly elevated on the IP form, however, on the OP forms (IHP and GLY), it was mainly total carboxylate release, PME activity, and morphological traits (SRL, fine root percentage, RLD) that were significantly higher. Within these species, Lens culinaris (C3) and Trifolium alexandrinum showed more physiological and morphological traits in the IHP source, while in the GLY source it was rather Lupinus albus (C1) and Vicia faba(C1). In general, these species showed only physiological traits on goethite, whereas on kaolinite, we observed the expression of both morphological and physiological traits. Furthermore, for some species, the expression of traits differed between minerals but was generally not significant.

Effect of crop species and their P acquisition strategies on OP availability and P acquisition

The response of P acquisition strategies to P forms affected species P acquisition, which depended strongly on P forms for some species and on the interaction between P form and mineral for others (Table 25 and26). We found that irrespective of soil minerals, the P acquisition traits of two of the eight species: Vicia faba(C1) and Pisum sativum(C1) resulted in significantly high P acquisition and available P from OP forms (P < 0.01) and also some significantly high biomass productions (Table 25 and26).

Specifically, among the OP forms, the acquisition of P and available P in these species was higher from the IHP as compared to GLY forms and the biomass produced higher on GLY form. By contrast Lolium perenne(C4) had a globally higher P uptake on IP form compared to OP forms. Conversely, compared with previous species, Lens culinaris (C3), Hordeum vulgare (C2) and Trifolium alexandrinum had a globally equivalent P uptake between P forms even though the available P was slightly higher on the IP form. The species Phacelia tanacetifolia, Lupinus albus had a highly soil mineral dependent P acquisition. On goethite, the P acquisition strategies expressed by these species led to significantly high P acquisition from IP forms (P < 0.05), whereas on kaolinite, P acquisition was significantly high from OP forms. Among OP forms, available P content and P uptake were higher in GLY forms than in IHP forms. In general, the biomass produced was higher on the IP form for these species and Available P was not different between P forms and minerals.

Modeling the relationships between leaf and root traits combination on P acquisition from OP

The overall relationships between P uptake and factors involved in group formation were investigated with GLM (Table 27). The best-fitting models have a lower AICc and a ΔAICc closer to zero. PLS was used to highlight the combinations of traits and the type of P acquisition strategies that best predict P uptake (Figure 30). Because the best selected models were similar for both mineral types, we presented the results by P forms (Table 27 and Figure 30).

For species expressing physiological traits, the best model fit on the IP form was achieved with total carboxylate release alone. On the IHP form, the best fit was with a combination of carboxylate release and PME activity and on the GLY form with a combination of carboxylate release and rhizosheath acidification. For species with intermediate traits, SRL, fine root percent, PME activity and leaf [P] was the best predictor of P uptake on the IP form. RSA, RLD and leaf [P] combination provided the best fit on the IHP form while on the GLY form it was RLD, PME activity and leaf [P] that provided the most suitable fit. For morphologically trait-using species, RLD and percent fine roots gave the best model fit for P acquisition on the IP form. The addition of SRL to the previous combination was also a better predictor, but performed worse than models incorporating both RLD and fine root percentage.

The model incorporating RLD was the best predictor on the IHP form, whereas on the GLY form, the best predictor was SRL. The combination of RLD and RSA was also a good predictor on the IHP form, but performed poorly compared with the model incorporating only RLD. Similarly, for GLY form, the RSA and SRL combination was also a good predictor, but with poor fit compared with the model with only SRL. The PLS approach gave similar results to the GLM model. On the IP form (GoFPLS = 0.73), total carboxylate release was the best single predictor of the physiological components. Fine root percentage topped the intermediate component contributors, followed by SRL, PME activity, and leaf [P]. SRL contributed as much as fine root percentage to the morphological components. In this form of IP, it was found that the intermediate component had the highest predictive weight (corr = 0.93), followed far behind by the morphological component (corr = 0.15). The physiological component was found to have very negligible predictive capacity (corr = 0.06). On the IHP form, PLS analysis (GoF = 0.72) highlighted the importance of the intermediate component (corr = 0.81), as well as the physiological component (corr = 0.17), whereas the morphological parameter showed poor predictive performance. PME activity and total carboxylate release were found to be the most significant contributors for the physiological component, respectively. For the intermediate component, it was leaf

[P], RLD, and RSA, respectively. The RLD was the unique contributor for the morphological component. On GLY form, and as for other forms of P, the greatest weight was associated with the intermediate component (corr = 0.58, AICc = 51) followed by the morphological component (corr = 0.22, AICc = 0); for this form, the lowest predictive ability was from the morphological component.

RLD and PME activity had the greatest impact on the intermediate component, followed by leaf [P].

SRL was the only contributor to the morphological component. In summary, the PLS analysis revealed that the intermediate component had the highest predictive ability on all forms of P. The physiological component was the second most important contributor on IHP while on GLY it was the morphological component.

Table 27: Selected models fitted to phosphorus uptake sorted from best fit to worst by strategies

The process of selecting the combinations of traits that give the best model fits for predicting P uptake was performed under R software with the stepAIC () and bestglm () functions that are based on the stepwise and best subset approaches. AICc second order Aikake's information, FR Fine root percentage (<0.5 mm ⌀), PME Phosphomonoesterase activity, RSA Root surface area, ΔpH change in rhizosheath pH. Phosphorus acquisition strategies of crop species may depend on P forms and thus the nature of the applied P fertilizer. Previous work has suggested that plant species have different P acquisition traits, leading to preferential sources for P acquisition [START_REF] Ceulemans | Phosphorus resource partitioning shapes phosphorus acquisition and plant species abundance in grasslands[END_REF]Nobile et al., 2019). Compared to IP, the response of P acquisition strategies to OP compounds has received much less attention (Amadou et al., 2021;Turner, 2008). Crop species traits could be used to recycle more P in soils amended with organic amendments, but this requires a better understanding of the response of P acquisition strategies to P sources, and their effect on P mobilization and acquisition from soil minerals [START_REF] Feng | Strategies for improving fertilizer phosphorus use efficiency in Chinese cropping systems[END_REF]Sulieman and Mühling, 2021). The results of the GLM model showed that two of the physiological traits (carboxylates and pH variation), one of the morphological traits (fine root percentage) and leaf [P] were significantly affected by P forms and their interaction with species and minerals. This suggests differential expression of P acquisition traits among the P forms examined and supports our hypothesis that P acquisition strategies (i.e., foraging and mining) differ among P sources (Wang and Lambers, 2020). However, this does not apply to all traits, as some traits showed no variation among P forms. Organic P forms impacted P acquisition traits in a species-specific manner. In Lolium perenne (C4) and Phacelia tanacetifolia (C4), carboxylate release and percent fine roots were significantly enhanced by OP application compared to IP form. PME activity and other traits were also higher under OP forms but were not significant. Between OP forms, P acquisition traits of both species were significantly higher in the IHP form than in the GLY form. These result shows that P-acquisition traits of Lolium perenne and Phacelia tanacetifolia mainly carboxylate release, PME activity and percent fine roots responded more to OP forms and that IHP form most impacted P-acquisition traits compared to GLY. [START_REF] Shahzad | Interaction of compost additives with phosphate solubilizing rhizobacteria improved maize production and soil biochemical properties under dryland agriculture[END_REF] showed that organic amendments increased the amount of carboxylate in the rhizosphere of maize compared to inorganic fertilization. Other studies have shown an increase in soil phosphatase activity in either incubation or field experiments [START_REF] Criquet | Short-term effects of sewage sludge application on phosphatase activities and available P fractions in Mediterranean soils[END_REF][START_REF] Hamdi | Repetitive land application of urban sewage sludge: Effect of amendment rates and soil texture on fertility and degradation parameters[END_REF]Houben et al., 2019). Chickpea, for example, appears to produce both phosphomonoesterases and diesterases following the input of organic fertilizers into the soil (Darch et al., 2018;Pang et al., 2010). Our observations are also consistent with other results showing that some species express higher levels of carboxylate and fine root to access more OP in the soil (Haling et al., 2018;Wen et al., 2019). The higher expression of the traits found on the IHP form compared to GLY, may be due to its greater affinity with soil, and its resistance to enzymatic hydrolysis that would stimulate the expression of traits in the species. This emphasize that the chemical nature of specific OP forms affects plant P acquisition strategies in soil. In contrast to the previous species, Pisum sativum (C1) and Hordeum vulgare(C2) P-acquisition traits (rhizosheath pH, total carboxylate release as well as SRL and fine root percentage) were higher under the IP form when compared to the OP form, indicating that these species were less affected by OP forms. Furthermore, we found that the P acquisition traits of Lupinus albus(C1), Vicia faba (C1), Lens culinaris (C3), and Trifolium alexandrinum responded to both forms of P. Change in rhizosphere pH of these species was significantly enhanced under the IP form, whereas under the OP forms (IHP and GLY), it was mainly the total carboxylate release, PME activity, and some morphological traits (SRL, percentage of fine roots) that were significantly important. This

indicates that these species respond to both IP and OP forms by expressing different P acquisition traits.

Thus, on IP forms, rhizosphere pH was more important and this was likely to promote P acquisition and on OP forms, carboxylate release, PME activity, and certain morphological traits were more important that were likely to access, solubilize, and mineralize OP forms (Damon et al., 2014;Neumann et al., 1999). These results are also evidence that the response of P acquisition traits to specific forms of OP is also species dependent [START_REF] Lambers | Plant nutrient-acquisition strategies change with soil age[END_REF]Wang and Lambers, 2020). For example, Lens culinaris and Trifolium alexandrinum showed a greater response to the specific form IHP and Lupinus albus and Vicia faba to the GLY form.

In conclusion, the P acquisition traits of the species studied changed between the application of the OP forms and the application of the IP form, a difference in trait expression was also observed between the specific OP forms, i.e. IHP and GLY. Furthermore, trait expression was highly species dependent, with some species expressing more traits exclusively on the IP or OP form while others had different important traits expressed based on the P forms. The contrasting physicochemical nature of the P forms as well as the nature of the different species may explain the varied responses of P acquisition strategies to the P forms.

Role of P acquisition strategies on OP availability and P acquisition

Various P mobilization and acquisition strategies in crop species and cultivars have been demonstrated, but their efficacy in acquiring P from different forms of OP remains poorly studied (Robles-Aguilar et al., 2019;Simpson et al., 2011). For example, the availability of different forms of OP (IHP, GLY, DNA, and RNA) as a direct effect of P acquisition strategies (P mining and foraging) remains unclear (Amadou et al., 2021). Here, P acquisition strategies (i.e., foraging and mining) were found to differ among P sources, and further GLM analysis showed that P availability and uptake were also significantly different among species, their interaction with P forms, and the overall interaction of factors (Species x Minerals

x P Forms). Hence, we infer that the different response of P acquisition strategies to P forms (IP and OP) led to varied P acquisition by species. We found P acquisition strategies of Vicia faba (C1) and with some variation depending on the mineral. This result contradicts the extensive literature that revealed the low availability of IHP to crops as compared to other forms of P in soils (Findenegg and Nelemans, 1993;Gerke, 2015;Xu et al., 2019). However, this indicates that the P acquisition strategies of the above species were effective in mobilizing IHP on the different soil mineral types. Thus, we suggest that despite the higher accumulation of IHP reported in most soils (Amadou et al., 2022;Vincent et al., 2013), its desorption and hydrolysis may be more facilitated by species with high physiological and morphological traits potential. However, although this is at odds with recent results (Amadou et al., 2022;Garcia-Lopez et al., 2015) it responds to Gerke (2015) who suggests that P acquisition from IHP and its mobilization from the surface of soil components could be effective by root exudates of cover crop species, primarily di-and tricarboxylic acids, which can increase the solubility of IHP. In contrast, compared to the previous species, Lentil culinaris (C3), Hordeum vulgare (C2), and Trifolium alexandrinum (4) showed broadly equivalent P uptake between P forms. It is thought that this nondifference in P uptake is due to the fact that these species, with the exception of Trifolium alexandrinum (4), had "intermediate" traits that varied very slightly, and their main characteristic was P concentration in the leaf. Finally, Lolium perenne (4) was more efficient in acquiring the IP form than the OP forms.

Indeed, Lolium perenne had P acquisition traits that generally did not differ between P forms. The inability of these species to mobilize OP is intensely demonstrated in the literature (Amadou et al., in press;[START_REF] Chen | Phosphorus dynamics in the rhizosphere of perennial ryegrass (Lolium perenne L.) and radiata pine (Pinus radiata D. Don.)[END_REF][START_REF] Chen | Phosphorus dynamics in the rhizosphere of perennial ryegrass (Lolium perenne L.) and radiata pine (Pinus radiata D. Don.)[END_REF]. Our hypothesis that P acquisition from OPs will be greater in strategies involving P mining than in those involving P foraging, because OPs will be hydrolyzed by the strong PME activities, was confirmed in this study [START_REF]Differential interaction of Aspergillus niger and Peniophora lycii phytases with soil particles affects the hydrolysis of inositol phosphates[END_REF]Richardson, 2005). The main result supporting the hypothesis was that species from the physiological trait group (Vicia faba, Pisum sativum, Phacelia tanacetifolia, Lupinus albus) were able to take up more P from the OP than those from the morphological and intermediate group species. However, our last hypothesis that regardless of the strategy, P acquisition from OPs will be lower than that from IPs due to their strong sorption on minerals was not confirmed, as the P acquisition strategies of the species studied led to higher or equal P uptake from OPs (except Lolium perenne). This exception with Lolium perenne is thought to be due to the fact that Lolium perenne has no P mobilization capacity and thus can only utilize readily available P.

According to our previous results (Amadou et al.,in press), Lolium perenne was able to utilize 2-3 times more P in the IP form than in the OP form, because IP was less sorbed and was more available.

Soil minerals affect P acquisition strategy on OP availability and P acquisition

Soil minerals and especially their interactions with species significantly affected the response of traits towards OPs because of their contrasting physicochemical properties. Global comparison of traits response to P forms revealed a greater expression of traits on goethite, although Phacelia tanacetifolia and Vicia faba had more traits on kaolinite. Nevertheless, the resulting P acquisition from OPs was generally more important on Kaolinite. Soil minerals such as Fe, Al oxides and clay minerals are known to significantly reduce the efficiency of crop species to utilize P from applied organic amendments (Amadou et al., 2022;Ganta et al., 2021;Giaveno et al., 2010). To date, there are relatively few studies that explore the effect of major soil minerals on P acquisition strategies of crop species and how these strategies influence OP mobilization. It is assumed that OP adsorbed on Fe and Al oxides is protected from being affected by plant P acquisition strategies, leading to its accumulation in the soil (Stutter et al., 2015). Yet, in this study, we showed that P acquisition strategies of individual species promoted P acquisition from OPs across all soil minerals. The greater expression of traits on goethite is thought to be due to its high P adsorption capacity and high-energy binding to OP, which renders the medium more P-deficient and thus leads to a stimulation of trait expression by the species (Faucon et al., 2015;Simpson et al., 2011). This corroborates the literature that most plants develop more P acquisition traits in high P-deficient soils to specifically access different forms of OP and increase soil P acquisition (Richardson et al., 2009;Simpson et al., 2011). However, although the P acquisition traits were more strongly expressed on goethite, we found that P acquisition from OPs was lower on this mineral but higher on kaolinite. This suggests that mineral-OP interaction properties affect plant P acquisition strategies. Indeed, OP is known to desorb more from clay minerals (montmorillonite and kaolinite) than from Fe and Al oxides (Amadou et al., 2022;[START_REF] Fang | Phosphorus adsorption onto clay minerals and iron oxide with consideration of heterogeneous particle morphology[END_REF]. Since clays have also been shown to have a lower P binding capacity, it can be expected that P acquisition strategies on this mineral will result in greater OP availability (Bortoluzzi et al., 2015;He et al., 1994). Overall, our results highlighted the central role of soil minerals and their interactions with P forms and species on the response of P acquisition traits and how this can promote P availability from OPs. A better understanding of these interactions is an important challenge for modeling OP dynamics and predicting P release depending on crop and soil type (Raven et al., 2018;Wen et al., 2019).

Highlight main traits involved in OP mining and foraging and the contribution on P availability and acquisition

Overall, the P mining and foraging strategies highlighted in this study positively affected P utilization from OP forms. However, it remains unclear which key traits of these strategies directly or indirectly contribute to P availability and acquisition, as the process differs depending on the nature of the P forms (Lambers et al., 2006). The results of GLM and PLS modeling of phosphorus uptake showed that RLD and SRL were the most important traits involved in OP foraging (for the specific forms IHP and GLY respectively). In the case of OP mining, it was rather a combination of TCE and PME or TCE and DpH. PME activity was the most important contributor for the IHP form and TCE for GLY. These findings suggested that among the plant architectural traits, root length density, would best enable plants to improve their foraging capacity for the specific form IHP and within the morphological traits, specific root length would contribute the most to GLY availability (Haling et al., 2018;Ma et al., 2018;Pang et al., 2010). Various individual effects of SRL, RLD or PME on P dynamics and its contribution to P uptake have been reported in several species (Wang and Lambers, 2020;Zhu et al., 2005). Higher RLD in the upper soil layers was found to be the most important root trait of wheat for P mobilization in response to organic fertilizer application (Lamont, 2003). In maize genotypes, the effects of varying RLD and root hair length led to a 100% increase in total P mobilized from organic amendments (Zhu et al., 2005). However, the very few studies on the forms of OP do not adequately quantify their potential contribution to P availability in the organic fertilizer-soil-plant system (Amadou et al., 2021;Klotzbücher et al., 2020;Sulieman and Mühling, 2021). The main features involved in P mining and foraging highlighted in this study and their strong contribution to the prediction of P acquisition, offer opportunities to improve P cycling in multi-species systems, including exploiting the inherited P pool.

Furthermore, the results of the PLS analysis show that phosphorus uptake is best predicted by root morphological traits (ΔAICc = 0), followed generally by intermediate traits. Although several correlations between a single trait and P uptake have been observed previously [START_REF] Pearse | Triticum aestivum shows a greater biomass response to a supply of aluminium phosphate than Lupinus albus, despite releasing fewer carboxylates into the rhizosphere[END_REF]Lambers et al. 2006;Roseetal.2010;Wen et al. 2017), our results add to our incomplete knowledge on the variation and contribution of individual traits to the acquisition of specific forms of soil organic P (Lyu et al. 2016). In sum, our results highlighted the specific traits of OP acquisition strategies that best predict P acquisition. Crop models to estimate total soil P reserves and at least its specific forms (IHP, G6P, GLY, etc.) in a multispecies cropping system can be developed based on the plant traits highlighted in this study, including inter-and intraspecific variability in traits and soil properties. This approach to trait-based OP mobilization modeling can be potentially useful in different climates.

Conclusion

Crop species traits could be used to improve OP cycling and availability in cropping systems, thereby helping to rethink P fertilization, but this requires a better understanding of the response of P acquisition strategies to OP sources, and their effect on OP mobilization and acquisition from soil minerals.

Morphological and physiological traits include various P acquisition strategies that differ depending on the nature of the IP or OP forms and the physicochemical properties of the soil.

Our results showed a differential P acquisition trait response to P forms and a strong dependence of trait expression on species type. We found that species P acquisition traits changed between the application of OP forms and the application of the IP form. In addition, a difference in trait expression was also observed between the specific OP forms, i.e., IHP and GLY. There was strong species dependence in the expression of traits, some species expressed more traits exclusively on the IP or OP form while others had different important traits expressed on both types of P. The contrasting physicochemical nature of P forms as well as the characteristics of different species may help explain the varied responses of P acquisition strategies to P forms. The improvement in P acquisition of most species from OPs demonstrated that the positive response of P acquisition strategies (i.e., foraging and than soils rich in Fe and Al oxyhydroxides or 1:1 mineral (Figure 31). Nevertheless, the observed higher desorption of GLY from Al oxyhydroxides (Chapters 1 and 2), which are known to limit P availability in highly weathered soils in tropical regions, emphasized the high potential for using GLY as a P source in these regions (Zhang et al., 2017). The low P uptake from kaolinite-OP complexes (Chapter 2) is consistent with previous observations showing that kaolinite-P is a bidentate, inner-sphere surface complex below pH 6 (Hu et al., 2020;Ruyter-Hooley et al., 2015), and that P adsorbed on kaolinite is difficult to desorb (Kafkafi et al., 1988;Xiong et al., 2022). This, therefore, emphasizes that Fe and Al oxyhydroxides were less responsible for limiting OP availability than kaolinite, despite their generally higher adsorption capacity in soil (Chapter 1). However, since the P concentration used in our study may be higher than that of real soil systems, it would be interesting as a prospect to investigate the effect of P concentration on adsorption processes by performing sorption experiments at different (and lower) P concentrations.

Evidence of important OP mobilization by plants as a result of N-OP interactions and plant trait responses

The N characteristics in organic fertilizers added to enhance P use can affect the availability of OP in the soil-plant system. The literature showed that the addition of N can increase plant P demand, which in turn promotes soil P mobilization (Schleuss et al., 2020;Zhang et al., 2017). This highlights the ecological importance of the beneficial effect of N on plant P use efficiency (Vitousek et al., 2010).

Overall, it has been stated that plants could trade N for P by adjusting N and P acquisition rates from the soil, potentially explaining synergistic growth responses to N and P addition (Long et al., 2016;Peng et al., 2019). Furthermore, different OP mobilization and acquisition strategies in crop species and cultivars have been demonstrated, but their efficacy in acquiring P from the different OP and IP forms remains understudied [START_REF] Lambers | Phosphorus Nutrition of Proteaceae in Severely Phosphorus-Impoverished Soils: Are There Lessons To Be Learned for Future Crops?[END_REF]. These strategies involve morphological, architectural [START_REF] Lynch | Root Phenes for Enhanced Soil Exploration and Phosphorus Acquisition: Tools for Future Crops[END_REF] and physiological traits (Richardson et al., 2009), microorganisms, or a combination of both to effectively contribute to the ability of plants to access different reservoirs of poorly available OP in soils [START_REF] Wang | Nitrogen enrichment buffers phosphorus limitation by mobilizing mineral-bound soil phosphorus in grasslands[END_REF]Wang and Lambers, 2020). To date, it remains unclear how the chemical forms of N, plant P acquisition strategies, and their interactions with OP and minerals influence OP availability, acquisition, and limitation by plants in ecosystems.

The beneficial effect of N addition and further positive consequences of the responses of P acquisition strategies by the plant on OP availability was highlighted in the characterization of N-OPmineral interactions (Chapter 3) and the effect of root traits-OP-mineral interaction (Chapter 4).

Compared to no N addition (Chapters 1 and 2), the increase of P uptake by plants with N addition, especially with NO3-N forms (Chapter 3), highlighted the synergistic effects of N and OP and their interactions with minerals on P dynamics, i.e. its availability and limitation (Figure 32). Within specific forms of OPs, results in Chapter 3 suggested that the addition of N would promote the mobilization of IHP (major forms of OPs in soil and organic amendments) and make it less limiting to plants compared to other forms of OPs, i.e., GLY or G6P, highlighting the central role of the interaction between N, OP, and minerals on the OP cycle (Hou et al., 2021(Hou et al., , 2020)). In addition, these results highlight a new mechanism by which interactions of N forms with OP pools could accelerate OP cycling, including increasing the availability of IHP, which is the important form of OP and also the most adsorbed and least available form (Chapters 1 and 2), and thus delay the onset of P limitation of this form for plant growth (Chapter 3). High phosphatase activity and P availability in the rhizosphere with the addition of N (Chapter 3) likely contributed to plant P uptake (Long et al., 2016). Correlations indicated that total P uptake was positively related to available P and phosphatase activity (Chapter 3). Most likely, the addition of N allowed plants to synthesize N-costly phosphatases (Schleuss et al., 2020), which then made OP available for plant uptake [START_REF] Helfenstein | Combining spectroscopic and isotopic techniques gives a dynamic view of phosphorus cycling in soil[END_REF]. Thus, it seems likely that with the addition of N, OP is recycled more intensively from OP pools irrespective of soil minerals (Widdig et al., 2019).

The interaction of N with IP forms led to greater P uptake and markedly reduced P limitation compared to the interaction of N with OP forms, presumably because of the high adsorption and low availability of OP, as shown in Chapters 1 and 2. Thus, it can be deduced that in agroecosystems where P is very strongly sorbed (such as OP forms), N additions can indeed lead to a rapid depletion of available P and thus to a very strong limitation of P, but in systems where P is relatively more available (such as IP forms), N additions do not lead to a systematic limitation of P but rather to a colimitation of N and P.

With the addition of N, more OP was recycled from the clay minerals (kaolinite) and thus delaying P limitation compared to iron and aluminum oxides (goethite) which highlights the importance of considering the soil mineral in the design of cropping systems to mobilize OP. Thus, Chapter 3 strongly suggests that despite the higher adsorption of OP forms (Chapter 1), N additions can indeed lead to OP use efficiency in the soil-plant system.

To further explore effective mechanisms for OP mobilization in the soil, the response of P acquisition strategies to various forms of OP interacting with soil minerals and their consequences for OP availability and acquisition were examined in eight major plant species (Chapter 4). The differential expression of P acquisition traits among the OP forms supports our hypothesis that P acquisition strategies (i.e., foraging and mining) are affected by the type of OP sources and their biogeochemical properties (Wang and Lambers, 2020). Similar to the effect of N-OP interactions (Chapter 3), the positive response of P acquisition strategies to OP sources (Chapter 4) resulted in greater P availability and acquisition from OPs (Figure 32). Irrespective of plant strategies, the higher P acquisition from OPs relative to IPs (Chapter 4) showed that, despite the higher sorption of OPs in the soil (Chapters 1 and 2), plant P foraging and mining strategies were able to improve the cycling and availability of OPs relative to IP forms. Taken together, the findings of Chapters 3 and 4 suggest that the various forms of N contained in organic inputs and the P acquisition strategies of crop species can be exploited to enhance the mobilization of OPs in the organic fertilizer-soil-plant system (Figure 32). The agronomic application of this result is particularly important for limiting the use of chemical fertilizers. OP (in green): Organic P includes the speciated forms that are: Myo-inositol hexakisphosphate, IHP , Glycerophosphate, GLY, glucose-6-phosphate, G6P . IP (in red): Inorganic P.

From theory to practice: Incorporate all mechanisms/processes into models and decision support tools to estimate soil P availability and manage P fertility from organic inputs

Agricultural systems modeling can be used to improve our understanding of the complex interactions between soil, plants, and the environment and thus support decision making [START_REF] Jones | Organic acid behavior in soilsmisconceptions and knowledge gaps[END_REF].

However, modeling changes in the cycling of OP forms with respect to their availability and contribution to plant growth is a challenging task (Honvault et al., 2020). The challenge of simulating complex chemical reactions related to OP is related to the fact that key processes can be very different across soil types, organic fertilizer types, application strategies, and environmental conditions. An effective soilcrop mineral OP model could serve as a tool to improve P fertilizer management for different soil types, climate, and farming practices (Li et al., 2019). However, while many attempts have been made to simulate P behavior in agricultural systems, most of them have focused on field and watershed scales and have been specifically designed to predict P losses and transport to groundwater and surface water (Achat et al., 2016), rather than to predict P dynamics in soil-plant systems (Table 28). Those that do are generally based on simplified OP cycles that seek to predict P transformations and soil P availability(Table 28), with an emphasis on the interaction between the available P pool and crop demand that determines crop P uptake (Achat et al., 2016). It is therefore unclear whether current modeling platforms are able to accurately account for the dynamics of OPs in different soil types, their interactions with N forms, and the plant acquisition strategies that determine their fate. The interaction with environmental factors such as soil water content, which affect both root activity/distribution and crop P acquisition, is also not well understood. To effectively simulate the dynamics of OP in an organic fertilizer-soil-crop system, an effective model must include four of the key components (Figure 33, Table 28): (i) a component that thoroughly simulates the intrinsic properties that govern mineral-OP interaction, i.e., modeling the adsorption and desorption dynamics of several major forms of OP on several representative soil minerals; (ii) a component capable of accurately reflecting the demand for and uptake of P from OP forms by plants, as well as the effects of P on crop growth, and one related to the cycling and transformations of soil OP that determine the amount of soil P available for uptake by plants; (iii) a component that evaluates and simulates the irrespective and interactive effects of N and P forms and their interaction with soil minerals on P limitation and P uptake in plants and finally (vi) a component on the role of P acquisition strategies on the mobilization and acquisition of specific forms of OP. The four components must of course accurately represent the key processes, but in order to effectively simulate the dynamics of OP or more generally P in a cropping system, the interactions between these components are also essential, particularly the responses of crop growth to changes in OP availability [START_REF] Daroub | Development of a soil-plant phosphorus simulation model for calcareous and weathered tropical soils[END_REF].

The need to incorporate the parameters of adsorption and desorption of OPs to develop a model to predict the release of OPs in agroecosystems

The first P model that attempted to integrate P pools, soil, and plant components was the P module developed in the 1980s for the Erosion-Productivity Impact Calculator (EPIC) model and reported by [START_REF] Jones | A Simplified Soil and Plant Phosphorus Model: I.Documentation[END_REF]. This EPIC model was constructed from regression analyses of 78 different soils from the United States and Puerto Rico [START_REF] Sharpley | A Simplified Soil and Plant Phosphorus Model: II. Prediction of Labile, Organic, and Sorbed Phosphorus1[END_REF], with the soils then divided into three categories: calcareous, slightly weathered, and heavily weathered. These three soil categories are then used to guide the initialization of the "labile P" pool by combining soil P pools with an equation related to soil type. On the other hand, the DSSAT model proposed by [START_REF] Daroub | Development of a soil-plant phosphorus simulation model for calcareous and weathered tropical soils[END_REF] sets the P pool size based on the sequential P fractionation results of [START_REF] Hedley | Changes in Inorganic and Organic Soil Phosphorus Fractions Induced by Cultivation Practices and by Laboratory Incubations[END_REF] and the transfer equations between P pools are linked to specific soil properties ("low pH weathered soils" and "high pH calcareous soils").

Some soil P models have also distinguished between IP and OP pools, allowing simulation of inorganic and organic P fertilization. However, these models are overall focused on a very simplified simulation of soil P dynamics and hardly any agricultural models have tested and integrated the dynamics of OP despite its importance in predicting plant productivity. The surface movement of dissolved P, for example, is considered in the ANIMO and GLEAMS models, but not the processes of P adsorption and desorption, nor those of OP in the soil, even though some very simplified equations are included in the GLEAMS model [START_REF] Raymond | Does the APSIM model capture soil phosphorus dynamics? A case study with Vertisols[END_REF]. The widely used APSIM and DAYCENT model considers only sorbed IP in equilibrium with soil labile P from which leaching occurs, and includes representation of P loss through soil erosion. Furthermore, none of these models consider the important desorption process of IP, with the exception of the MACRO model, which incorporates it in a very simplified manner without linking it to the forms of OP [START_REF] Yang | The role of phosphorus dynamics in tropical forests a modeling study using CLM-CNP[END_REF]. A major implication of deciphering the interactions between soil minerals and the predominant forms of OP in soils and organic fertilizers (Chapter 1) and of studying P availability to plants from several mineral-OP complexes (Chapter 2) is the incorporation of these product parameters into modeling approaches or to improve existing models (Figure 33). Adsorption parameters, determined by fitting data to the nonlinear form of Langmuir and

Freundlich isotherm models (Chapter 1; Amadou et al., 2022a), provide several equations that could be incorporated as predictive mechanisms for OP immobilization in existing models such as EPIC, DSSAT or MACRO. In addition, desorption-related parameters calculated by fitting data to the nonlinear form of the Elovich kinetic model (Bulut et al., 2008) also emerge as important parameters to strengthen existing models to predict OP release to soils while reducing OP losses to the environment.

Current models do not consider properties related to specific forms of OPs such as IHP and other important OP pools such as GLY or G6P [START_REF] Raymond | Does the APSIM model capture soil phosphorus dynamics? A case study with Vertisols[END_REF][START_REF] Yang | The role of phosphorus dynamics in tropical forests a modeling study using CLM-CNP[END_REF], which, together with IHP, nevertheless account for a significant portion of total P in soil (Darch et al., 2014).

Furthermore, the influence of physicochemical properties of the main specific soil minerals, which are major determinants of the ability of soil minerals to interact with P, is not considered. Through the study of the mechanisms controlling the dynamics of various OP compounds (IHP, GLY and, G6P) into and from several soil minerals, including Fe and Al oxides (goethite and gibbsite, respectively) and clay minerals (kaolinite and montmorillonite), we argue that factors related to soil properties and OP molecular traits directly affect OP reactions and release in soil. Therefore, the integration of these information is necessary to improve the accuracy of the prediction models (Table 28). In addition, the consequences of interactions between minerals and OP forms on plant P nutrition elucidated in Chapter 2, provide important information for the development of a specific model for predicting OP release to the soil (Figure 33). Ecosystem N and P cycles consist of multiple biogeochemical pools and processes that are linked and interdependent, jointly controlling soil P availability, plant P uptake and plant P limitation [START_REF] Zhang | En outre, différentes stratégies de mobilisation et d'acquisition des OP dans les espèces et cultivars de cultures ont été démontrées, mais leur efficacité dans l'acquisition de P à partir des différentes formes d'OP et d'IP reste peu étudiée[END_REF]. Recently, P modules have been integrated into ecosystem models such as CASA-CNP [START_REF] Wang | Fertilization and litter effects on the functional group biomass, species diversity of plants, microbial biomass, and enzyme activity of two alpine meadow communities[END_REF], JSBACH-CNP (Goll et al., 2012), CLM-CNP [START_REF] Yang | The role of phosphorus dynamics in tropical forests a modeling study using CLM-CNP[END_REF], and N-COM [START_REF] Zhu | Multiple soil nutrient competition between plants, microbes, and mineral surfaces: model development, parameterization, and example applications in several tropical forests[END_REF] to study nutrient limitations on carbon cycling and C-N-P interactions. In these models, P is typically stored in several pools, including plant biomass, litter, available soil P forms (Vitousek et al., 2010). P dynamics are often coupled to C and/or N cycling through the stoichiometric relationship of C, N, and P in plant tissues and soils (Goll et al., 2012;[START_REF] Wang | Fertilization and litter effects on the functional group biomass, species diversity of plants, microbial biomass, and enzyme activity of two alpine meadow communities[END_REF]. With the ANIMO and DAYCENT models (Achat et al., 2016), soil N is represented as NO3N and NH4N. They consider the movement of N from applied fertilizer or manure. Although efforts have been made recently to add interactions between N-IP pools in some models, the influence of N forms, OP chemical forms, and their interactions with soil minerals are poorly represented or simplified in C-N-P models, which could have consequences for model predictions (table 28). More importantly, this limits the ability of ecosystem models to analyze the effects of potential future climate change on overall ecosystem productivity (Deng et al., 2017;Goll et al., 2012). We found that irrespective of soil minerals, when N is added, the plant becomes co-limited in N and P in the presence of IP, whereas the plant systematically shifts to P limitation in the presence of OP forms (Chapter 3). The pattern of available P and P limitation after N addition (IP > IHP > GLY, Chapter 1), reinforces the assumptions that the type and biochemical nature of OP sources determine the degree of nutrient limitation in plants (Amadou et al., 2022b).

Therefore, the biochemical properties of OP forms and the properties of soil minerals are both required in C-N-P models to account for the N-P interaction in the soil-plant system (Figure 33). The influences of N additions on OP pools and processes revealed in this study could help for understanding the roles that N and P play in controlling plant growth and internal nutrient accumulation and to accurately parameterize the C-N-P models (Achat et al., 2016). The degree of P limitation varies considerably between mineral types and forms of P (Chapter 3) due to the contrasting physicochemical properties of the minerals used ( Chapter 1, Bai et al., 2021;[START_REF] Yang | The role of phosphorus dynamics in tropical forests a modeling study using CLM-CNP[END_REF]) and the biochemical nature of P sources (Anderson, 1980;Condron et al., 2005). Thus, incorporating physicochemical properties of specific key soil minerals that drive N-OP interactions into ecosystem models is necessary to specifically simulate the effects of N on ecosystem productivity and carbon accumulation potential by mitigating N and/or P limitations (Elser and Bennett, 2011). The data generated on the effects of specific interactions of several forms of OP, N interacting with different soil minerals (Chapter 3) in combination with the properties deciphered in Chapter 1 could potentially be specified in the CASA-CNP and CLM-CNP models for optimization. The integration of the data and parameters generated from Chapters 1, 2 and 3 into the C-N-P models is necessary for more comprehensive studies of ecosystem processes, feedback, and responses to environmental change. In particular, because tropical ecosystems have a significant effect on the global carbon cycle, future C-N-P models will need to be able to account for the heterogeneity of N versus P limitation in these ecosystems (Figure 33).

modeling (Chapter 4) of plant-specific traits involved in the dynamics of species of different forms of OP (IHP, GLY) under different soil mineral types can be considered in future models (Figure 33).

Targeted elucidation of these plant P acquisition strategies in a range of contexts and at the field level could provide more accurate estimates of crop effects on P availability via P release from OP forms.

However, as noted in Chapter 4, the relative contribution of a specific process to the effects of P acquisition strategies (mining and foraging) on P availability is likely to be highly dependent on species, biochemical nature of P forms, and soil conditions, and in particular P availability. Plant P mining and foraging strategies have been successful in improving the cycling and availability of OPs relative to IP forms (Chapter 4), despite the stronger sorption of OPs to soil demonstrated in Chapter 1, which limited their availability to plants (Chapter 2). A better understanding of these processes should contribute to the development of more accurate and comprehensive models for agroecological intensification.

A proposed global model design to improve the efficiency of OP utilization on a global scale

Significant advances have been made in recent years in ecosystem models, incorporating formulations of P-specific processes and C-N-P interactions (Achat et al., 2016). However, there is considerable room for further improvement, especially in processes related to soil mineralogy, the OP forms of organic fertilizers, and their interactions with C and N forms and concentrations that are known to control plant response to climate change and nutrient limitation (Table 28). At the global scale, results related to soil minerals, P forms and to some extent plant P acquisition strategies as well as pH and climatic data are highly relevant for P availability and dynamics (i. e. different OP and IP forms). Based on the results of simulations and modeling of processes related to N-OP-mineral interactions and related crop traits, we suggest to modelers and empiricists the following building blocks complement the current C-N-P model processes and thus improve soil OP mobilization (Figure 34).

Rôle des plantes et leurs traits dans la dynamique du P organique

Plusieurs approches directes et innovantes ont été identifiées pour améliorer la mobilisation et l'acquisition des formes OP par les plantes. Il s'agit notamment de l'identification et de la sélection d'espèces/génotypes cultivés sur la base de leurs traits fonctionnels. Cette approche utilise des traits morphologiques, architecturaux et physiologiques, des micro-organismes ou une combinaison des deux pour accéder à des formes de OP peu disponibles. En général, ces caractéristiques pourraient être classées en trois types de stratégies d'acquisition du P : La stratégie de " foraging ", la stratégie de "

mining " et une stratégie combinant les deux. La stratégie de " foraging "de P des plantes est l'acquisition de P dans la solution du sol par des traits morphologiques et architecturaux en maximisant l'exploration du sol. Grâce à ces stratégies, les plantes peuvent induire un gradient de diffusion qui, à son tour, favoriserait le processus de désorption des différentes formes de OP adsorbées [START_REF] Fang | Phosphorus adsorption onto clay minerals and iron oxide with consideration of heterogeneous particle morphology[END_REF]White et Hammond, 2008). La stratégie de " foraging "implique des traits morphologiques tels que la longueur spécifique des racines, le pourcentage de racines fines et la surface des racines, et des traits architecturaux incluant la densité de la longueur des racines, la biomasse racinaire et la formation de racines groupées ou de symbioses mycorhiziennes à arbuscules qui permettent aux plantes d'augmenter leur capacité de butinage. La la stratégie de " mining " du P par les plantes, est l'acquisition du P dans la solution du sol par des traits physiologiques qui sont libérés dans le sol par les racines, y compris les 2), indiquant que les OP adsorbés peuvent agir comme une source de P pour les plantes (Amadou et al., 2022b). La tendance de la disponibilité des OP (GLY >> G6P > IHP) mise en évidence dans le chapitre 2 a été potentiellement expliquée par leur dynamique de désorption distincte (chapitre 1), car la désorption la plus faible a été trouvée pour IHP-P, suivie par G6P-P et ensuite GLY-P (chapitre 2).

Cette tendance pourrait également être liée à leurs différents degrés d'hydrolyse par l'activité enzymatique (Annaheim et al., 2010), puisque l'activité phosphatase était la plus élevée en présence de GLY et la plus faible en présence de IHP (chapitre 2).

La relation positive entre la dynamique d'adsorption des OP et le nombre de groupes phosphates dans la molécule organique (chapitre 1) était cohérente avec la littérature et montre que la capacité d'adsorption de chaque composé OP est déterminée par le nombre de groupes orthophosphates associés à la fraction C (Bai et al., 2021). Le IHP, qui possède six orthophosphates par fragment C, a été adsorbé en plus grande quantité que les autres monoesters d'orthophosphate (G6P et GLY), ce qui renforce les explications précédentes concernant sa faible désorption (chapitres 1 et 2) et son utilisation limitée par les plantes (chapitre 2). La force de liaison généralement plus faible ou égale du myo-HP aux minéraux par rapport au GLY ou au G6P (chapitre 1), bien qu'en désaccord avec des résultats récents (Ganta et al., 2019 ;Kubicki et al., 2012) a souligné le fort potentiel d'utilisation du GLY comme source de P dans ces régions (Zhang et al., 2017). La faible absorption de P par les complexes kaolinite-OP (chapitre 2) est cohérente avec les observations précédentes montrant que la kaolinite-P est un complexe de surface bidenté, à sphère interne, en dessous de pH 6 (Hu et al., 2020 ;Ruyter-Hooley et al., 2015), et que le P adsorbé sur la kaolinite est difficile à désorber (Kafkafi et al., 1988 ;Xiong et al., 2022). Cela souligne donc que les oxyhydroxydes de Fe et d'Al étaient moins responsables de la limitation de la disponibilité des OP que la kaolinite, malgré leur capacité d'adsorption généralement plus élevée dans le sol (chapitre 1).

Cependant, étant donné que la concentration en P utilisée dans notre étude peut être plus élevée que celle des systèmes de sol réels, il serait intéressant comme perspective d'étudier l'effet de la concentration en P sur les processus d'adsorption en réalisant des expériences de sorption à des concentrations en P différentes (et plus faibles).

Preuve d'une mobilisation importante des OP par les plantes en raison des interactions N-OP et des réponses des traits des plantes

il semble probable qu'avec l'ajout de N, l'OP soit recyclée plus intensivement à partir des pools d'OP, indépendamment des minéraux du sol (Widdig et al., 2019). L'interaction de N avec les formes IP a conduit à une plus grande absorption de P et à une limitation de P nettement réduite par rapport à l'interaction de N avec les formes OP, probablement en raison de la forte adsorption et de la faible disponibilité de l'OP, comme le montrent les chapitres 1 et 2. Ainsi, on peut déduire que dans les agro- La conception d'une meilleure disponibilité du P dans les agroécosystèmes via la gestion de la teneur en N des amendements organiques et des traits d'acquisition du P par les plantes peut donc contribuer à relever des défis majeurs tels que l'augmentation de l'utilisation d'engrais recyclés (Faucon et al., 2015).

Cependant, cela suggère une réflexion approfondie lors de la conception de la composition des cultures et de l'approvisionnement en amendements (Hallama et al., 2019). Une implication majeure de cette Par conséquent, dans un système de rotation, cela pourrait améliorer la disponibilité du P qui profiterait alors aux cultures suivantes, qui sont généralement non mobilisatrices (Haling et al., 2018). En pratique, étant donné que les apports organiques augmentent lentement la disponibilité du P du sol pour les plantes après incorporation dans le sol (Gerke, 2015), ces espèces de Fabaceae pourraient être le premier choix dans une rotation de cultures ou dans une culture de couverture pour améliorer la teneur en P des cultures

  grade de Docteur de l'Université de Picardie Jules Verne Rôle des formes de phosphore organique, des minéraux du sol, de l'azote et des traits fonctionnels des plantes sur la disponibilité et l'acquisition du phosphore par les plantes AVANT-PROPOS Ce projet de thèse a débuté en octobre 2019 et est financé par FEDER/FSE Picardie 2014-2020 et UniLaSalle (rattaché à l'Université Picardie Jules Verne), basé à Beauvais (France). Le projet est réalisé au sein de l'équipe de recherche AGHYLE (Agroécologie, Hydrogéochimie, Environnements et Ressources) d'UniLaSalle. Le manuscrit de la thèse est rédigé comme une thèse sur articles en anglais. Les chapitres 1 et 2 ainsi qu'un article de synthèse (présenté dans l'introduction générale) ont été publiés dans des revues internationales et les chapitres 3 et 4 sont en cours de correction pour publication dans une revue internationale. Une liste des publications est disponible à la fin du manuscrit, ainsi qu'un résumé étendu du manuscrit en français.

  je me suis contenté de les prendre pour alliés, quitte à faire preuve de beaucoup d'abnégation et à dompter mon âme... ******************************************* Aussi, Par ce manuscrit, je rends hommage à tous les enseignants du monde Voici mes vers :

Figure 1 :Figure 2 :Figure 3 :Figure 4 :Figure 5 :Figure 6 :Figure 7 :Figure 8 :Figure 9 :Figure 11 :Figure 12 :Figure 13 :Figure 14 :Figure 15 :Figure 17 :Figure 18 :Figure 19 :Figure 20 :Figure 21 :Figure 25 :Figure 26 :Figure 27 :Figure 28 :Figure 29 :Figure 30 :Figure 33 :Figure 34 :

 123456789111213141517181920212526272829303334 Figure 1: Chemical structure of IHP ..................................................................................................... 23 Figure 2: Chemical structure of β-D-Glucopyranose-6-phosphate ....................................................... 26 Figure 3: Chemical structure of Glycerol 2-phosphate. ........................................................................ 27 Figure 4: Plausible surface complexes of OP compounds at soil properties interface.e.g. Inner-sphere complex of β-D-Glucopyranose-6-phosphate with iron (oxy)hydroxides. ........................................... 30 Figure 5: Plausible surface complexes of OP compounds at soil properties interface.eg. Outer-sphere complex of β-D-Glucopyranose-6-phosphate with iron (oxy)hydroxides. ........................................... 30 Figure 6: Organic input-soil-plant system-related biogeochemical processes that may ultimately modify the dynamics of the OP pool in the rhizosphere. ................................................................................... 49 Figure 7: The main objectives of the thesis project. OP: Organic P, IHP: Myo-inositol hexakisphosphate, GLY: glycerophosphate, G6P: glucose-6-phosphate, and IP: Inorganic P; N: nitrogen ....................... 72 Figure 8: RHIZOtest device experiment setting .................................................................................... 77 Figure 9: Experiment setup ................................................................................................................... 78 Figure 10: Experimental mesocosms, with square petri dishes ............................................................. 81 Figure 11: Chemical structure of potassium dihydrogen phosphate, IP (a), myo-inositol hexakisphosphate, IHP (b), β-D-Glucopyranose-6-phosphate, G6P (c) and Glycerol phosphate, GLY(d) ............................................................................................................................................................. 111 Figure 12 : Adsorption isotherms of OP forms by different soil minerals in 0.1 M KCl at pH 5.5 ... 115 Figure 13: Desorption kinetics of IHP, GLY and G6P by 0.1 M KCl at pH 5.5 and at 25°C ............. 118 Figure 14: Variation in P desorption rates of mineral-OP complexes ................................................. 120 Figure 15: Successive desorption of (a) IHP, (b) GLY and (c) G6P from OP-mineral complexes by KCl ............................................................................................................................................................. 122 Figure 16: Conceptual framework showing the linkage among soil minerals properties (PZC, SSA) and adsorption/desorption parameters (bonding strength, KL; adsorption capacity, Qm, and desorption capacity, Dm). ..................................................................................................................................... 123 Figure 17: Picture of the experimental Setup and Plant growth using the RHIZOtest device. ........... 142 Figure 18: Phosphorus uptake by root and shoot ryegrass plants with different P sources. ................ 147 Figure 19: Phosphatase activity in the rhizosphere at the end of the experiment. ............................... 148 Figure 20: Relationship between P uptake and the different methods of P extraction (ΔP resin: difference in resin P concentration between bulk soil and rhizosheath. ............................................................... 149 Figure 21: Relationship between Δ resin P (difference in resin P concentration between bulk soil and rhizosheath) and P uptake. ................................................................................................................... 150 Figure 22: Picture of the experimental Setup and Plant growth .......................................................... 167 Figure 23 : Effect of N, P and soil mineral interactions on total biomass production by ryegrass. .... 171 Figure 24: Effect of N forms, and their interactions with minerals-P complexes on N:P ratios. ........ 172

  ............................................................................................................................................................. 170 Table 20 : Percent of P recovered by ryegrass from adsorbed OP complexes with the addition of N forms. ................................................................................................................................................... 173

Figure 1 :

 1 Figure 1: Chemical structure of IHP

Figure

  Figure 2: Chemical structure of β-D-Glucopyranose-6-phosphate

Figure

  Figure 3: Chemical structure of Glycerol 2-phosphate.

  studied sorption of different OP (GLY, ATP and IHP) on aluminium (oxyhydr)oxides. They found that the maximum adsorbed phosphate normalized to the mass of adsorbent increases with decreasing crystallinity of the minerals: Al2O3 < boehmite AlO (OH) < amorphous Al (OH)3. Moreover, they concluded that OP adsorption and phosphate fate in the environment are strongly affected by the degree of crystallinity and crystal structure of mineral surfaces.

Figure 4 :

 4 Figure 4 : Plausible surface complexes of OP compounds at soil properties interface.e.g. Inner-sphere complex of β-D-Glucopyranose-6-phosphate with iron (oxy)hydroxides. (a) Inner-sphere mono-dentate mono-protonated complex pH = 1-7, (b) Inner-sphere bi-dentate complex pH = PZC, (c) mono-dentate mono-protonated complex characterized by Lewis Acid-Base Interaction pH = 8-12 and (d) mono-dentate unprotonated complex characterized by Lewis Acid-Base Interaction pH = 8-12.

Figure 5 :

 5 Figure 5 : Plausible surface complexes of OP compounds at soil properties interface.eg. Outer-sphere complex of β-D-Glucopyranose-6-phosphate with iron (oxy)hydroxides.

Figure 6 :

 6 Figure 6: Organic input-soil-plant system-related biogeochemical processes that may ultimately modify the dynamics of the OP pool in the rhizosphere.

Figure 7 :

 7 Figure 7: The main objectives of the thesis project. OP: Organic P, IHP: Myo-inositol hexakisphosphate, GLY: glycerophosphate, G6P: glucose-6-phosphate, and IP: Inorganic P; N: nitrogen

Figure 8 :

 8 Figure 8 : RHIZOtest device experiment setting

Figure

  Figure 9 : Experiment setup

  representatives of the major soil minerals: goethite [Fe (OH)O] was chosen as representative of iron oxyhydroxide, and kaolinite as a clay mineral. The two soil minerals were loaded with the two OP compounds or inorganic P to serve as a P source for the different species. Eight (sub)species of diverse phylogenetic lineages (Poaceae: Hordeum vulgare, Lolium perenne; Fabaceae: Lens culinaris Medik., Pisum sativum subsp. arvense L., Trifolium alexandrinum L., Vicia faba L., Lupinus albus;

Figure

  Figure 10: Experimental mesocosms, with square petri dishes

Figure 11 :

 11 Figure 11 : Chemical structure of potassium dihydrogen phosphate, IP (a), myo-inositol hexakisphosphate, IHP (b), β-D-Glucopyranose-6-phosphate, G6P (c) and Glycerol phosphate, GLY(d)

1 𝛽 and 𝐵 = 1 𝛽

 11 𝐿𝑛𝛼 𝛽 (α and β are the constants in the original formula of Elovich equation). The A value (mgP kg-1 )

Figure 12 :

 12 Figure 12 : Adsorption isotherms of OP forms by different soil minerals in 0.1 M KCl at pH 5.5 Symbols are data points, solid lines are Langmuir isotherms, and dashed lines are Freundlich isotherms. Gibbsite was different from other minerals because of the large difference in the maximum adsorption amount. Values of adsorbed quantities (Qads) and error bars (Se) are also provided as supplementary data (APPENDIX A TableS2).

  strong than with IP. The results for the adsorption capacity and binding energy of montmorillonite are only valid for the K-saturated montmorillonite used in this study. Al or Ca saturated montmorillonite would result in different adsorption mechanisms. Figure16illustrates a conceptual framework showing the relationship between soil mineral properties (PZC, SSA) and Langmuir model adsorption parameters (KL and Qm). A positive relationship was found between the ability of soil minerals to adsorb and strongly bind OP and the chemical and physical properties of the soil minerals (PZC, SSA).

Figure 13 :

 13 Figure 13 : Desorption kinetics of IHP, GLY and G6P by 0.1 M KCl at pH 5.5 and at 25°C

Figure 14 :

 14 Figure 14 : Variation in P desorption rates of mineral-OP complexes

  clay minerals than from the Fe and A1 oxides, but from the second cycle, Fe and Al oxides had desorbed almost as much IHP and GLY as the clays. At the fourth cycle, the amount of IHP

Figure 15 :Figure 16 :

 1516 Figure 15 : Successive desorption of (a) IHP, (b) GLY and (c) G6P from OP-mineral complexes by KCl

Figure 17 :

 17 Figure 17: Picture of the experimental Setup and Plant growth using the RHIZOtest device. a-soil layer of quartz -mineral-OP complex; b-preculture period; c-contact between the soil and plant device; d-result at the end of the experiment.

Figure 18 :

 18 Figure 18: Phosphorus uptake by root and shoot ryegrass plants with different P sources.

  Means with different letters were significantly different according to Tukey's HSD test at P < 0.05. Error bars indicate standard error. Soils minerals (Go: goethite, Gib: gibbsite, K: kaolinite, and M: montmorillonite); Phosphorus compounds (IHP: myoinositol hexakisphosphate, GLY: glycerophosphate, G6P: glucose-6-phosphate and IP: KH2PO4); The dashes (-) identify the mineral-phosphorus complexes produced by the adsorption of P forms onto soil minerals. Example Go-IHP refers to goethite and myo-inositol hexakisphosphate complexes.

Figure 19 :

 19 Figure 19: Phosphatase activity in the rhizosphere at the end of the experiment. Means with different letters were significantly different according to the Tukey's HSD test at P < 0.05. Error bars indicate standard error. Soils minerals (Go: goethite, Gib: gibbsite, K: kaolinite, and M: montmorillonite); Phosphorus compounds (IHP: myo-inositol hexakisphosphate, GLY: glycerophosphate, G6P: glucose-6-phosphate and IP: KH2PO4); The dashes (-) identify the mineral-phosphorus complexes produced by the adsorption of P forms onto soil minerals. Example Go-IHP refers to goethite and myo-inositol hexakisphosphate complexes.

Figure 20 :

 20 Figure 20 : Relationship between P uptake and the different methods of P extraction (ΔP resin: difference in resin P concentration between bulk soil and rhizosheath. KCl.P: KCl extracted P). Values are average (n = 4) ± standard deviations. All values are means (n = 4) ± standard deviations. The marked correlation coefficient r is the Pearson's correlation coefficient. *p < 0.05; **p < 0.01; ***p < 0.001. Dots colors distinguish the forms of P. Red dots correspond to myo-inositol hexakisphosphate (IHP), green to glucose-6-phosphate (G6P)and blue to glycerophosphate (GLY). Dots colors distinguish the forms of P. Red dots correspond to myo-inositol hexakisphosphate (IHP), green to glucose-6-phosphate (G6P) and blue to glycerophosphate (GLY).

Figure 21 :

 21 Figure 21: Relationship between Δ resin P (difference in resin P concentration between bulk soil and rhizosheath) and P uptake. Soils minerals (Go: goethite, Gib: gibbsite, K: kaolinite and M: montmorillonite); Phosphorus compounds (IHP: myo-inositol hexakisphosphate, GLY: glycerophosphate, G6P: glucose-6-phosphate and IP: KH2PO4 ); The dashes (-) identify the mineralphosphorus complexes produced by the adsorption of P forms onto soil minerals. Example Go-IHP refers to goethite and myo-inositol hexakisphosphate complexes.

Figure 22 :

 22 Figure 22: Picture of the experimental Setup and Plant growth

Figure 23 :Figure 24 :

 2324 Figure 23 : Effect of N, P and soil mineral interactions on total biomass production by ryegrass.The interaction effect of N forms, P compounds and soil minerals on total biomass was significant (P < 0.05) according to GLM model results testing the impact of factors (N forms, P compounds, soil minerals, and their combined effect) on total biomass. Means with different letters were significantly different according to Tukey's HSD test at P < 0.05. Error bars indicate standard error. Soils minerals (Go: goethite and K: kaolinite); N forms (NO3-N: nitrate and NH4-N: Ammonium); Phosphorus compounds (IHP: myo-inositol hexakisphosphate, GLY: glycerophosphate and IP: KH2PO4); The dashes (-) identify the mineral-phosphorus complexes produced by the adsorption of P forms onto soil minerals. Example Go-IHP refers to goethite and myo-inositol hexakisphosphate complexes.

  of P recovered by ryegrass from adsorbed OP complexes with the addition of N forms.

Figure 25 :

 25 Figure 25: Effect of N, P and soil mineral interactions total P uptake by ryegrass plants with different mineral-P complexes.

Figure 26 :Figure 27 :

 2627 Figure 26 : Changes in foliar N (c), P (c), rhizosphere pH (c) and available P (c) in response to N addition

  soil minerals: goethite [Fe (OH)O] was chosen as representative of iron oxyhydroxide, and kaolinite as a clay mineral, particularly the 1:1 phyllosilicate. All mineral powders were purchased from Sigma-Aldrich Chemie and VWR (France) for the experiments. Eight (sub)species of diverse phylogenetic lineages (Poaceae: Hordeum vulgare, Lolium perenne; Fabaceae: Lens culinaris Medik., Pisum sativum subsp. arvense L., Trifolium alexandrinum L., Vicia faba L., Lupinus albus; Hydrophyllaceae:

Figure 29 :

 29 Figure 29 : Principal component analysis (PCA) of P-acquisition strategies involved in phosphorus acquisition from inorganic P form (a) and organic P forms (IHP and GLY) (b). Analysis was performed irrespective of minerals. (1) Variable covariation along first two components, (2) groups/clusters formed with classification on PCA. Abbreviations: DpH: change in rhizosheath pH; FR: percentage roots with diameters less than 0.5 mm; Leaf[P]: foliar phosphorus concentration; PME: acid phosphomonoesterase activity; RLD: root length density;

Figure 30 :

 30 Figure 30 : Partial least square-path models predicting phosphorus uptake. Based on three latent variables, namely root physiological traits, root morphological traits and intermediate in tree IP and organic P (IHP and GLY) Corr is the correlation effect. Variables negatively transformed indicated by -(variable). GoF = Goodness of Fit of the model. ΔpH: change in rhizosheath pH; FR: percentage roots with diameters less than 0.5 mm; PME: acid phosphomonoesterase activity; RLD: root length density; RSA: root surface area

Figure 31 :

 31 Figure 31: Illustration summarizing the effects of OPs and soil mineral interactions properties on OP dynamics and plant P availability. OP: Organic P, IHP: Myo-inositol hexakisphosphate, GLY: glycerophosphate, G6P: glucose-6-phosphate, and IP: Inorganic P; Fe and Al oxides included goethite and gibbsite and clay minerals included kaolinite and montmorillonite

Figure 32 :

 32 Figure 32 : Synthesis of the effect of N-OP interactions and plant trait responses on OP mobilization by plants.

  traits involved in mining and foraging OPs and their ability to better predict P acquisition Design of crop species composition and more specifically the functional structure of crop communities (e.g. intercrops, cover crops...) to estimate total soil OP reserves and at least its specific forms (IHP, G6P, GLY, etc.) in a multi-species cropping Need for highlighting the major traits involved in OP-based mining and foraging and their contribution to

Figure 34 :

 34 Figure 34: Proposed process for a C-N-P model to improve the efficiency of OP use and measure its impact on P limitation.The basic processes existing in C-N-P models have been simplified (processes that include the blue arrows). Black arrows connect the processes proposed in our study (globally non-considered in C-N-P models) and blue arrows represent the simplified processes of C-N-P models from previous studies. The red-green icons show the C-N-P interactions that are generally considered. The

  l'optique d'une gestion plus durable du P dans les systèmes de culture, les amendements organiques renouvelables et riches en nutriments sont de plus en plus considérés comme un complément aux engrais P produits à partir de roches phosphatées, non seulement par les scientifiques mais aussi par les politiciens et les parties prenantes. L'utilisation d'intrants organiques représente le passage d'une utilisation linéaire d'une ressource limitée à une économie circulaire, car elle favorise la réduction de l'utilisation des combustibles fossiles et des émissions de gaz à effet de serre, tout en contribuant au développement de nouveaux marchés verts et d'emplois en favorisant la conversion des déchets en produits à valeur ajoutée. L'utilisation d'intrants biologiques privilégie la transition vers une agriculture durable, en mettant l'accent sur la prévention des impacts environnementaux, grâce à l'adoption de systèmes technologiques innovants. L'avantage en termes de durabilité de l'utilisation de P organique renouvelable dépend des systèmes agricoles associés à de faibles émissions de carbone provenant du trafic de P renouvelable, tels que les systèmes d'élevage qui utilisent des effluents ou des digestats, ou d'autres systèmes agricoles qui utilisent des coproduits de l'agro-industrie à l'échelle du territoire, et les systèmes d'agriculture urbaine et périurbaine qui valorisent les boues. L'utilisation d'intrants organiques comme ressource durable et renouvelable est une nécessité pour répondre aux questions socioéconomiques et scientifiques qui ont été récemment soulevées concernant les approches de gestion durable du P. Par exemple, en France, 78 % et 62 % du P et du N, respectivement, utilisés en agriculture proviennent d'intrants organiques. En 2007, on estime qu'un total de 10 millions de tonnes de boues d'épuration ont été produites dans l'UE. Ce chiffre devrait dépasser 13 millions de tonnes en 2020 et continuer à augmenter en raison de la mise en oeuvre de la directive sur le traitement des eaux urbaines résiduaires (directive 91/271/CE). Cependant, contrairement aux engrais P conventionnels, tels que le superphosphate triple, le P est présent dans les intrants organiques sous diverses formes inorganiques et organiques qui varient dans leur disponibilité pour les plantes. La plupart des recherches sur le devenir du P appliqué au sol se sont concentrées sur la dynamique du P inorganique (IP). En revanche, le devenir des formes de OP, qui peuvent représenter jusqu'à 80 % du P total du sol, a été négligé jusqu'à présent, et il reste un manque de connaissances sur la contribution de ces formes à la nutrition des plantes. Des études ont montré que le P provenant d'apports organiques pouvait être plus disponible que le P provenant d'engrais chimiques. Cependant, cette disponibilité était affectée par les minéraux du sol, les niveau et formes de d'azote (N) et les traits d'acquisition du P des racines des plantes cultivées. Par conséquent, une meilleure compréhension des interactions entre les formes de OP, les minéraux du sol, les caractéristiques des racines et les microbiomes de la rhizosphère, peut aider à mieux gérer la fertilisation en P organique.Rôle des minéraux du sol dans la dynamique du phosphore organiqueLes minéraux du sol tels que les oxyhydroxydes de fer (Fe) et d'aluminium (Al) (par exemple, la goethite et la gibbsite, respectivement) et les minéraux argileux (par exemple, la kaolinite, la montmorillonite) sont des composants majeurs du sol. Ils ont fait l'objet d'une attention considérable en raison de leur forte capacité d'adsorption du P qui peut conduire à une utilisation inefficace des OP dans les sols (de 5 à 10 %). Cela conduit à une piètre utilisation des sources d'OP dans les agroécosystèmes. En effet, des formes spécifiques d'OP telles que l'inositol hexakisphosphate (IHP), le glycérophosphate (GLY) et le glucose-6-phosphate (G6P), sont généralement considérées comme des formes majeures dans les engrais organiques. Chaque forme diffère des autres par sa teneur en P et sa taille moléculaire. Ces composés organiques de P adsorbés sur les minéraux se sont avérés être les formes les plus stables de P dans différents types de sol. Cela est dû à leur mécanisme de liaison spécifique. En effet, il a été constaté que le nombre de groupes phosphate dans un certain composé OP détermine la stabilité de son complexe avec la surface minérale. Par exemple, l'IHP, avec ses six groupes phosphates, présente généralement une forte liaison et une grande stabilité par rapport à d'autres composés OP ou IP qui ont un plus petit nombre de groupes phosphates. Jusqu'à quatre groupes phosphates de l'IHP interagissent avec la surface de la goethite, ce qui entraîne la formation de complexes de sphère interne entre les groupes phosphates de l'IHP et la surface de la goethite. Un mécanisme similaire a été suggéré pour d'autres complexes OPminéraux. La désorption du P des surfaces minérales serait plus limitée pour les composés OP que pour les IP. Cependant, la mesure dans laquelle les composés OP adsorbés aux minéraux du sol peuvent se désorber reste mal comprise et leur disponibilité pour les plantes est encore débattue. Il a été suggéré que les complexes minéraux-OP ne sont pas disponibles pour les plantes parce que ces complexes sont formés pendant la phase de réaction lente avec les minéraux du sol. Ce processus a été supposé être une cause majeure de la limitation de la croissance des plantes. Ainsi, il a été suggéré que la disponibilité de l'OP est principalement limitée par sa solubilité et non par l'activité enzymatique. Quoi qu'il en soit, l'affinité des composés OP pour les minéraux du sol est plus grande que celle des composés IP, ce qui indique la formation d'un complexe très stable d'OP avec les surfaces minérales. Par conséquent, on peut s'attendre à ce que la désorption et la disponibilité pour les plantes des complexes minéraux-OP soient plus faibles que celles des composés IP. Cependant, les très rares études sur les OP ne permettent pas de quantifier correctement leur contribution potentielle à la disponibilité du P dans le système engrais organique-sol-plante. À ce jour, on ne sait pas comment les formes chimiques des OP, et leurs interactions avec les minéraux du sol, influencent l'absorption du P à partir des OP par les plantes dans les écosystèmes. La rareté des recherches sur le processus limite considérablement notre capacité à comprendre la dynamique globale du cycle du P dans les écosystèmes et à optimiser l'utilisation des engrais P renouvelables qui contiennent souvent diverses formes d'OP.Processus biogéochimiques impliqués dans la disponibilité et la limitation des OP : influence des formes de N et d'OP et de leur interaction avec les minéraux du sol sur la disponibilité et l'absorption de P par les plantesLes intrants organiques, en plus des différentes formes d'OP qu'ils contiennent, diffèrent également en termes de concentration en N. Les interactions N-OP jouent un rôle majeur dans la dynamique des OP, créant des effets de Co-limitation ou de synergie selon leurs concentrations. Les interactions N-OP jouent un rôle majeur dans la dynamique des OP, créant des effets de Co-limitation ou de synergie en fonction de leurs concentrations, ce qui explique que la fertilisation organique soit gérée conjointement dans le système de culture. Ces interactions déterminent si les plantes sont limitées par le P, ou à la fois par le N et le P, ce qui influence la productivité et le fonctionnement des écosystèmes. L'ajout d'azote affecte l'absorption de P par les plantes directement en favorisant la croissance des plantes et la production de protéines, mais aussi indirectement en interagissant avec les pools de OP du sol. En particulier, il est bien connu que selon sa forme inorganique dans la solution du sol (c'est-à-dire NH4-N ou NO3-N), l'azote peut augmenter ou diminuer la solubilité de l'OP, ce qui entraîne des changements dans la limitation et la disponibilité du P. Globalement, il a été déclaré que les plantes pourraient échanger N contre P en ajustant les taux d'acquisition de N et de P du sol, expliquant potentiellement les réponses synergiques de la croissance à l'ajout de N et de P. En outre, selon la disponibilité du P, l'effet de l'azote peut être plus ou moins prononcé, ce qui entraîne une limitation du P différenciée entre les formes IP et OP. Les avantages de l'ajout de N sur le cycle du P dépendent aussi fortement des propriétés des minéraux impliqués. Cela suggère que l'interaction entre les formes d'azote et les minéraux du sol est également cruciale dans le processus de mobilisation des formes de P. Le cycle de N et du OP dans l'écosystème consiste en de multiples bassins biogéochimiques et processus qui sont liés et interdépendants, contrôlant conjointement la disponibilité du P dans le sol, l'absorption du P par les plantes et la limitation du P. À ce jour, la manière dont les formes de N, les formes chimiques de OP et leurs interactions avec les minéraux du sol influencent à la fois la limitation du P et l'absorption par les plantes dans les écosystèmes n'est toujours pas claire. La rareté des recherches sur l'effet de ces importants processus biogéochimiques (N-OP-minéraux du sol) limite considérablement notre capacité à comprendre les processus écologiques qui sous-tendent l'altération du cycle du OP dans les écosystèmes avec les ajouts d'azote. Plus important encore, cela limite notre capacité à comprendre le cycle du P dans l'écosystème. Une meilleure compréhension du cycle du P de l'écosystème en cas d'ajouts de N et des propriétés biogéochimiques impliquées est nécessaire non seulement pour permettre aux modèles d'écosystème de prédire avec précision la limitation de N-P des plantes et ses impacts, mais aussi pour développer des modèles d'écosystème robustes avec des interactions N-P ou C-N-P entièrement couplées.

  glucides, les acides organiques et aminés, les composés phénoliques, les protéines, les acides gras, les stérols, les enzymes, les polysaccharides et les phospholipides. La stratégie collective fait référence à l'investissement de ressources par les plantes pour interagir avec la communauté microbienne afin d'accéder aux OP du sol. Plusieurs espèces végétales sont supposées être relativement efficaces dans l'utilisation des OP sans l'aide du microbiome de la rhizosphère. Les défis de la mobilisation et de l'acquisition des OP sont de comprendre la réponse des traits fonctionnels des plantes en fonction des formes d'OP et des propriétés du sol pour améliorer l'acquisition et la mobilisation du P des espèces cultivées. Globalement, les traits d'acquisition du P des plantes sont connus et leurs effets indirects et parfois même directs sur l'acquisition/mobilisation du P ont été démontrés. Les processus diffèrent en fonction de la nature des formes IP ou OP (phosphate mono ou diester) et des propriétés physico-chimiques du sol. Ainsi, la disponibilité des différentes formes OP (IHP, G6P, GLY, ADN et ARN) en tant qu'effet direct des stratégies d'acquisition du P (P-foraging, mining) reste peu claire probablement en raison de sa forte liaison au sol. Ainsi, il a été suggéré que les stratégies des plantes peuvent être exploitées en utilisant des combinaisons d'espèces avec des stratégies contrastées ou en utilisant une seule espèce pour mieux comprendre leurs effets réels sur la mobilisation et l'acquisition des OP dans les agroécosystèmes. En bref, une meilleure compréhension de l'impact des stratégies d'acquisition du P sur la mobilisation et l'acquisition des OP par les plantes, qui sont liées aux multiples traits morphologiques et physiologiques et aux interactions entre eux, est essentielle pour la gestion de la disponibilité des OP. Par rapport à la IP, la réponse des stratégies d'acquisition du P aux composés OP et leur impact sur l'acquisition du P dans les sols amendés avec diverses formes d'OP ont reçu beaucoup moins d'attention. Les caractéristiques des espèces cultivées pourraient être utilisées pour augmenter la mobilisation des OP, ce qui aiderait à repenser la fertilisation en P, à maintenir la production et à recycler davantage d'OP dans les sols amendés avec des amendements organiques.ObjectifsCe projet de doctorat vise à mieux comprendre le rôle des formes de P organique, des minéraux du sol, de l'azote et des traits fonctionnels des cultures et leurs interactions sur la disponibilité et l'acquisition du P par les plantes pour optimiser la gestion des fertilisants organiques dans les agrosystèmes. Pour répondre à cet objectif général, quatre chapitres ont été produits pour examiner les questions centrales et toujours en suspens.Le chapitre 1 a examiné la dynamique de sorption et la désorption des formes majeur du P organique sur la goethite, la gibbsite, la kaolinite et la montmorillonite avec pour objectif de d'élucider la dynamique de l'adsorption et de la désorption de plusieurs formes d'OP sur plusieurs minéraux du sol représentatifs des different type de sol. Plus spécifiquement, il s'agissait de déterminer les facteurs déterminants de l'adsorption et de la désorption des OP sur les minéraux du sol.Le chapitre 2 a ensuite examiné le rôle des minéraux du sol sur la disponibilité du OP et l'absorption du P par les plantes avec pour objectif d'élucider dans quelle mesure l'OP lié aux oxyhydroxydes de Fe et d'Al et aux complexes de minéraux argileux contribue à l'acquisition de P par les plantes. Plus précisément, nous avons déterminé la disponibilité du P pour les plantes à partir de plusieurs complexes de IHP, G6P et GLY qui ont été adsorbés sur des oxyhydroxydes de Fe et d'Al (goethite et gibbsite) et des minéraux argileux (kaolinite et montmorillonite). Les trois principales hypothèses suivantes ont été abordées : (1) le P des composés OP adsorbés est disponible pour le ray-grass et varie avec les propriétés minérales du sol ; (2) l'absorption relative du P des différents complexes OP-minéraux dépend de leur force de liaison et (3) les composés OP adsorbés sont moins disponibles que l'IP adsorbé car il se désorbe moins et nécessite non seulement une désorption mais aussi un clivage enzymatique avant d'être absorbé par le ray-grass. 6-phosphate (G6P) et de composés de P inorganique (IP) qui ont été préalablement adsorbés sur des oxyhydroxydes de Fe et d'Al (goethite et gibbsite, respectivement) et des minéraux argileux (montmorillonite et kaolinite). La disponibilité du P et l'absorption de P ont ensuite été déterminées par la caractérisation de la rhizosphère et des plantes. Indépendamment du type de minéral, le ray-grass a été capable d'absorber environ 3-18% des composés OP adsorbés. L'ampleur de la disponibilité et de l'absorption dépendait des composés OP et du type de minéraux du sol. La disponibilité potentielle des OP adsorbés par différents minéraux a été fortement médiée par les types et les propriétés de l'interaction minéral-OP. L'absorption de P a augmenté dans l'ordre suivant : kaolinite-OP << gibbsite-OP ≤ goethite OP << montmorillonite-OP. L'absorption de P à partir des composés OP adsorbés a montré des tendances contrastées par rapport à l'IP adsorbé et dépendait davantage de la concentration de P disponible dans la rhizosphère plutôt que de la force de liaison des OP à la surface minérale. Chapitre 3 : L'azote et la minéralogie du sol déterminent la limitation du phosphore et l'absorption de P par les plantes à partir de formes inorganiques et organiques de P Les cycles de l'azote et du phosphore dans les écosystèmes sont composés de multiples formes et processus biogéochimiques qui contrôlent conjointement l'absorption et la limitation du P par les plantes. À ce jour, la manière dont les formes chimiques de l'azote, le P organique (OP) et leurs interactions avec les minéraux du sol influencent à la fois la limitation du P et son absorption par les plantes dans les écosystèmes n'est toujours pas claire. La rareté des recherches sur l'effet de ces importants processus biogéochimiques (N-P-minéraux du sol) limite considérablement notre capacité à comprendre les processus écologiques qui sous-tendent l'altération du cycle du P dans les écosystèmes avec des ajouts d'azote. Les objectifs de cette étude étaient d'évaluer les effets indépendants et interactifs des formes de N et P et leur interaction avec les minéraux du sol sur l'absorption et la limitation du P chez les plantes. Nous avons caractérisé le rapport N:P, l'absorption de P et les propriétés de la rhizosphère du ray-grass cultivé sous plusieurs complexes d'IP et d'OP (IHP et GLY) adsorbés sur des oxyhydroxydes de Fe (goethite) et des minéraux argileux (kaolinite) avec et sans ajout de N. Nous avons émis l'hypothèse que l'ajout de N sous diverses formes spécifiques augmenterait la limitation de P dans des conditions de faible disponibilité de P, c'est-à-dire, avec les formes d'OP et les minéraux du sol, et que le passage des plantes d'une limitation de N à une limitation de P serait dû à l'effet bénéfique de l'ajout d'azote. Nous avons constaté que les interactions entre les formes de N, les formes de P et les minéraux du sol modifiaient fortement la dynamique du P, par rapport aux effets individuels. Ces interactions ont augmenté la limitation en P des plantes et l'absorption de P via la modification de la chimie de la rhizosphère. Le degré de limitation du P dépendait fortement du degré de disponibilité des sources de P, nous avons donc constaté que l'interaction entre les formes de P et les minéraux du sol était un déterminant majeur de la limitation du P. Par conséquent, nous avons constaté que l'interaction de l'azote avec les formes IP a conduit à une plus grande absorption du P et à une réduction marquée de traits physiologiques des racines. Cette étude a montré que la réponse positive des stratégies d'acquisition de P aux formes de OP a conduit à l'acquisition de P à partir de OP, améliorant ainsi potentiellement l'utilisation des ressources renouvelables de OP par l'optimisation des combinaisons de cultures et du type d'engrais P appliqué Discussion générale et perspectives Effet des formes d'OP et des minéraux du sol sur la dynamique des OP et la disponibilité du P pour les plantes Avec l'utilisation croissante d'intrants organiques pour remplacer les engrais minéraux P et la nécessité de récupérer le P du sol, il est essentiel de mieux comprendre les interactions entre les différentes formes d'OP et les minéraux du sol et leurs conséquences sur la disponibilité du P (Amadou et al., 2021). Un grand nombre de recherches ont évalué l'adsorption de diverses sources individuelles de P organique et inorganique sur les sols ou sur les minéraux du sol. Cependant, aucune étude n'a évalué et comparé la désorption du P des principaux composés OP qui ont été adsorbés aux principaux minéraux du sol et leurs conséquences sur la nutrition des plantes (Amadou et al., 2022a, 2022b). Pour aider à combler ce manque de connaissances, les chapitres 1 et 2 ont élucidé la dynamique de l'adsorption et de la désorption de plusieurs formes d'OP sur plusieurs minéraux du sol représentatifs et les conséquences sur l'absorption du P. Les facteurs liés aux propriétés minérales du sol et aux caractéristiques moléculaires des OP ont directement affecté les réactions des OP et leur libération dans le sol (chapitre 1). De même, ces facteurs ont affecté la disponibilité du P dans la rhizosphère et son absorption par la plante (chapitre 2). Toutes les formes OP étudiées (IHP, GLY, et G6P) ont montré des processus d'adsorption contrastés et significativement différents les uns des autres, ainsi que de la forme IP utilisée pour la comparaison (Chapitre 1). Les expériences de désorption ont révélé qu'environ 30% pouvaient être facilement désorbés (Chapitre 1) et que ce P désorbé était disponible pour une utilisation par les plantes (Chapitre

  a suggéré que l'adsorption plus élevée du IHP par rapport aux autres composés OP (chapitre 1) n'implique pas nécessairement que sa capacité et/ou son énergie de liaison soit toujours forte et stable dans toutes les conditions environnementales. Ainsi, il est concevable que dans des conditions d'approvisionnement en intrants organiques, si les espèces GLY et G6P entrent en compétition avec le IHP pour les mêmes sites actifs sur les minéraux du sol, la différence d'énergie de liaison pourrait faciliter la désorption du IHP du sol plus efficacement que celle du GLY et du G6P(Amadou et al., 2022a). L'analyse de corrélation effectuée sur différentes données d'extraction a montré que la disponibilité des OP adsorbés pour les plantes ne dépend pas de leur force de liaison aux minéraux du sol (chapitres 1 et 2) mais plutôt de leur degré d'hydrolyse par les enzymes du sol et des racines (chapitre 2). Nous avons également souligné que l'idée générale d'une adsorption plus élevée des OP par rapport à la IP suggérée par la littérature ne s'applique pas à tous les composés OP puisque, bien que le IHP ait été plus fortement retenu par rapport à la IP, le G6P et le GLY l'ont été plus faiblement.La désorption (chapitre 1) et l'acquisition (chapitre 2) élevées d'OP à partir de la montmorillonite par rapport aux autres minéraux (chapitre 2) ont indiqué que les sols riches en phyllosilicate 2:1 peuvent avoir une plus grande disponibilité de P que les sols riches en oxyhydroxydes de Fe et Al ou en minéraux 1:1. Néanmoins, la désorption plus élevée observée du GLY à partir des oxyhydroxydes d'Al (chapitres 1 et 2), qui sont connus pour limiter la disponibilité du P dans les sols très altérés des régions tropicales,

  écosystèmes où le P est très fortement sorbé (comme les formes OP), les ajouts de N peuvent en effet conduire à un épuisement rapide du P disponible et donc à une très forte limitation du P, mais dans les systèmes où le P est relativement plus disponible (comme les formes IP), les ajouts de N ne conduisent pas à une limitation systématique du P mais plutôt à une colimitation de N et P. Avec l'ajout de N, plus d'OP a été recyclé à partir de minéraux argileux (kaolinite) et a ainsi retardé la limitation de P par rapport aux oxydes de fer et d'aluminium (goethite), ce qui souligne l'importance de considérer le minéral du sol dans la conception des systèmes de culture pour mobiliser l'OP. Ainsi, le chapitre 3 suggère fortement que malgré l'adsorption plus élevée des formes d'OP (chapitre 1), les ajouts de N peuvent effectivement conduire à une efficacité d'utilisation des OP dans le système sol-plante.Pour explorer davantage les mécanismes efficaces de mobilisation de l'OP dans le sol, la réponse des stratégies d'acquisition du P à diverses formes d'OP interagissant avec les minéraux du sol et leurs conséquences sur la disponibilité et l'acquisition de l'OP ont été examinées chez huit espèces végétales majeures (chapitre 4). L'expression différentielle des traits d'acquisition du P parmi les formes d'OP soutient notre hypothèse selon laquelle les stratégies d'acquisition du P (c'est-à-dire la recherche de nourriture et l'extraction) sont affectées par le type de sources d'OP et leurs propriétés biogéochimiques (Wang et Lambers, 2020). Comme pour l'effet des interactions N-OP (chapitre 3), la réponse positive des stratégies d'acquisition du P aux sources d'OP (chapitre 4) a entraîné une plus grande disponibilité du P et son acquisition à partir des OP (figure 32). Indépendamment des stratégies des plantes, l'acquisition plus élevée de P à partir des OP par rapport aux IP (chapitre 4) a montré que, malgré la sorption plus élevée des OP dans le sol (chapitres 1 et 32), les stratégies de recherche et d'extraction de P des plantes ont été capables d'améliorer le cycle et la disponibilité des OP par rapport aux formes IP. Pris ensemble, les résultats des chapitres 3 et 4 suggèrent que les diverses formes de N contenues dans les intrants organiques et les stratégies d'acquisition de P des espèces cultivées peuvent être exploitées pour améliorer la mobilisation des OP dans le système engrais organique-sol-plante (figure 32). L'application agronomique de ce résultat est particulièrement importante pour limiter l'utilisation d'engrais chimiques. Conception de cultures fonctionnellement optimales à forte capacité de mobilisation de l'OP : aperçu de la sélection des espèces, des stratégies d'acquisition du phosphore et des formes d'azote.

  thèse est le potentiel de gérer les formes d'azote dans les intrants organiques tout en adaptant la composition des cultures pour améliorer la disponibilité des OP dans les agroécosystèmes grâce à l'effet avantageux des interactions N-OP (chapitre 3) mais aussi grâce à la réponse positive et à l'effet des stratégies et des traits fonctionnels des plantes (chapitre 4). En général, les interactions N-OP ont entraîné une mobilisation beaucoup plus importante des OP (chapitre 3), de plus, les effets des stratégies d'acquisition du P des différentes espèces discutées dans le chapitre 4 ont été trouvés pour favoriser une plus grande acquisition du P à partir des OP que des IP. Toutes ces observations indiquent que malgré la sorption plus forte des OP au sol démontrée au chapitre 1, qui a limité leur disponibilité pour les plantes au chapitre 2, les stratégies d'extraction et de recherche de P des plantes ont réussi à améliorer le cycle et la disponibilité des OP par rapport aux formes IP (chapitre 4). Pris ensemble, ces résultats peuvent aider à guider la sélection de systèmes de culture efficaces et la formulation de l'azote dans les engrais organiques pour une meilleure mobilisation des formes OP. Les groupes d'espèces composés de Vicia faba, Pisum sativum et Lupinus albus qui ont produit une plus grande exsudation d'acide carboxylique et une activité PME significative dans la rhizosphère que les autres espèces en réponse aux formes OP(Nobile et al., 2019), peuvent bénéficier d'une fertilisation avec des intrants organiques (Figure32). Ces espèces, qui appartiennent toutes à la famille des Fabaceae et dont les stratégies impliquent l'exploitation du P, ont favorisé une plus grande mobilisation/acquisition des OP que des IP.

à

  partir des formes OP du sol. Les espèces Lens culinaris, Hordeum vulgare, et Trifolium alexandrinum qui répondent aux formes d'OP avec un pourcentage élevé de racines fines et de longueur spécifique de racine et une expression intermédiaire des traits de minage du P, peuvent être plus efficaces pour libérer les différentes formes d'OP adsorbées et/ou précipitées sur les constituants du sol, comme l'IHP qui est très fortement adsorbé sur le sol (Figure 32). D'un point de vue agronomique, un système qui combine un engrais organique riche en N sous forme de NO3-N et l'établissement d'espèces de Fabaceae peut être efficace pour utiliser les OP et spécifiquement l'IHP, qui est la principale forme d'OP dans le sol.

Table of content

 of 1 INTRODUCTION .........................................................................................................................

	1.1	ORGANIC PHOSPHORUS SORPTION IN SOILS: PROCESSES, MODELS AND IMPLICATIONS FOR

Table 1 :

 1 Organic P accumulation according to some soil properties ................................................... 21

Table 2 :

 2 Summary of the main investigations on the adsorption of OP forms on soil minerals under pH 4 to 6. ..................................................................................................................................................... 31

Table 3 :

 3 Desorption of P from Boehmite with KCl and Citrate and from different mineral surface saturations of 50% and 100% ................................................................................................................ 33

Table 4 :

 4 Binding patterns of P-forms and their interaction energies per number of bonds (Eint/bond) on goethite and two diaspore surface planes. ............................................................................................. 37

Table 5 :

 5 Total IP and OP forms in organic inputs ................................................................................. 44

Table 6 :

 6 Total IP and OP forms in different soil properties (in mg.kg -1 ). ............................................. 45

Table 7 :

 7 Amount of IP and OP species in organic input ...................................................................... 46

Table 8 :

 8 Amount of IP and OP species in soil ...................................................................................... 47

Table 9 :

 9 Possible root traits and microbial activity involved in OP mobilization (solubilization and

mineralization)....................................................................................................................................... 55 Table 10: Case studies used to promote and improve OP-use efficiency in the soil-plant system ...... 61 Table 11:. Isotherm parameters of the Langmuir and Freundlich models for P adsorption ................ 116 Table 12: Organic P desorption isotherm parameters of the Elovich model ....................................... 119 Table 13 : P adsorption capacity of the produced minerals-P adsorption complexes. ........................ 140 Table 14: Effect of different P-mineral complexes on the root, shoot, and whole plant biomass (root + shoot biomass). .................................................................................................................................... 144 Table 15: The GLM model results testing the impact of factors (P compounds, soil minerals, and their combined effect) on total P uptake ...................................................................................................... 145 Table 16 : Effect of different P-mineral complexes on the percentage of P recovered by ryegrass from adsorbed OP compounds. .................................................................................................................... 145 Table 17: One-way ANOVA results testing the effects of OP compounds by soil minerals on total P uptake, P availability, and dry weight. ................................................................................................ 147 Table 18: P adsorption capacity of the produced minerals-P adsorption complexes ......................... 165

Table 21 :

 21 Spearman product-moment correlation (r-values) between total P uptake, foliar N and P and

rhizosphere properties. ........................................................................................................................ 175 Table 22: Maximum P adsorption capacity of the produced minerals-P adsorption complexes. ........ 188 Table 23:List of abbreviations and associated units ............................................................................ 193

Table 24 :

 24 The generalized linear models (GLM) results testing the impact of factors (species, P compounds, soil minerals, and their combined effect) on P-acquisition traits, total P uptake, and biomass production. ........................................................................................................................................... 195

Table 25 :

 25 Mean values ± standard error and P-acquisition strategies by species among different P forms on goethite. .......................................................................................................................................... 197

Table 26 :

 26 Mean values ± standard error and P-acquisition strategies by species among different P forms on kaolinite. ......................................................................................................................................... 198

Table 27 :

 27 Selected models fitted to phosphorus uptake sorted from best fit to worst by strategies ... 201

Table 28 :

 28 Biogeochemical and crop model characteristics and roadmap for improving coupled biogeochemical and ecosystem C-N-P cycle models based on this study........................................... 226

INTRODUCTION 1 INTRODUCTION 1.1 Organic phosphorus sorption in soils: processes, models and implications for sustainable phosphorus management

.4 Organic P desorption and availability from mineral-OP bridging complexes Compared

	1.1
	minerals	IP	IHP	GLY	G6P	G1P	AMP	ATP	DNA
	Goethite	+ + + + +	+ + + + +	+ +	+ + + +	+ + + + +	+	+ + +
	Gibbsite	0	+ + + + +	0	0	0	0	0	0
	Ferrihydrite	+ + + + +	+ + + + +	0	+ + + +	0	+	+ + +
	Hematite	+ + + + +	+ + +	0	+ + + +	0	+ + + +	+ +	0
	Akaganeite	+ + + + +	0	0	0	0	0	0	0
	Amorphous Al (OH)3	+ + +	+ + + + +	+ +	+	0	0	+	0
	Maghemite	+ + + +	+ + +	0	0	0	0	0	0
	Magnetite	+ + + +	+ + +	0	0	0
	GoethiteHumic acid	+ + + +	0	0	0	0	0	0	0
	Ferrihydrite Humic acid	+ ++	0	0	0	0	0	0	0
	Boehmite	+ + + +	+	+ + + + +	+ + +	0	0	+ +	0
	Dolomite	+ ++	0	0	0	0	0	0	0
	Kaolinite	+ ++	+	0	0	0	0	0	+ + + + +
	Montmorillonite	0	0	0	0	0	0	0	.+ + +
	Illite	0	+ + +	0	0	0	0	0	+ + + +
	Humic acid	+ + +	+ + + + +

to adsorption, desorption of OP from soil minerals has received less attention. Factors such as P saturation

Table 3 : Desorption of P from Boehmite with KCl and Citrate and from different mineral surface saturations of 50% and

 3

	Desorbtion of P from boehmite			Effect of surface saturation on desorption
	(Yan et al., 2014)			(He et al. 1994)
	Complex	KCl	Citrate	Complex	Resin extraction
	Boehmite-IP	-	-	Montmorillonite-P50	45.5%
	Boehmite-IHP	0.93%	4,33%	Montmorillonite-P100	41.4%
	Boehmite-GLY	8%	39,50%	Kaolinite-P50	3.6%
	Boehmite-G6P	13%	59,68%	Kaolinite-P100	5.4%
	Boehmite-ATP	5%	21,33%	Goethite-P50	0%

100%.

Phosphorus compounds (IHP: myo-inositol hexakisphosphate, GLY: glycerophosphate, G6P: glucose-6-phosphate and IP: KH2PO4); The dashes (-) identify the mineral-phosphorus complexes produced by the adsorption of P forms onto soil minerals.

Example Go-IHP refers to goethite and myo-inositol hexakisphosphate complexes.

Table 4 : Binding patterns of P-forms and their interaction energies per number of bonds (Eint/bond) on goethite and two diaspore surface planes.

 4

  ).

	P forms	Binding motif	Binding energy: Eint/bond (kcal/mol)
			Goethite	010 diaspore surfaces	100 diaspore surfaces
	IP	Monodentate	-36	..	..
		Bidentate	-41	..	..
	GLY	Monodentate	-48	-63	-23
		Bidentate	-38	-148	-15
	IHP	Monodentate	-85	..	-33
		2-monodentate	-69	-170, -115	-18
		3-monodentate	-72	-145	-109

Table 5 : Total IP and OP forms in organic inputs.

 5

		Values in parentheses are percentage of total extractable P.
	N°	Organic input	Extractant	Analysis	Total IP	Total OP	References
	1	Feces (dairy)	NaOH-EDTA	31 PNMR	4961 mg.kg -1 (64)	2650 mg.kg -1 (36)	(Toor et al., 2006)
	2	Manure (dairy)	NaOH-EDTA	31 PNMR	4231 mg.kg -1 (75)	1396 mg.kg -1 (26)	(Toor et al., 2006, 2005)
	3	Dairy manure -dry	NaOH-EDTA	31 PNMR	4736 mg.kg -1 (67)	2342 mg.kg -1 (30)	(He et al., 2007)
	4	Dairy manure -wet	NaOH-EDTA	Enzymatic hydrolysis	3840 mg.kg -1 (57)	2957 mg.kg -1 (49)	(He et al., 2009)
	5	Dung	NaOH-EDTA	31 PNMR	58 mg.kg -1 (22)	399 mg.kg -1 (40)	(Bol et al., 2006)
	6	Solid manure (dairy)	NaOH-EDTA	31 PNMR	5731 mg.kg -1 (67)	2848 mg.kg -1 (33)	(Hansen et al., 2004)
	7	Lagoon manure (dairy)	NaOH-EDTA	31 PNMR	19 mg.kg -1 (66)	10 mg.kg -1 (34)	(Hansen et al., 2004)
	8	Cattle manure	NaOH-EDTA	31 PNMR	3120 mg.kg -1 (74)	1080 mg.kg -1 (25)	(Turner, 2004)
	9	Dairy manure	Water	31 PNMR	1870 mg.kg -1 (85)	221 mg.kg -1 (15)	(He et al., 2009)
	10	Dairy manure	NaAcNa2S2O4	31 PNMR	3680 mg.kg -1 (79)	944 mg.kg -1 (21)	(He et al., 2009)
	11	Dairy manure	NaOH-EDTA	31 PNMR	3637 mg.kg -1 (77)	964 mg.kg -1 (23)	(He et al., 2009)
	12	Animal species (beef and dairy cattle, swine, chicken, turkey, dairy goat, horse, and sheep)	H2O, NaHCO3, NaOH	-	-	500-8800 mg.kg -1	(Pagliari and Laboski, 2012)
	13	Broiler litter	NaHCO3	31 PNMR	1300 mg.kg -1 (12)	2800 mg.kg -1 (25)	(Li et al., 2014)
	14	Dairy manure	NaHCO3	31 PNMR	2400 mg.kg -1 (35)	890 mg.kg -1 (13)	(Li et al., 2014)
	15	Swine manure	NaHCO3	31 PNMR	6500 mg.kg -1 (21)	1600 mg.kg -1 (5)	(Li et al., 2014)

Table 6 : Total IP and OP forms in different soil properties (in mg.kg-1).

 6

		Values in parentheses are percentage of total extractable P.
	N°	Land use	Extractant	Analysis	Total IP	Total OP	Refference
	1	Semi-arid irrigated arable soils (U.S.)	EDTA	31 PNMR	141 mg.kg -1 (72)	57 mg.kg -1 (27)	(Turner et al., 2003)
	2	Semi-arid irrigated arable soils (U.S.)	Bicarbonate	31 PNMR	31 mg.kg -1 (76)	7 mg.kg -1 (26)	(Turner et al., 2003)
	3	Grassland (Australia)	Deionised water	Enzymatic hydrolysis	1.3 mg.kg -1 (36)	1.5 mg.kg -1 (48)	(Turner et al., 2002a)
	4	Grassland (New Zealand)	NaOH-EDTA	Enzymatic hydrolysis	454 mg.kg -1 (56)	23 mg.kg -1 (4)	(McDowell et al., 2008)
	5	Clover and arable plots (Australia)	NaOH-EDTA	31 PNMR	345 mg.kg -1 (76)	6 mg.kg -1 (2.5)	(Bünemann et al., 2006)
	6	Grassland (U.S.)	NaOH-EDTA	31 PNMR	221 mg.kg -1 (82)	54 mg.kg -1 (19)	(Hansen et al., 2004)
	7	Grassland (Netherlands)	NaOH-EDTA	31 PNMR	406 mg.kg -1 (56)	207 mg.kg -1 (44)	(Koopmans et al., 2007)
	8	Grassland (Ireland)	NaOH-EDTA	31 PNMR	358 mg.kg -1 (47)	373 mg.kg -1 (54)	(Murphy et al., 2009)
	9	Grassland (New Zealand)	NaOH-EDTA	31 PNMR	(32)	(68)	(Newman and Tate, 1980)
		Grassland (England and Wales)	NaOH-EDTA	31 PNMR	275 mg.kg -1 (40)	480 mg.kg -1 (70)	(Turner et al., 2003)
		Grassland (England and Wales)	NaHCO3	31 PNMR	18 mg.kg -1 (25)	70 mg.kg -1 (80)	(Turner, 2005)
		Grassland (New Zealand)	NaOH-EDTA	31 PNMR	500 mg.kg -1 (50)	20 mg.kg -1 (3)	(McDowell et al., 2005)
		Forest, grassland and arable (Germany)	NaOH	31 PNMR	52 mg.kg -1 (30)	149 mg.kg -1 (56)	(Guggenberger et al., 1996)
		Grassland (England)	NaOH	31 PNMR	224 mg.kg -1 (50)	140 mg.kg -1 (40)	(Hawkes et al., 1984)
		Semi-arid grassland and arable (Canada)	H2O and NaOH	31 PNMR	175 mg.kg -1 (58)	117 mg.kg -1 (42)	(Condron et al., 2005)
		Grassland (U.S.)	NaOH-EDTA	31 PNMR	23 mg.kg -1 (20)	66 mg.kg -1 (67)	(Cheesman et al., 2014)
		Arable (Canada)	NaOH-EDTA	31 PNMR	504 mg.kg -1 (73)	370 mg.kg -1 (48)	(Cade-Menun, 2017)
		Grassland (New Zealand)	NaOH-EDTA	31 PNMR	620 mg.kg -1 (54)	465 mg.kg -1 (45)	(McDowell et al., 2005)

Table 7 : Amount of IP and OP species in organic input IP forms OP forms Phosphomonoesters Phosphodiesters

 7

	N°	Organic input	Orthophosphate Pyrophosphate Polyphosphate	IHP	Labile	Phospholipi ds	DNA/ polynaucleotide	Other	Phospha nate	Unidenti fied
	1	Feces (dairy)	4961mg.kg -1	1325 mg.kg -1	624 mg.kg -1	423 mg.kg -1	154 mg.kg -1	113 mg.kg -1	73 mg.kg -1	-
	2	Manure (dairy)	4231mg.kg -1	496 mg.kg -1	503 mg.kg -1	210 mg.kg -1	108 mg.kg -1	83 mg.kg -1	55 mg. kg -1	-
	3	Dairy manure dry	4736 mg. kg -1	268 mg.kg -1	204 mg.kg -1	-	24 mg.kg -1	-	-	1842 mg. kg -1

Table 8 : Amount of IP and OP species in soil IP forms OP forms Phosphomonoesters Phosphodiesters Other P forms Soil types

 8

			Orthophosphate Pyrophosphate Polyphosphate	IHP	Labile	Phospholipids	DNA/ polynaucleotide	Phosphanate	Unidenti fied
	1	Semi-arid
		irrigated arable soils	150 mg.kg -1	45 mg. kg -1	10 mg.kg -1	1 mg.kg -1	0.3 mg.kg -1	1.3 mg.kg -1	-
		(U.S.)
	2	Semi-arid
		irrigated arable soils	31 mg.kg -1	1.6 mg. kg -1	1.4 mg. kg -1	0.1 mg.kg -1	0.9 mg.kg -1	1 mg. kg -1	2.2 mg. kg -1
		(U.S.)
	3	Grassland (Australia)	1.3 mg.kg -1	0.28 mg. kg -1	0.04 mg.kg -1	0.2 mg.kg -1	0.03 mg.kg -1	0.23 mg.kg -1	0.8 mg. kg -1

Table 9 : Possible root traits and microbial activity involved in OP mobilization (solubilization and mineralization). Organic phosphorus forms Mode of action that root traits and microbes act to mobilize the OP. Associated microorganisms Reference

 9

	Glycerophosphate and phytate	Alkaline phosphatase and acid phosphatase; phytase	Bacillus coagulans	(Yadav et al., 2012)
	Ca-phytate	pH reduced; phytase	Bacillus altitudinis WR10	(Yue et al., 2019)
	OP pools	Alkaline phosphatase	Aphanothece halophytica	(Kageyama et al., 2011)
	Na-phytate	pH reduced; phytase	Tetrathiobacter sp. PB-03 and Bacillus sp. PB-13	(Kumar et al., 2013)
	Phytic acid	Phytase	Bacillus amyloliquefaciens US573 Acromobacter sp. PB-01	(Boukhris et al., 2015)
	Total OP pools	Alkaline phosphatase and acid phosphatase	Bacillus pumilus strain JPVS11	(Kumar et al., 2021)
	beta-Glycerophosphate	pH reduced; acid phosphatase	Agrobacterium sp. and Bacillus sp.	(Barua et al., 2012)
	5-bromo-4-chloro-3-indolyl phosphate (BCIP)	pH reduced; phosphatase	Pantoea agglomerans strain P5 Microbacterium laevaniformans strain P7 and Pseudomonas putida strain P13	(Malboobi et al., 2009)
	p-nitrophenyl phosphate
	(pNPP) and guanosine 5-triphosphate	Alkaline phosphatase/phosphodiesterase activity	Cobetia amphilecti	(Noskova et al., 2019)
	(GTP)

Table 10 : Case studies used to promote and improve OP-use efficiency in the soil-plant system

 10

	Case studies	Observation/concept	OP forms	Test plant	Reference
		Sludge is as effective as TSP to
	Sewage sludge application in an agroecosystem (long-term (> 20 years) cropland field in northern France	improve soil P availability. activities (phosphatases) for OP Sludge promotes soil enzymatic	OP forms, Apatite-P, Nonapatite-P	Oilseed rape-winter wheat -rotation winter barley	(Houben et al., 2019)
		hydrolysis

Table 11 : Isotherm parameters of the Langmuir and Freundlich models for P adsorption

 11

				Langmuir equation		Freundlich equation
	Soil components	P Forms	Qm (µg g -1 )	KL (L mg -1 )	R 2	MBC (L Kg -1 )	KF	n	R 2
		IP	2810	0.16	0.97	450		3.77	0.99
		myo-IHP	3742	0.4	0.97	1497	1584	4.88	0.98
	Goethite
		GLY	1398	3.31	0.99	4626	1228	9.7	0.99
		G6P	4337	0.05	0.98	217		2.35	0.99
		IP	20949	0.99	0.91	20740	7158	3.31	0.96
		myo-IHP	56698	0.08	0.99	4536	5703	1.62	0.99
	Gibbsite
		GLY	6237	0.14	0.97	873	1584	3.26	0.98
		G6P	5588	0.4	0.98	2235	2254	4.58	0.96
		IP	1736	0.04	0.99	69		2.08	0.98
		myo-IHP	6082	0.02	0.99	122		1.53	0.98
	Kaolinite
		GLY	1222	0.02	0.96	24	57	1.68	0.96
		G6P	2295	0.04	0.98	92		2.01	0.92
		IP	3709	0.05	0.99	185		2.34	0.97
		myo-IHP	4857	0.32	0.97	1554	1966	4.82	0.87
	Montmorillonite
		GLY	1045	0.28	0.98	293		5.71	0.96
		G6P	2338	0.1	0.96	234		3.1	0.92

Qm: maximum adsorption capacity, KL: binding-energy related constant, R 2 : model fitting degree, MBC: maximum buffer capacity (ability of soil minerals to resist a change in solution P concentration ).

Table 12 : Organic P desorption isotherm parameters of the Elovich model

 12

				Elovich equation
	Soil components	P Forms
			Dm (%P g -1 )	A (%P day -1 )	B (%P g -1 )	R 2
		IP	33	8	25	0.99
	Goethite	myo-IHP	14	6	9	0.97
		GLY	13	2	11	0.97
		G6P	56	23	33	0.90
		IP	12	5	7	0.91
	Gibbsite	myo-IHP	3	2	2	0.97
		GLY	15	2	13	0.98
		G6P	15	2	13	0.94
		IP	59	21	38	0.94
	Kaolinite	myo-IHP	39	12	27	0.95
		GLY	6	0.01	6	0.98
		G6P	23	0.01	23	0.98
		IP	49	16	33	0.99
	Montmorillonite	myo-IHP	36	10	26	0.96
		GLY	24	0	23	0.92
		G6P	45	12	33	0.97

Table 13 : P adsorption capacity of the produced minerals-P adsorption complexes.

 13

Table 14 : Effect of different P-mineral complexes on the root, shoot, and whole plant biomass

 14

		Root Biomass (g)	Shoot Biomass (g)	Total Biomass (g)
	Go-IP	0.27 ± 0.01 a	0.55 ± 0.10 a	0.82 ± 0.11 a
	Go-IHP	0.27 ± 0.03 a	0.85 ± 0.11 b	1.12 ± 0.13 b
	Go-GLY	0.33 ± 0.03 a	0.64 ± 0.09 ab	0.96 ± 0.12 ab
	Go-G6P	0.27 ± 0.09 a	0.54 ± 0.09 a	0.81 ± 0.19 ab
	Gib-IP	0.26 ± 0.03 a	0.60 ± 0.12 a	0.86 ± 0.16 a
	Gib-IHP	0.17 ± 0.09 a	0.42 ± 0.16 a	0.60 ± 0.25 a
	Gib-GLY	0.19 ± 0.03 a	0.43 ± 0.08 a	0.62 ± 0.12 a
	Gib-G6P	0.21 ± 0.01 a	0.45 ± 0.06 a	0.66 ± 0.07 a
	K-IP	0.22 ± 0.03 ab	0.83 ± 0.15 a	1.05 ± 0.15 a

(root + shoot biomass).

Results are mean ± standard error. Means with a different letter were significantly different according to Tukey's HSD test at P < 0.05. Comparisons of means were made for each mineral category. Soil minerals (Go: goethite, Gib: gibbsite, K: kaolinite, and M: montmorillonite); Phosphorus compounds (IHP: Myo-inositol hexakisphosphate, GLY: glycerophosphate, G6P: glucose-6-phosphate, and IP: KH2PO4); Dashes (-) identify mineral-phosphorus complexes produced by adsorption of forms of P onto soil minerals. The example Go-IHP refers to goethite and Myo-inositol hexakisphosphate complexes.

Table 15 : The GLM model results testing the impact of factors (P compounds, soil minerals, and their combined effect) on total P uptake

 15

	Variables effects	P uptake
		p-value	AIC
	P forms	<0.001	268-329
	Minerals: P forms	<0.001	156-199
	Soil minerals	<0.001	314-388
	R²	0.92

Table 16 : Effect of different P-mineral complexes on the percentage of P recovered by ryegrass from adsorbed OP compounds.

 16

	Results are mean ± standard error. Means with a different letter were significantly different according to Tukey's HSD test at
	P < 0.05. Comparisons of means were made for each mineral category. Soil minerals (Go: goethite, Gib: gibbsite, K: kaolinite,
	and M: montmorillonite); Phosphorus compounds (IHP: myo-inositol hexakisphosphate, GLY: glycerophosphate, G6P:

Table 17 : One-way ANOVA results testing the effects of OP compounds by soil minerals on total P uptake, P availability, and dry weight.

 17

	Soils minerals (Go: goethite, Gib: gibbsite, K: kaolinite, and M: montmorillonite); OP: Organic Phosphorus.
	Variables effects	P uptake	P availability	Dry weight
		p-value	p-value	p-value
	Go-OP	< 0.001	< 0.001	0.07
	Gib-OP	< 0.001	< 0.001	0.92
	K-OP	0.05	< 0.05	0.08
	M-OP	<0.001	< 0.01	0.72
	(a)

Table 19 : GLM model results testing the impact of factors: N form (NO3-N or NH4-N), minerals (goethite and kaolinite), and P forms (IP, IHP, and GLY) on N: P ratio, total P uptake, and total biomass.

 19

	Explanatory factor		N : P ratio			P uptake			Total biomass
		LR Chisq	Df	Pr	F	Pr	AICc	F	Pr	AICc
	N forms	4.1	2	0.12	65.03	< 0.001	84	34.5	< 0.001	-149
	Minerals	5.3	1	< 0.05	18.08	< 0.001	98	2.1	0.1	-121
	N forms x Minerals	5.3	2	< 0.05	3.24	< 0.05	87	3.1	< 0.05	-146
	P forms	11.5	2	< 0.01	131.38	< 0.001	62	10.5	< 0.001	-126
	N forms x P forms	19.5	4	< 0.001	11.09	< 0.001	31	4.7	< 0.01	-161
	Minerals x P forms	21.1	2	< 0.001	26.98	< 0.001	53	11.7	< 0.001	-129
	N forms x Minerals x P forms	20.9	4	< 0.001	13.3	< 0.001	-35	2.5	< 0.05	-172

Table 21 : Spearman product-moment correlation (r-values) between total P uptake, foliar N and P and rhizosphere properties.

 21

	*p < 0.05; **p < 0.01; ***p < 0.001
		N:P	Total P uptake	Foliar N	Foliar P
	Rhizosphere pH	-0.036	0.159	0.063	0.182
	Available P	-0.209 *	0.537***	0.037	0.404***
	Phosphatase activity	0.381***	0.463***	0.363***	0.282
	Foliar N	0.640***	0.359***	-	0.362**

Table 22 : Maximum P adsorption capacity of the produced minerals-P adsorption complexes.

 22

Go: goethite; K: kaolinite; IP: inorganic P; IHP: Myo-inositol hexakisphosphate and GLY: glycerophosphate

Table 23 :List of abbreviations and associated units

 23

	Variable

1 Highlighting phosphorus acquisition strategies among P forms in crop species

  The first "physiological/ exudation" group C1 included Vicia faba, Pisum sativum, and Lupinus albus. It had positive values on PC1 and showed the greatest exudation of carboxylic acids, an important activity of PME in the rhizosheath, as well as the lowest fine root percentage and SRL. The second "intermediate/morphological" group C2 encompassed Hordeum vulgare. This group were spread on negative values on PC1 and 2. It presented the lowest carboxylate release while presenting the highest leaf [P] concentration and RLD and an important fine root percentage compared with other groups. The third "intermediate" group C3 encompassed Lens culinaris. It presented intermediate values of all measured morphological/architectural and physiological traits, and important leaf [P] content. Finally, the fourth "morphological" group C4, encompassing Lolium perenne, Trifolium alexandrinum, and Phacelia tanacetifolia, presented low to the intermediate expression of P mining traits, a high fine root percentage and the highest SRL observed in all groups. It had negative values on PC1.

	Figure 29 shows the results of the principal components analysis (PCA) performed on P-acquisition
	strategies and leaf [P] concentration in IP and OP forms. The two principal components extracted by
	PCA accounted for 54.9% and 56,2% of the variance in IP and OP respectively. In both P forms, the
	PC1 was negatively associated with fine root percentage and SRL, and positively related to root length
	density, root surface area and total carboxylate release rate (Figure 29). The PC2 was negatively
	correlated by leaf [P] concentration and root length density, and positively related to rhizosheath pH
	change. Overall, on both forms of P, species clustered into four groups of P acquisition strategies (Figure
	29).

Table 24 : The generalized linear models (GLM) results testing the impact of factors (species, P compounds, soil minerals, and their combined effect) on P-acquisition traits, total P uptake, and biomass production.

 24

	Abbreviations: ΔpH: change in rhizosheath pH; FR: percentage roots with diameters less than 0.5 mm; Leaf_P: foliar
	phosphorus concentration; PME: acid phosphomonoesterase activity; RLD: root length density; RSA: root surface area; SRL:
	specific root area; TCE: total carboxylate release rate; AICc second order Aikake's information. p < 0.05, **p < 0.01, ***p <
	0.001.
			Minerals	P forms	Species	Minerals x P	Species x	Species x P	Species x
									forms		Minerals	forms		Minerals x P
															forms
			P	AIcc P	AIcc P	AIcc	P	AIcc	P	AIcc	P	AIcc	P	AIcc
	Morphological/	RSA	**	2201 Ns	2203 *** 1687	Ns	2209	*	1686	Ns	1711	Ns	1739
	architectural traits	RLD	*** 752	Ns	755	*** 342	Ns	759	**	335	*	357	Ns	378
		SRL	*	2409 Ns	2411 *** 2155	Ns	2416	***	2150	*** 2131	Ns	2150
		FR	Ns	-8.3	Ns	-6.5	*** -393	*	-1.4	Ns	-379	*** -418	***	-420
	Physiological	ΔpH	*** -210 *** -271 *** -332	***	-281	***	-499	*** -361	***	-686
	traits	PME	**	74.7 Ns	80.2 *** 30	Ns	80.8	***	5.17	*** 31	Ns	23
		TCE	Ns	2682 **	2681 *** 2403	Ns	2687	Ns	2418	*** 2392	***	2424
		Leaf [P]	Ns	-853 **	-855 *** -1012	***	-856	***	-1017 *	-1007	***	-1026
	P acquisition	P uptake	Ns	-515 Ns	-513 *** -7716	***	-515	**	-714	*** -729	**	-736
		Available	*** -123 *** -130 *** -173	**	-139	*	-175	*** -212	***	-228
		_P
		Biomass	Ns	-187 Ns	-185 *** -782	Ns	-179	***	-790	*** -795	***	-807

Table 25 : Mean values ± standard error and P-acquisition strategies by species among different P forms on goethite.

 25 FR Fine root percentage (<0.5 mm diameter), Leaf [P] Leaf phosphorus concentration (mg P g -1 ), PME Phosphomonoesterase activity (μg nitrophenol g -1 hour -1 ), RLD Root length density (cm cm -3 ), SRL Specific root length (m g -1 ), TCE Total carboxylate release rate (μmol g root -1 hour -1 ), ΔpH Change in rhizosheath pH, P uptake (mgPpot -1 ), P available (mgPpot-1 )

	and biomass (g).
	Species/Clusters	P forms	RSA	RLD	SRL	FR	ΔpH	PME	TCE	Leaf [P] Available P	P uptake	Biomass
	C1: Physiological/exudation
	Lupinus albus	IP	67,52±	2,62±	26,62±7	0,41±	-0,42±	18,82±	445,5±	0,05±	0,29±	0,20±	0,65±
			18,32	0,61	33	0,09	0,066	0,137	155,9	0,04	0,15	0,06	0,04
		IHP	74,37±	2,86±	23,96±	0,36±	-0,15±	18,83±	269,5±	0,13±	0,06±	0,14±	0,65±
			9,159	0,15	4,877	0,05	0,040	0,142	89,24	0	0,06	0,00	0,02
		GLY	67,64±	2,69±	35,97±	0,39±	-0,06±	19,01±	551,2±	0,02±	0,03±	0,10±	0,54±
			17,69	0,73	10,26	0,03	0,020	0,053	160,0	0,00	0,00	0,08	0,11
		p-value	Ns	Ns	Ns	Ns	0.001	0.04	0.02	0.0001	0.01	Ns	Ns
	Pisum sativum	IP	112,1± 6,805	5,22± 0,98	63,99± 44,43	0,61± 0,05	-0,23± 0,013	18,82± 0,047	144,4± 22,74	0,04± 0,01	0,17± 0,09	0,23± 0,03	0,40± 0,10
		IHP	132,1± 57,29

Table 26 : Mean values ± standard error and P-acquisition strategies by species among different P forms on kaolinite.

 26

	0,01

Table 28 : Biogeochemical and crop model characteristics and roadmap for improving coupled biogeochemical and ecosystem C-N-P cycle models based on this study

 28

	Models	Main gaps	Priority	Modelers' roadmap	Empiricists' roadmap

Introduction Enjeux agroécologiques de la mobilisation du phosphore organique pour une fertilisation phosphorée durable

  Le phosphore (P) est un nutriment limitant pour la productivité des agroécosystèmes. Ceci est dû à sa faible disponibilité dans le sol qui résulte de sa faible solubilité et de sa forte affinité pour les surfaces minérales. La fertilisation phosphorée est donc nécessaire pour obtenir des rendements élevés. La plupart du P actuellement utilisé dans les engrais chimiques provient des roches phosphatées. Ces ressources sont inégalement réparties à la surface de la Terre et, dans l'Union européenne (UE), la production alimentaire dépend des importations de P primaire. Étant donné que les réserves ne se trouvent qu'à quelques endroits sur la Terre, et qu'elles sont donc contrôlées par quelques pays, l'approvisionnement en P de l'UE est vulnérable aux questions géopolitiques, avec des problèmes possibles d'accessibilité et de prix des engrais P à moyen terme. De plus, le phosphate naturel est une ressource stratégique dont l'exploitation peut entraîner des occupations et des conflits armés. Dans

			C6 C1	1393.07 298.92	±13.39 ±46.53
		G6P	C0 C2	0 570.49	±0.62 ±97.98
			C1 C3	477.7 1127.46	±21.34 ±17.12
			C2 C4	1063.39 2152.24	±26.06 ±54.83
			C3 C5	1826.11 3148.88	±143.4 ±195.33
			C4 C6	2695.29 3566.47	±12.22 ±693.4
		GLY	C5 C0	3400.51 0	±348.3 ±0
			C6 C1	3549.65 98.64	±905.97 ±2.45
	Gibbsite	IP	C0 C2	0 174.59	±0 ±2.83
			C1 C3	3786.76 302.89	±1.32 ±30
			C2 C4	4176.71 560.54	±1.84 ±49.47
			C3 C5	4044.4 750.07	±2.86 ±108.59
			C4 C6	19087.85 821.24	±181.93 ±243.52
		G6P	C5 C0	20353.51 0	±401.35 ±2.94
			C6 C1	20553.76 286.46	±425.39 ±40.72
		IHP	C0 C2	0 502.73	±0 ±171.83
			C1 C3	1191.95 850.57	±4.55 ±28.5
			C2 C4	2334.82 1306.37	±9.1 ±366.46
			C3 C5	8312.38 1672.42	±36.39 ±213.77
			C4 C6	15660.78 1765.95	±53.51 ±387
	Montmorillonite	IP	C5 C0	30263.72 0	±160.54 ±0
			C6 C1	36017.74 444.46	±170.16 ±12.57
		GLY	C0 C2	0 916.56	±0 ±171.05
			C1 C3	920.96 1484.75	±5.17 ±74.51
			C2 C4	1976.18 2412.39	±28.16 ±130.14
			C3 C5	3655.18 2890.91	±232.31 ±149.94
			C4 C6	5049.36 3078.23	±38.48 ±137.43
		IHP	C5 C0	5613.24 0	±290.24 ±0
			C6 C1	5757.88 1401.83	±109.6 ±35.95	The
		G6P	C0 C2	0 2477.21	±0 ±68.48
			C1 C3	1569 3491.83	±27.33 ±224.4
			C2 C4	2608.53 4399.07	±125.59 ±256.06
			C3 C5	4433.58 4633.78	±2.04 ±226.87
			C4 C6	5118.91 4689.44	±829.85 ±150.78
		GLY	C5 C0	5373.9 0	±465.71 ±0
			C6 C1	5422.82 489.81	±371.52 ±12.35
	Kaolinite	IP	C0 C2	0 686.71	±0 ±60.02
			C1 C3	189.38 835.58	±69.48 ±17.56
			C2 C4	366.07 956.52	±160.83 ±257.07
			C3 C5	608.51 996.78	±126.23 ±10.31
			C4 C6	1018.9 1007.43	±79.97 ±48.28
		G6P	C5 C0	1259.62 0	±68.06 ±1.36
			C6 C1	1357.61 512.69	±90.75 ±198.69
		IHP	C0 C2	0 940.61	±0 ±128.54

DISCUSSION

Mots clés : agroécologie ; biogéochimie ; apports organiques ; phosphore organique ; traits végétaux ; adsorption ; désorption ; phosphore organique ; disponibilité du phosphore ; fertilité des sols ; (co)-limitation de l'azote et du phosphore ; stratégies d'acquisition du phosphore ; fourrage du phosphore ; extraction du phosphore ; niches écologiques.

ACKNOWLEDGMENTS Acknowledgements

Acknowledgments: The authors thank the Institut Polytechnique UniLaSalle Beauvais and Pro-gramme Opérationnel FEDER/FSE Picardie 2014-2020 for their support for the start of the global research project in agriculture focusing on sustainable management of soil fertility and ecoeffi-ciency of phosphorus management in farming systems. We also thank Adaline Adam, Céline Roisin, Aurore Coutelier, Nicolas HONVAULT, Philippe Jacolot, Hamza MOHIEDDINNE for their technical assistance.

Acknowledgements: This research was partly funded by Bpifrance and the Région Hauts-de-France (FUI Biochar 2021). The authors thank the Campus UniLaSalle Beauvais and Pro-gramme Opérationnel FEDER/FSE Picardie 2014-2020 for their support for the start of the global research project in agriculture focusing on sustainable management of soil fertility and ecoefficiency of phosphorus management in farming systems. We thank Adeline Adam, Céline Roisin, Aurore Coutelier, Nicolas Honvault and Philippe Jacolot for their technical assistance. We also thank Frederic Gerard, Alain Mollier, Gilles Colinet and Olivier Pourret for all their suggestions and contributions. extraite, une ressource limitée et en constante diminution. Dans l'optique d'une gestion plus durable de la nutrition en P dans les agroécosystèmes, le phosphore organique (OP) provenant d'intrants organiques et du sol est de plus en plus considéré comme un complément aux engrais minéraux P. Cependant, la dynamique de l'apport de P par le biais de l'engrais organique n'est pas toujours bien comprise. Nous avons montré que les facteurs liés aux propriétés minérales du sol et aux caractéristiques moléculaires des OP affectaient directement les réactions des OP et leur libération dans le sol. De même, ces facteurs ont affecté la disponibilité des OP dans la rhizosphère et leur absorption par la plante. En caractérisant les interactions N-OP-minéraux nous avions fourni des informations importantes sur le cycle du P dans les écosystèmes en cas d'ajout de N et sur les propriétés biogéochimiques impliquées, ce qui permettra aux modèles d'écosystèmes de prédire avec précision la limitation N-P des plantes et ses impacts, et aidera également à construire des modèles d'écosystèmes robustes avec des interactions N-P ou C-N-P entièrement couplées. La réponse positive des stratégies d'acquisition de P aux sources d'OP a entraîné une plus grande disponibilité et acquisition de P à partir des OP. Enfin, l'identification par modélisation des traits majeurs impliqués dans les stratégies d'acquisition du P et leur capacité à mieux prédire l'acquisition du P, offre des opportunités pour concevoir des compositions d'espèces cultivées et plus spécifiquement la structure fonctionnelle des communautés végétales cultivées. Ces systèmes permettraient à leur tour d'évaluer les effets globaux des interactions entre les intrants organiques, le sol et les plantes sur la disponibilité du P et de soutenir les décisions de gestion des agriculteurs, telles qu'une fertilisation P adaptée.

Data Availability Statement:

The study did not report any data.

OBJECTIVES

 [START_REF] Turner | Genetic variability for root hair traits as related to phosphorus status in soybean[END_REF]Optimizing Phosphorus Characterization in Animal Manures by Solution Phosphorus-31 Nuclear Magnetic Resonance Spectroscopy. J Env. QUAL 33, 10. Turner, B.L., Blackwell, M.S.A., 2013. Isolating the influence of pH on the amounts and forms of soil organic phosphorus. Eur. J. Soil Sci. 64, 249-259. Turner, B.L., Cade-Menun, B.J., Westermann, D.T., 2003. Organic phosphorus composition and potential bioavailability in semi-arid arable soils of the western United States. Soil Sci. Soc. Am. J. 67, 1168-1179. Turner, B.L., Engelbrecht, B.M., 2011. Soil organic Philos. Trans. R. Soc. Lond. B. Biol. Sci. 357,. https://doi.org/10.1098/rstb.2001.0837 Urrutia, O., Erro, J., Guardado, I., San Francisco, S., Mandado, M., Baigorri, R., Claude Yvin, J., Ma Garcia-Mina, J., 2014. Physico-chemical characterization of humic-metal-phosphate complexes and their potential application to the manufacture of new types of phosphate-based fertilizers. J. Plant Nutr. Soil Sci. 177, 128-136.

Vance, C.P., Uhde-Stone, C., Allan, D.L., 2003. Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol. 157, 423-447. https://doi.org/10.1046/j. 1469-8137.2003.00695.x Vestergren, J., Vincent, A.G., Jansson, M., Persson, P., Ilstedt, U., Gröbner, G., Giesler, R., Schleucher, J., 2012. High-Resolution Characterization of Organic Phosphorus in Soil Extracts Using 2D 1 H-31 P NMR Correlation Spectroscopy. Environ. Sci. Technol. 46,[3950][3951][3952][3953][3954][3955][3956]. https://doi.org/10.1021/es204016h Vincent, A.G., Schleucher, J., Gröbner, G., Vestergren, J., Persson, P., Jansson, M., Giesler, R., 2012. Changes in organic phosphorus composition in boreal forest humus soils: the role of iron and aluminium.

Biogeochemistry 108, 485-499. Vincent, A.G., Vestergren, J., Grobner, G., Persson, P., Schleucher, J., Giesler, R., 2013. Soil

CHAPTER 1

only valid for the K-saturated montmorillonite used here. If Al-or Ca-saturated montmorillonite, which are the most common types of montmorillonite in soils, had been used, much higher P sorption and lower P desorption would be expected compared to K-saturated montmorillonite. Finally, despite their overall high adsorption, the higher desorption of G6P or GLY relative to IP from Fe and Al oxides indicated that G6P and GLY release would be less affected than IP by such soil compounds, which are especially abundant in highly weathered soils. However, since the P concentration used in our study may be higher than that of real soil systems, it would be interesting to investigate the effect of P concentration on adsorption processes by performing sorption experiments at different (and lower) P concentrations.

By simultaneously analyzing the interactions between various OP forms and various soil minerals, this study provides new insight into the OP adsorption and desorption dynamics on soil minerals which is important to optimize the use of organic input as fertilizer and to improve or develop prediction model of OP release in agroecosystems.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

CHAPTER 2 some amount of P can be available from the adsorbed OP compounds demonstrating, therefore that adsorbed OPs can act as a source of P for plants.

The availability of P from adsorbed OP differed between OP compounds. The P uptake from the adsorbed GLY compound was much higher than that of adsorbed G6P which was more available than adsorbed IHP. It appears that the difference in availability between adsorbed OP compounds was determined by the adsorption/desorption capacity more than their binding strength. The trend in availability (GLY >> G6P > IHP) would be mainly explained by the distinct desorption dynamics of the different minerals, leading to the lowest desorption for IHP-P, followed by G6P-P and then GLY-P (Amadou et al., 2022). This is also corroborated by the results of desorption dynamics (see supplementary data Appendix B Figure S1). Yan et al. (2014) similarly showed lower desorption of IHP from different structures of aluminum (oxyhydr)oxides compared to other OP compounds. In addition, the trend in availability (GLY >> G6P > IHP) could also be related to their different degrees of hydrolysis by enzymatic activity (Annaheim et al., 2010;[START_REF] Bünemann | Enzyme additions as a tool to assess the potential bioavailability of organically bound nutrients[END_REF] as phosphatase activity was the highest in the presence of GLY and the lowest in the presence of IHP (Figure. 19). Basically, we expected G6P to be more available than GLY due to its higher desorption and its likely instability on soil minerals due to its higher molecular weight than GLY (Annaheim et al., 2013;[START_REF] Park | Strategies of organic phosphorus recycling by soil bacteria: acquisition, metabolism, and regulation[END_REF]Yan et al., 2014). The opposite result we found may be the consequence of its more negatively charged surface compared to GLY (Giaveno et al., 2008;[START_REF] Peters | How longterm excessive manure application affects soil phosphorous species and risk of phosphorous loss in fluvoaquic soil[END_REF]Ruttenberg and Sulak, 2011). These reasons would also explain why the binding energy of G6P predicted from the Langmuir model is often higher than that of GLY or IP ( Bai et al., 2021;Goebel et al., 2017). Finally, adsorbed GLY was the higher source of P for plant uptake compared to other compounds, consistently with [START_REF] Adams | Availability of organic and inorganic forms of phosphorus to lupins (Lupinus spp.)[END_REF]. In conclusion, the availability of OPs for plant nutrition from organic inputs and soil would be determined by the stability of OP-mineral complexes or by their (de)sorption dynamics as well as their hydrolysis by enzymes.

Effect of mineral-OP interactions on P uptake by ryegrass

The potential availability of P adsorbed by different minerals was strongly affected by mineral-OP interaction properties. Except for the IHP, the P uptake from OP forms increased in the following order: kaolinite-OP << gibbsite-OP ≤ goethite OP << montmorillonite-OP (Tableau 4). Montmorillonite-OP complexes showed the highest P uptake, with a maximum of up to 18%. On the other hand, P uptake from kaolinite-OP was the lowest. Less than 4% of the initially adsorbed P was desorbed and mineralized for plant uptake. These results indicated that regardless of the type of mineral and its OP sorption strength and stability, plants are able to take up at least a small portion of it for their nutrition.

This agrees with laboratory and greenhouse studies indicating that specifically adsorbed P was potentially available to plants although it was very difficult to desorb (Bollyn et al., 2017;D'Amico et resistance of some of OP compounds to enzymatic hydrolysis because of their chemical properties.

Therefore, the availability of adsorbed OPs to plants does not depend on their binding strength to soil minerals but rather on their degree of hydrolysis by soil and root enzymes.

Finally, P uptake by ryegrass was positively correlated with ΔP resin (R = 0.73, p<0.01),

suggesting that the variation of available P in the rhizosphere determined the P uptake by plant (Figure 21). The ΔP resin values of the majority of the mineral-OP complexes were generally negative, showing that in addition to the spontaneously released P, there would have been a subsequent release of P from soil minerals that would occur in response to plant-induced depletion of available P in the rhizosphere.

This means that plant roots mobilized additional P from minerals. However, this finding did not apply to all OP-minerals complexes. For instance, GLY-mineral complexes (Figure 21) showed almost no variation in ΔP resin, i.e. no variation between P resin in the bulk soil and P resin in the rhizosphere, suggesting that plant absorbed only the spontaneously available P without any other mobilization. This confirms that GLY was sufficiently available from soil minerals. Thus, when the plant was in the presence of soil minerals associated with GLY, there was little or no additional P mobilization.

Phosphorus uptake from adsorbed OP relative to adsorbed

IP

Our third hypothesis was that P derived from adsorbed OP would be less available than P derived from adsorbed IP because it desorbs less and requires also enzymatic cleavage before being taken up by ryegrass. Our results support only partially this hypothesis as they showed that the different adsorbed OP compounds led to contrasted P uptake compared to the adsorbed IP compound. Phosphorus uptake from adsorbed IHP and G6P was significantly lower than that of adsorbed IP, whereas P uptake from adsorbed GLY, depending on the mineral, was slightly equal or higher than that of IP. Several studies have shown lower plant availability of adsorbed OP compounds compared to IP compounds (Andrino et al., 2019;D'Amico et al., 2020;[START_REF] Klotzbücher | Testing mechanisms underlying the Hedley sequential phosphorus extraction of soils[END_REF], probably due to the specific binding mechanisms of OP and its low desorption from soil (Bollyn et al., 2017;Ruyter-Hooley et al., 2015). However, in all of these studies, "organic P" refers only to IHP. In addition to IHP, GLY and G6P are also commonly found in soils, soils treated with organic inputs, sediments and wetlands [START_REF] Missong | Phosphorus forms in forest soil colloids as revealed by liquid-state 31 P-NMR[END_REF]Vincent et al., 2013) but these OP forms have not been considered potential sources of P for plants, except in a few studies [START_REF] Adams | Availability of organic and inorganic forms of phosphorus to lupins (Lupinus spp.)[END_REF]. Here, our results highlight the relative availability of these major OP forms compared to that of IP. In agreement with previous studies (Andrino et al., 2019;D'Amico et al., 2020;Ruttenberg and Sulak, 2011), IHP was less available than IP. Similar to IHP, we also found that adsorbed G6P was less available than IP. This would be due to the fact that, unlike IP, both IHP and G6P forms must be hydrolyzed after desorption to be available (D'Amico et al., 2020). In the present study, the phosphatase activity measured for IHP was very low

Abstract

Nitrogen and phosphorus cycles in ecosystems are composed of multiple biogeochemical forms and processes that jointly control P uptake and limitation by plants. To date, it remains unclear how the chemical forms of N, organic P (OP), and their interactions with soil minerals influence both P limitation and plant uptake in ecosystems. The paucity of research on the effect of these important biogeochemical processes (N-P-soil minerals) severely limits our ability to understand the ecological processes underlying the alteration of P cycling in ecosystems with N additions. The aims of this study were to evaluate the irrespective and interactive effects of N and P forms and their interaction with soil minerals on P uptake and limitation in plants. We characterized the N:P ratio, P uptake, and rhizosphere properties of ryegrass grown under several complexes of IP and OP (IHP, and GLY) adsorbed on Fe oxyhydroxides (goethite) and clay minerals (kaolinite) with and without the addition of N. We hypothesized that the addition of N in various specific forms would increase P limitation under conditions of low P availability, i.e., with OP forms and soil minerals, and that the shift of plants from N limitation to P limitation would be due to the beneficial effect of N addition. We found that interactions between N forms, P forms, and soil minerals strongly modified P dynamics, relative to individual effects. These interactions increased plant P limitation and P uptake via modification of rhizosphere chemistry. The degree of P limitation was strongly dependent on the degree of availability of P sources, so we found that the interaction between P forms and soil minerals was a major determinant of P limitation.

Therefore, we found that the interaction of N with IP forms led to greater P uptake and a marked reduction in P limitation compared to the interaction of N with OP forms. Thus, we inferred that in addition to the degree of P availability, the characteristics and biochemical nature of P sources determine the degree of P limitation in plants. Furthermore, we found that with the addition of N, more P was recycled from clay minerals and P limitation was delayed compared to iron oxides. This study therefore provides important information on ecosystem P cycling under N addition and the biogeochemical properties involved, which will allow ecosystem models to accurately predict plant N-P limitation and its impacts, and will also help build robust ecosystem models with fully coupled N-P or C-N-P interactions. Wang et al., 2012). Thus, it was concluded that in Luvisols P would be dissolved by acidification, whereas in Oxisols adsorbed P would be mobilized by ligand exchange. This suggests that the interaction between N forms and soil minerals is also crucial in the mobilization process of P forms. In brief, current major research has studied the effect of N on P uptake and P limitation by focusing mainly on inorganic P. However, in the soil, there are also pools of organic P that can contribute significantly to plant nutrition, but this depends in particular on the mineralogy of the soil (Amadou et al., 2022(Amadou et al., , 2021)).

Ecosystem N and P cycling consists of multiple pools and biogeochemical processes that are interrelated and interdependent, jointly controlling soil P availability, plant P uptake and its limitation (Vitousek et al., 2010). To date, it remains unclear how N forms, P chemical forms, and their interactions with soil minerals influence both P limitation and P uptake by plants within ecosystems. The paucity of research on the effect of these important biogeochemical processes (N-P-soil minerals), severely limits our ability to understand ecological processes underlying the alteration of ecosystem P cycling with N additions. More importantly, it limits our ability to incorporate the actual impact of P limitation into ecosystem models used to analyze the effects of potential future climate change on overall ecosystem productivity (Deng et al., 2017;Goll et al., 2012). A better understanding of ecosystem P cycling under N additions and the biogeochemical properties involved are needed not only to enable ecosystem models to accurately predict plant N-P limitation and its impacts, but also to develop robust ecosystem models with fully coupled N-P or C-N-P interactions.

The aims of this study were to assess the independent and interactive effects of N and P forms and their interaction with soil minerals on P limitation in plants, to unravel biogeochemical processes involved in P limitation by characterization of the role of N and P forms and their interaction with soil minerals in P availability and uptake by plants. We hypothesized that (1) addition of N in various specific forms would increase P limitation under conditions with low P availability, i.e. with OP forms and soil minerals , (2) plants shift from N limitation to P limitation would be due to the beneficial effect of N addition on rhizosphere processes involved in P mobilization/acquisition by plants, and (3) the degree of both P limitation and total plant P uptake would vary significantly by mineral type and P forms because of the contrasting physicochemical properties of the minerals used and the biochemical nature of the P sources.

MATERIALS AND METHODS

Organic P compounds, soil minerals and N forms

Two organic P compounds, IHP, GLY, and an IP form (KH2PO4) were chosen for the experiments.

These OP compounds were selected based on their prevalence in most soils and organic wastes. Each selected form differed from the others in P content and molecular size. The minerals were chosen to be representative of the predominant minerals in the soils. Two contrasting individual minerals were used.

Goethite [Fe (OH)O] was chosen as representative of Fe oxyhydroxides; kaolinite was chosen as the

Discussion

Effect N forms and P forms on plant P limitation and P uptake

The N:P ratio is a common indicator of P or N (co-)limitation. Usually, N:P < 12 and N:P > 16 indicate N and P limitation, respectively while co-limitation occurs between 12 and 16 [START_REF] He | Leaf nitrogen and phosphorus of temperate desert plants in response to climate and soil nutrient availability[END_REF][START_REF] Koerselman | The Vegetation N:P Ratio: a New Tool to Detect the Nature of Nutrient Limitation[END_REF][START_REF] Zheng | Altered leaf functional traits by nitrogen addition in a nutrient-poor pine plantation: A consequence of decreased phosphorus availability[END_REF]. Here, we have shown that interactions among N forms, P forms, and soil minerals strongly influence plant N:P ratio and P uptake of ryegrass as compared to individual effects (Table 19). The range in plant N:P ratio (2.5 to 32.31) was consistent with those reported in other studies [START_REF] Güsewell | N : P ratios in terrestrial plants: variation and functional significance[END_REF][START_REF] Von Oheimb | N:P Ratio and the Nature of Nutrient Limitation in Calluna-Dominated Heathlands[END_REF][START_REF] Yang | Divergent Responses of Foliar N:P Stoichiometry During Different Seasons to Nitrogen Deposition in an Old-Growth Temperate Forest, Northeast China[END_REF]. The increase in N:P ratio when N was added to the different mineral-P complexes (Figure 24) suggests that a clear shift from N limitation to P limitation occurred [START_REF] Sardans | Changes in nutrient concentrations of leaves and roots in response to global change factors[END_REF][START_REF] Yang | Divergent Responses of Foliar N:P Stoichiometry During Different Seasons to Nitrogen Deposition in an Old-Growth Temperate Forest, Northeast China[END_REF]. This supports our first hypothesis that N addition under conditions of low P availability would lead to increased P limitation for plant growth [START_REF] Harpole | Nutrient co-limitation of primary producer communities: Community co-limitation[END_REF]Vitousek et al., 2010). In general, with N addition, the N:P ratio of plants grown on mineral-IP sources was between 14.8 and 15.8 which was lower than that observed for plants grown on mineral-OP sources (i.e. between 19.12 to 32.2) (Figure 24). This suggests that, regardless of soil minerals, when N is added the plant becomes N and P co-limited in the presence of IP, whereas the plant switches to P limitation in the presence of OP forms. These results strengthen our expectation that the type and biochemical nature of P sources determine the degree of nutrient limitation in plants (Amadou et al., 2022;Long et al., 2016). The N-induced plant P limitation in the presence of OP forms (IHP, GLY) is likely related to the lower availability and uptake of OP compared to IP forms (Figure 25 and26d). This low availability has been widely demonstrated (Bollyn et al., 2017;Lagos et al., 2016) and would be the result of the high affinity and low desorption of OP forms onto and from soil minerals (Amadou et al., 2022;Ganta et al., 2019). Here, the trend in available P after N addition (mineral-IP > mineral-IHP > mineral-GLY, Figure 26d) resulted in a respective decrease in N:P ratio (Figure 24). Similarly, there was a negative correlation between available P and N:P ratio (Table 21). This means that the degree of P limitation would be strongly dependent on the available P (Long et al., 2016;[START_REF] Zheng | Altered leaf functional traits by nitrogen addition in a nutrient-poor pine plantation: A consequence of decreased phosphorus availability[END_REF], with P limitation being less pronounced under IP forms due to their greater availability to the plant (Figure 25 and Figure 26d). Thus, in systems where P is very highly sorbed (such as OP forms), N additions can indeed lead to rapid depletion of available P (Figure 26d) and thus very high P limitation (Figure 24), but in systems where P is relatively more available (such as IP forms), N additions do not lead to systematic P limitation but rather to colimitation of N and P.

CHAPTER 4

Figure 28 : Picture of the experimental Setup

Plant traits measurement

At harvest (25 days) plants were manually separated from the bulk soil with special care given to ensure minimum damage. Rhizosheath adhering to the roots up to a maximum of 2 mm after shaking was collected and stored at -20 °C for further analysis. Roots were then immersed in 0.20 mM CaCl2 for 1 h, after removing any remaining soil particles by quickly rinsing with CaCl2.The CaCl2 volume was adjusted to ensure a complete immersion of the root system. The solution was then sampled and stored at -20 °C before measuring carboxylic acid exudation by reversed phase column liquid chromatography (RPLC) (Cawthray 2003;Yacoumas et al. 2020). Briefly, an acid mobile phase (93% 25 mM KH2PO4 at pH 2.5 and 7% methanol) allowed a good resolution of five acids (citric, fumaric, maleic, malic, malonic) on a C18 column with a 15 min elution time and a 1 mL min -1 flow rate. Total carboxylate release rate was later calculated as the sum of all previously mentioned acids (see Table 23 for abbreviations).

transformation of the variables and to get rid of the strict assumption that "the residuals will follow a conditionally normal distribution" [START_REF] Mccullagh | Generalized linear models[END_REF][START_REF] Warton | Three points to consider when choosing a LM or GLM test for count data[END_REF] and allow the use of a variety of other distributions of the exponential family for the residuals [START_REF] Cohen | Applied multiple regression/correlation analysis for the behavioral sciences[END_REF]. All factors were tested individually, and the models were compared based on second-order Aikake information (AICc), with the lowest relative value being considered the best fit. The ANOVA of the best-fit GLM model with a chi-square test generated the deviance analysis table that gave the significance level of all factors. Statistical analyses to compare the average results of percent P recovered, enzyme activities, and biomass were performed using a one-way analysis of variance (ANOVA) followed by Tukey's honest significant difference (HSD) test (p < 0.05). As multiple differences were observed between minerals, further analysis was performed separately for each soil minerals type. To identify the main covariation in P-acquisition traits and rhizosphere processes, a principal component analysis (PCA) was performed using the "FactomineR" package on logtransformed data (Lê et al. 2008). The number of components was selected to represent more than 75% of the total variability. Relation between traits were confirmed with Spearman correlation tests as some data did not fulfil the condition of normality. Classification of species on principal components (HCPC)

was then performed to define groups species with similar patterns of P-acquisition traits and influence on the rhizosphere. Classification was performed with a confidence level of over 80%. Differences between clusters/groups for each individual factor were then investigated, either with tests of variance (ANOVA and post-hoc test of Tukey) or non-parametric tests (Kruskall-Wallis test + post-hoc test of Mann Whitney). The selection of the combinations of traits that give the best model fits to predict P uptake was performed in R software with the stepAIC () and bestglm () functions, which are based on the stepwise and best subset approaches. The best-fitting models have a lower AICc and a ΔAICc closer to zero. Differences between models were tested with ANOVA as well as the criteria ΔAICc.

Complementary to GLM regression, partial square path modelling (PLS) was performed to underline the relative ability of trait combinations and type for predicting P uptake. The main goal of PLS was to characterize the contribution of each strategy to P uptake and highlight the main traits involved in these strategies for P acquisition, and how this varies especially with P form. Three clusters of variables, or "latent variables" were defined, respectively, the "morphological traits" variables encompassing root surface area, SRL, fine root percentage, root length density, the "physiological traits" variables encompassing PME activity, carboxylate release and change in rhizosheath pH and the "intermediate traits" variables encompassing foliar [P] and mixed of the previous variables. To ensure the condition of positively correlated variables in a latent variable, the sign of some variables was changed. Variables and components were selected based on their loading and correlation as suggested in Sanchez (2013).

Overall model quality was evaluated with the Goodness of Fit (GoF) index. Analyses were performed with the package "plspm" version 0.4.9. All tests were performed in R version 3.6.0 with a significance level of 0.05.

GLY form

Pisum sativum (C1) showed higher P availability and uptake from OP forms compared to IP forms across both soil minerals. Similarly, the P acquisition strategies of Phacelia tanacetifolia (C4) and

Lupinus albus (C1) led to significantly high P acquisition from OP forms, but only in kaolinite. This improvement in P acquisition from OPs supports our overall hypothesis that P acquisition strategies would differ in their responses to P sources, which would promote greater OP availability and acquisition. Indeed, Vicia faba (C1), Pisum sativum (C1), and Lupinus albus (C1) comprised the "physiological/exudation" group C1 that exhibited the greatest exudation of carboxylic acids, an important activity of PME in the rhizosphere. In addition, trait response analysis to P forms showed that these species had greater total carboxylate release, PME activity, and some morphological traits (SRL, percentage of fine roots) on OP forms than on the IP form. All of these may collectively explain their ability to promote P availability and uptake from OPs forms (García-López et al., 2020;Li et al., 2004).

Thus, in agreement with our second hypothesis, the P acquisition strategies of these species, i.e., pH modification, carboxylate and phosphatase release, would have increased the turnover of OP forms sorbed on goethite and kaolinite via desorption, solubilization and mineralization processes; thus, resulting in increased P availability and acquisition (Guppy et al., 2005;Weisskopf et al., 2006). Indeed, similar to the above species, many plant species belonging to the Fabaceae family have already been classified as efficient solubilizers of OP (Schneider et al., 2019). A wide range of biochemical, physiological, and molecular mechanisms may give Fabaceae a superior dynamic capacity to utilize soil OP more efficiently. Simultaneously, most legumes have a high potential capacity to establish a dual symbiosis with AMF and rhizobia (Sulieman and Mühling, 2021). This tripartite symbiosis may provide an additional potential benefit that could aid in OP mobilization. Similarly, Phacelia tanacetifolia (C4), which belonged more to the morphological group C4, had a high percentage of fine roots and the highest SRL, as well as carboxylates that were all higher on the OP form than on the IP forms. These traits, which would be involved in P foraging, would induce a diffusion gradient which, in turn, would favor the desorption process of the different adsorbed OP forms and thus the availability of P in the soil confirming our first hypothesis (Haling et al., 2018;Rubio et al., 2003;White and Hammond, 2008). These observations are consistent with other results reporting that plant species with finer roots may be more efficient in mobilizing OP from the soil (Haling et al., 2018;Wen et al., 2019) because of their ability to promote the exploration and contact of a larger volume of soil per unit root area (Hammond et al., 2009).

Numerous studies have demonstrated that plants have a limited ability to access P in the form of IHP (the major form of OP) due to its low availability in the soil solution and the low level of extracellular phosphatase or phytase (George et al., 2008;Richardson et al., 2009). It has also been

shown that wheat and many other species are able to utilize P from GLY, and phosphodiesters (DNA and RNA) due to their mining ability, but are limited to acquiring P directly from IHP, although it is abundant in many soils [START_REF]Differential interaction of Aspergillus niger and Peniophora lycii phytases with soil particles affects the hydrolysis of inositol phosphates[END_REF]. However here we found that P acquisition of species (Vicia faba Pisum sativum Phacelia tanacetifolia Lupinus albus) was higher from IHP forms than on GLY forms mining) to OP sources has resulted in greater availability and acquisition of P from OPs. Regardless of strategy, the higher P acquisition from OPs compared to IPs showed that, despite stronger sorption of OPs to the soil, limiting their availability, both plant P foraging and mining strategies were able to improve the cycling and availability of OPs compared to IP forms. Nevertheless, our results highlighted that soil minerals have a central role on the response of P acquisition traits and P availability from OPs is driven by soil mineral properties. The greater P acquisition from OPs in strategies involving P mining than in those involving P foraging emphasizes the importance of plant physiological traits in recycling OPs in the soil. Finally, the identification by modeling of the major traits involved in P mining and foraging and their ability to better predict P acquisition, offer opportunities to design crop species compositions and more specifically functional structure of cultivated plant communities (e.g.

intercropping, cover crops…) to estimate total soil OP reserves and at least its specific forms (IHP, G6P, GLY, etc.) in a multi-species cropping system. We found some species and strategies specific to certain P forms, highlighting specialized ecological niches. In addition, some species and strategies with high plasticity show a wide ecological niche and a strong potential to improve P availability, P recycling from the diversity of P forms in soils or bio-based fertilizers.

DISCUSSION

Facing the depletion of rock phosphate resources, instability of fertilizer prices, and the adverse environmental effects of over-fertilization, practices, and technologies proposing to increase P cycling efficiency in agroecosystems are gaining interest [START_REF] Menezes-Blackburn | Opportunities for mobilizing recalcitrant phosphorus from agricultural soils: a review[END_REF]Richardson et al., 2011) and are increasingly adopted (Sulieman and Mühling, 2021). In this way, P from organic input is increasingly considered as a complement to P fertilizers produced from phosphate rocks (Bennett and Schipanski, 2013). Organic input usa represents a shift from linear utilization of a finite resource to a circular economy as it promotes the reduction of fossil fuel use and greenhouse gas emissions (McCormick and Kautto, 2013) while contributing to the development of new green markets (Zulkifli et al., 2019). The use of OPs to improve P cycling efficiency in cropping systems, however, requires a better understanding of the forms and biochemical properties of various OP interactions with soil minerals and the mechanisms governing their mobilization/acquisition for crop plants. The objectives of this thesis were to understand better the role of OP forms, soil minerals, N, and crop functional traits and their interactions on P availability and acquisition by plants to optimize organic fertilizer management in agroecosystems. Based on a biogeochemical approach, the dynamics of adsorption and desorption of several forms of OP on several representative soil minerals and their influence on OP uptake by plants in ecosystems were elucidated (Chapters 1 and 2). Importantly, the study of interactions between N and OP (Chapter 3) has improved our understanding of ecosystem P cycling under N addition and the biogeochemical properties involved, which is necessary for ecosystem models to accurately predict plant N-P limitation and its impacts. The functional approach adopted here provides valuable information on plant traits and strategies that are very useful for designing cropping systems (the multispecific cover crops, and the succession of cash crops) to increase P availability (Chapter 4).

Furthermore, the references produced and the new knowledge acquired on the influence of plant P acquisition strategy on the P cycle in agroecosystems could contribute to the improvement of existing models and their integration into decision support systems. These systems would in turn allow us to assess the overall effects of organic input-soil-plant interactions on P availability and to support farmers' management decisions such as adapted P fertilization.

Effect of OP forms and soil minerals on OP dynamics and P availability to plants

With the increasing use of organic inputs to replace mineral P fertilizers and the need to recover P from the soil, it is essential to understand better the interactions between various forms of OP and soil minerals and their consequences on P availability (Amadou et al., 2021). A large body of research has evaluated the adsorption of various individual sources of organic and inorganic P to soils or to soil minerals. However, no study has evaluated and compared the P desorption of major OP compounds that have been adsorbed to major soil minerals and their consequence on plant nutrition (Amadou et al., 2022a(Amadou et al., , 2022b)). To help fill this knowledge gap, Chapters 1 and 2 elucidated the dynamics of adsorption and desorption of several forms of OP on several representative soil minerals and the implications for P uptake. Factors related to soil mineral properties and molecular characteristics of OPs directly affected the reactions of OPs and their release into the soil (Chapter 1). Similarly, these factors affected P availability in the rhizosphere and its uptake by the plant (Chapter 2). All OP forms studied (IHP, GLY, and G6P) showed contrasting and significantly different adsorption processes from each other, as well as from the IP form used for comparison (Chapter 1). Desorption experiments revealed that approximately 30% could be readily desorbed (Chapter 1) and this desorbed P was available for plant use (Chapter 2), indicating that adsorbed OPs can act as a source of P for plants (Amadou et al., 2022b).

The trend in OP availability (GLY >> G6P > IHP) highlighted in Chapter 2 was potentially explained by their distinct desorption dynamics (Chapter 1), as the lowest desorption was found for IHP-P, followed by G6P-P and then GLY-P (chapter 2). The trend could also be related to their various degrees of hydrolysis by enzyme activity (Annaheim et al., 2010), as phosphatase activity was the highest in the presence of GLY and the lowest in the presence of IHP (Chapter 2).

The positive relationship between the adsorption dynamics of OPs and the number of phosphate groups in the organic molecule (Chapter 1) was consistent with the literature and shows that the adsorption capacity of each OP compound is determined by the number of orthophosphate groups associated with the C moiety (Bai et al., 2021). IHP, which has six orthophosphates per C moiety, was adsorbed in greater amounts than the other orthophosphate monoesters (G6P and GLY), reinforcing previous explanations of its low desorption (Chapters 1 and 2) and limited utilization by plants (Chapter 2). The generally lower or equal binding strength of IHP to minerals compared to GLY or G6P (Chapter 1), albeit at odds with recent results (Ganta et al., 2019;Kubicki et al., 2012) suggested that the higher adsorption of the IHP compared to other OP compounds (Chapter 1) does not necessarily imply that its binding capacity and/or energy is always strong and stable under all environmental conditions. Thus, it is conceivable that under organic input supply conditions, if GLY and G6P species compete with IHP for the same active sites on soil minerals, the difference in binding energy could facilitate the desorption of IHP from the soil more effectively than GLY and G6P (Amadou et al., 2022a). Correlation analysis performed on different extraction data showed that the availability of adsorbed OPs to plants does not depend on their binding strength to soil minerals (Chapters 1 and 2) but rather on their degree of hydrolysis by soil and root enzymes (Chapter 2). We also pointed out that the general idea of higher adsorption of OPs relative to IP suggested by the literature does not apply to all OP compounds since, although IHP was more strongly retained relative to IP, G6P and GLY were more weakly retained (Figure 31).

The high OP desorption (Chapter 1) and acquisition (Chapter 2) from montmorillonite relative to other minerals (Chapter 2) indicated that soils rich in 2:1 phyllosilicate may have greater P availability

Designing functionally optimal crops with high OP mobilization capacity: insights into species selection, phosphorus acquisition strategies, and N forms

Designing for improved P availability in agroecosystems via management of organic amendment N content and plant P acquisition traits can therefore help address major challenges such as increasing recycled fertilizer use (Faucon et al., 2015). However, this suggests careful consideration when designing crop composition and amendment supply (Hallama et al., 2019). A major implication of this thesis is the potential to manage N forms in organic inputs while adapting crop composition to improve OP availability in agroecosystems through the advantageous effect of N-OP interactions (Chapter 3) but also through the positive response and effect of plant strategies and functional traits (Chapter 4). In general, N-OP interactions resulted in the much greater mobilization of OPs (Chapter 3), furthermore, the effects of the P acquisition strategies of the different species discussed in Chapter 4 were found to favor greater P acquisition from OPs than from IPs. All of these observations indicate that despite the stronger sorption of OPs to soil demonstrated in Chapter 1, which limited their availability for plants in Chapter 2, plant P mining and foraging strategies were successful in improving the cycling and availability of OPs over IP forms (Chapter 4). Taken together, these results can help guide the selection of efficient cropping systems and the formulation of N in organic fertilizers for better mobilization of OP forms. Species groups consisting of Vicia faba, Pisum sativum, and Lupinus albus that produced greater carboxylic acid exudation, and significant PME activity in the rhizosphere than other species in response to OP forms (Nobile et al., 2019), may benefit from fertilization with organic inputs (Figure 32). These species, which are all belonging to the Fabaceae family and whose strategies involve P mining, have promoted greater mobilization/acquisition of OPs than IPs. Consequently, in a rotational system, this could improve P availability that would then benefit subsequent crops, which are generally non-mobilizing (Haling et al., 2018). In practice, since organic inputs slowly increase soil P availability to plants after incorporation into the soil (Gerke, 2015), these Fabaceae species could be the first choice in a crop rotation or in a cover crop to improve crop P content from soil OP forms. The species Lens culinaris, Hordeum vulgare, and Trifolium alexandrinum that respond to OP forms with a high percentage of fine roots and specific root length and intermediate expression of P mining traits, may be more effective in releasing the various forms of OPs adsorbed and/or precipitated on soil constituents, such as IHP which is very strongly adsorbed on the soil (Figure 32). From an agronomic standpoint, a system that combines N-rich organic fertilizer in the form of NO3-N and the establishment of Fabaceae species may be effective in utilizing OPs and specifically IHP, which is the major form of OP in the soil. The arrows represent the different interactions and influences between N forms, organic P forms, and soil minerals and plant P acquisition strategies in the organic fertilizer-soil-plant system.

Considering these processes is expected to allow ecosystem models to accurately predict plant N-P limitation and its impacts, but also to develop robust ecosystem models with fully coupled N-P or C-N-P interactions. At the agricultural level, this would allow the design of crop communities (i.e., multi-species crops), such as cover crops or intercrops, to enhance P

The importance of incorporating the role of P acquisition strategies in OP availability into models and decision support systems for optimal crop and organic fertilizer management

A major implication of examining the response of P acquisition strategies to various forms of inorganic and organic P (Chapter 4) and their consequences for OP availability and P acquisition is the incorporation of this knowledge into modeling approaches. Modeling the role and impact of plant P acquisition strategies, which are related to multiple morphological and physiological traits and interactions among them, allows for the assessment and quantification of the potential benefits and effectiveness of cropping strategies on OP availability and uptake from soil minerals and its potential availability to subsequent crops. Attempts to model these processes, even partially, could provide a basis for incorporating the effects of P acquisition strategies on P availability into decision support systems, allowing farmers to optimize their crop design and management and tailor their OP-rich fertilization (Damon et al., 2014). While the contribution of cover crop P mobilization to subsequent crop P uptake is highlighted in a recent study that suggests incorporating it into models (Hallama et al., 2019;[START_REF] Zhu | Multiple soil nutrient competition between plants, microbes, and mineral surfaces: model development, parameterization, and example applications in several tropical forests[END_REF], as is the contribution of positive microbial feedbacks (Hallama et al., 2019), no model contains a module developed to specifically assess the impact of P acquisition strategies on plant mobilization of different forms of OP. Several models have demonstrated the ability to incorporate P release from crop residues and manures into crop growth and yield projections, including the modeling frameworks The Agricultural Production Systems Simulation (APSIM) [START_REF] Keating | An overview of APSIM, a model designed for farming systems simulation[END_REF], Century [START_REF] Parton | Dynamics of C, N, P and S in grassland soils: a model[END_REF] and CERES-Wheat [START_REF] Daroub | Development of a soil-plant phosphorus simulation model for calcareous and weathered tropical soils[END_REF][START_REF] Nain | Calibration and validation of CERES model for simulating[END_REF]. However, these models require specific and detailed information about the biogeochemical processes that govern the dynamics of OPs, and simple tools that can be used by a layman (Table 28) . The implication of soil types, N and OP composition of amendments, and crop strategies is not widely recognized, and there is currently no decision support system that can predict it from a set of simple and readily available variables (Table 28). Thus, optimization of current models requires detailed information that is not readily available at the farm level (Damon et al., 2014). For instance, several species in this study (Chapter 4) were efficient in utilizing OPs without the assistance of the rhizosphere microbiome.

Several other crop species with different root traits are similarly known to access and mobilize more OP in low P soil (Bates and Lynch, 2000). Thus, the knowledge generated here (Chapter 3 and 4) could be formulated into simple, readily available, and easy-to-use variables, which is advantageous for implementing models as part of a larger decision support system accessible to farmers. Modeling the relationships between the combination of leaf and root traits on P acquisition from OP (Chapter 4) allowed us to reinforce observations of changes in the direct contribution of P acquisition strategies (mining and foraging) on different forms of OP (IHP, G6P, GLY, DNA and RNA) sorbed to different soil mineral conditions, but they also had the benefit of highlighting remaining knowledge gaps to be filled in evaluating the effects of different crop design systems on OP availability. Selection by PLS main gaps in C-N-P interactions that were proposed in this study (black box numbers) are: (1) response and effect of foraging and P-plant mining strategies on OP dynamics; (2) modeling of specific root traits involved in the mobilization efficiency of the OPs used;

(3) a detailed description of the biogeochemical and molecular properties of specific forms of OPs such as IHP, GLY, G6P, and others; (4) trade-offs between root P acquisition traits of crop species for OP mobilization; (5) modeling OP dynamics from various soil minerals; (6) interactive effects of N and OP forms and their interaction with soil minerals on P limitation; (7) mechanistic approach to model C:N:P flexibility and other plant adjustments; (8) modeling the impact of N-OP-mineral interaction on P uptake and P limitation; (9) inorganic P dynamics: effects of soil properties, consistency between time to reach equilibrium between P pools and model time steps; (10) mechanistic representation of root traits, i.e., PME, TCE production, controlled by N and P (other exudates and fungal infection are generally not considered in the models). Role of organic phosphorus forms, soil minerals, nitrogen, and plant functional traits on phosphorus availability and acquisition by plants for optimal organic fertilizer management in agroecosystems Phosphorus (P) deficiency in soils limits the productivity of many agroecosystems. Modern agricultural practices rely heavily on mineral fertilizers derived from mined phosphate rock, a limited and constantly diminishing resource. In an effort to manage P nutrition in agroecosystems more sustainably, organic phosphorus (OP) from organic and soil inputs is increasingly considered as a complement to mineral P fertilizers. However, the dynamics of P supply through organic fertilizer are not always well understood.

APPENDICES APPENDIX A-SUPPLEMENTARY INFORMATION FIRST

We have shown that factors related to soil mineral properties and molecular characteristics of OPs directly affected the reactions of OPs and their release into the soil. Similarly, these factors affected the availability of OPs in the rhizosphere and their uptake by the plant. By characterizing N-OP-mineral interactions we provided important information on ecosystem P cycling under N addition and the biogeochemical properties involved, which will allow ecosystem models to accurately predict plant N-P limitation and its impacts and will also help build robust ecosystem models with fully coupled N-P or C-N-P interactions. The positive response of P acquisition strategies to OP sources has resulted in greater P availability and acquisition from OPs. Finally, the identification through modeling of major traits involved in P acquisition strategies and their ability to better predict P acquisition offers opportunities to design crop species compositions and more specifically the functional structure of crop plant communities. These systems would in turn allow the assessment of the overall effects of organic input, soil, and plant interactions on P availability and support farmers' management decisions, such as appropriate P fertilization.

Keywords: agroecology; biogeochemistry; organic inputs; organic phosphorus; plant traits; Adsorption; desorption; organic phosphorus; phosphorus availability; soil fertility; N and P (co)-limitation; P acquisition strategies; P-foraging; P-mining; ecological niches Rôle des formes de phosphore organique, des minéraux du sol, de l'azote et des traits fonctionnels des plantes sur la disponibilité et l'acquisition du phosphore par les plantes pour une gestion optimale des engrais organiques dans les agroécosytèmes La carence en phosphore (P) des sols limite la productivité de nombreux agroécosystèmes. Les pratiques agricoles modernes sont fortement tributaires des engrais minéraux dérivés de la roche phosphatée