Moez Shiri

Dr Mokded Rabhi
email: mokded.rabhi@gmail.com

Abdelhak El Amrani

Chedly

Abdelhak El Amrani

Chedly Abdelly

Cross-tolerance to abiotic stresses in halophytes: Application for phytoremediation of organic pollutants

Keywords: genomic level, metabolomic level, physiological level, proteomic level, transcriptomic level

published or not. The documents may come

Introduction

Halophytes are plants known for their ability to tolerate high salt levels in the soil. However, no clear definition was given to them and researchers still cannot certainly distinguish between halophytes and glycophytes. [START_REF] Flowers | Salinity tolerance in halophytes[END_REF] call a halophyte any plant able to complete its seed-to-seed cycle at 200 mM NaCl or higher. Halophytes are considered to be rare plant species that arose separately in unrelated plant families during the diversification of Angiosperms (O' Leary and Glenn 1994;[START_REF] Flowers | Salt sensitivity in chickpea[END_REF] similarly to epiphytes, saprophytes, xerophytes, aquatics, and marsh plants [START_REF] Kremer | Evolutionary aspects of life forms in angiosperm families[END_REF]. They were estimated to constitute 1 to 2% of the flora [START_REF] Flowers | Salinity tolerance in halophytes[END_REF]. Several fundamental and applied (economical) potential uses were attributed to halophytes as promising phytoresource. At the fundamental level, they help understand mechanisms involved in high salinity tolerance using morphological, anatomical, ultrastructural, physiological, biochemical, and molecular tools [START_REF] Jithesh | Antioxidative response mechanisms in halophytes: their role in stress defence[END_REF][START_REF] Barhoumi | Ultrastructure of Aeluropus littoralis leaf salt glands under NaCl stress[END_REF][START_REF] Smaoui | Localization of potential ion transport pathways in vesicular trichome cells of Atriplex halimus L[END_REF]Rabhi et al. 2010b;[START_REF] Ellouzi | Early effects of salt stress on the physiological and oxidative status of Cakile maritima (halophyte) and Arabidopsis thaliana (glycophyte)[END_REF][START_REF] Debez | Ecophysiological and genomic analysis of salt tolerance of Cakile maritima[END_REF][START_REF] Hamed | Growth, sodium uptake and antioxidant responses of coastal plants differing in their ecological status under increasing salinity[END_REF]. At the applied level, halophytes are used for food, fodder, forage, edible oil, biofuel, medicines, phytoremediation, phytodesalination, sandy soil fixation, ornamentation… (Khan and Qaiser 2006;Rabhi et al. 2010a, Rabhi et al. 2010d[START_REF] Zaier | Comparative study of Pb-phytoextraction potential in Sesuvium portulacastrum and Brassica juncea: tolerance and accumulation[END_REF][START_REF] Al-Oudat | The halophytic flora of Syria[END_REF].

Among several classifications of halophytes, a habitat-based one distinguishes between xerohalophytes, those thriving under saline arid conditions, and hydrohalophytes, those thriving under saline moist conditions [START_REF] Al-Oudat | The halophytic flora of Syria[END_REF]. In their natural habitats, halophytes are simultaneously subjected to a multitude of abiotic stresses. However, data about pretreatment of halophytes with abiotic stresses such as draught, heavy metals, flooding, and nutrient deficiencies to enhance their tolerance to salinity are scarce. Recently, Ellouzi et al. (2013) investigated the responses of the halophyte Cakile maritima to increasing salt concentrations after pretreatment with three abiotic stresses: drought, salinity, and cadmium. They found that all pretreatments enhanced salt tolerance in this species through oxidative stress alleviation, in particular under severe salinity conditions. A seed priming with a relatively high CaCl2 concentration (50 mM) was also shown to alleviate the adverse effects of high KCl, NaCl, Na2SO4, and MgSO4 concentrations on germination of Urochondra setulosa [START_REF] Shaikh | Effect of calcium and light on the germination of Urochondra setulosa under different salts[END_REF]).

In literature, there are more works about salt-enhanced tolerance to other abiotic stresses than about enhanced salt tolerance by other abiotic stresses in halophytes (See Ben [START_REF] Hamed | Physiological response of halophytes to multiple stresses[END_REF]. In Artemisia anethifolia and Suaeda salsa, salt adaptation enhanced PSII tolerance to heat stress through an improvement of thermotolerance of PSII reaction centers, oxygen-evolving complexes, and light-harvesting complex [START_REF] Lu | The expression of tga1 a gene from tobacco affects the expression of exogenous gene in transgenic plant[END_REF]. In Hordeum maritimum, it was also shown that moderate salinity alleviated the effects of phosphorus deficiency [START_REF] Talbi-Zribi | Alleviation of phosphorus deficiency stress by moderate salinity in the halophyte Hordeum maritimum L[END_REF]. Moreover, under low potassium availability conditions, salt stress improved K/Na selectivity in this halophyte [START_REF] Hafsi | Interactive effects of salinity and potassium availability on growth, water status, and ionic composition of Hordeum maritimum[END_REF]). In the same context, [START_REF] Glenn | Comparison of salinity tolerance of three Atriplex spp. in well-watered and drying soils[END_REF] showed that salinity enhances Atriplex spp. tolerance to drought in drying soils. Beneficial salt effects on Sesuvium portulacastrum responses to drought [START_REF] Slama | Effect of sodium chloride on the response of the halophyte species Sesuvium portulacastrum grown in mannitol-induced water stress[END_REF]) and heavy metals [START_REF] Ghnaya | Cadmium effects on growth and mineral nutrition of two halophytes: Sesuvium portulacastrum and Mesembryanthemum crystallinum[END_REF][START_REF] Zaier | Comparative study of Pb-phytoextraction potential in Sesuvium portulacastrum and Brassica juncea: tolerance and accumulation[END_REF] were also reported. Salt priming was also shown to improve Distichlis spicata establishment under low to moderate salinity conditions [START_REF] Sargeant | Salt priming improves establishment of Distichlis spicata under saline conditions[END_REF].

Cross-tolerance is defined as the phenomenon by which a plant resistance to a stress induces resistance to another (Genoud and Metraux 1999). Because much of the injuries they induce in plants are associated with oxidative damage at the cellular level, oxidative stress tolerance is thought to play a key role in cross-tolerance to a variety of environmental stresses [START_REF] Iseki | Genotypic diversity of cross-tolerance to oxidative and drought stresses in rice seedlings evaluated by the maximum quantum yield of photosystem II and membrane stability[END_REF].

Mechanisms involved in halophyte salt-induced tolerance are common to other abiotic stresses

Cross-tolerance physiology

Intracellular compartmentalization of toxic molecules and osmotic adjustment

As subjected to salt stress, halophytes compartmentalize excess ions predominantly in vacuoles, maintaining in this way their concentrations in the cytoplasm within tolerable limits. They accumulate organic osmolytes such as proline, glycinebetaine, and sugars mainly in cytoplasm for osmotic adjustment without impairing metabolic activities [START_REF] Debez | Responses of Batis maritima plants challenged with up to two-fold seawater NaCl salinity[END_REF]. This significantly contributes to the overall water relations that allow halophytes to obtain water from saline soils [START_REF] Flowers | Salinity tolerance in halophytes[END_REF]. Osmolyte accumulation under salt-induced water deficiency was also observed in the case of direct (insufficiently-irrigated soil) and PEG-and mannitol-induced drought [START_REF] Slama | Effect of sodium chloride on the response of the halophyte species Sesuvium portulacastrum grown in mannitol-induced water stress[END_REF][START_REF] Rouached | Differential performance of tow forage species, Medicago truncatula and Sulla carnosa, under water-deficit stress and recovery[END_REF]. The comparison between Hordeum martimum and H. vulgare after 60 h of salt stress showed that the former is more able to accumulate inorganic solutes (such as Na + ) in vacuoles for osmotic adjustment and to keep organic solutes and a large part of K + for metabolic activities. Such an economic strategy was absent in H. vulgare whose osmotic adjustment was based on organic osmolytes regardless of stress severity [START_REF] Yousfi | Differences in efficient metabolite management and nutrient metabolic regulation between wild and cultivated barley grown at high salinity[END_REF]. [START_REF] Munns | Comparative physiology of salt and water stress[END_REF] reported that the use of one mole of Na + , mannitol, proline, glycinebetaine, or sucrose as an osmoticum in leaf cell needs 3.5, 34, 41, 50, or 52 moles of ATP, respectively. Moreover, even within halophytes themselves, species differ in succulence and in the solutes they accumulate, Chenopodiaceae being more able to use salt ions in osmotic adjustment than Poaceae [START_REF] Flowers | Salinity tolerance in halophytes[END_REF]. Succulence results in an increase in cell size and a decrease in growth extension, this process reduces surface area per tissue volume, leading to higher water content per unit area (Weber 2008).

Maintaining water status within plant tissues requires, in addition to osmotic adjustment, a decrease in water losses through a decline in stomatal conductance (gs). Nevertheless, differences between halophytes were described. For instance, in a comparative study between two obligate halophytes Sesuvium portulacastrum (C3) and Tecticornia indica (C4), different stomata responses were observed at moderate salt concentration (200 mM NaCl); in the former gs was enhanced whereas in the latter it showed no variation. At higher salt concentration (400 mM NaCl), this parameter was decreased in both species. The decrease in gs constitutes an identical early response to water and salt stress [START_REF] Munns | Comparative physiology of salt and water stress[END_REF]. Indeed, plant responses to salt stress occur in two phases: a fast osmotic phase (whose period depends on species and stress severity) due to the increase in external osmotic pressure followed by a slower ionic phase due to ion accumulation in leaves [START_REF] Munns | Mechanisms of salinity tolerance[END_REF]. Water use efficiency (WUE = A / E with A and E standing respectively for net CO2 assimilation and transpiration rate) was shown to be a good tool for measuring the aptitude of a plant to adjust its gas exchanges under stressful conditions by increasing CO2 capture and reducing water losses [START_REF] Gleick | Water-use efficiency and productivity: rethinking the basin approach[END_REF]).

Vacuole sequestration is not limited to salt ions but it is also extended to a variety of toxic ions and molecules such as heavy metals [START_REF] Hossain | Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation[END_REF]) and organic pollutants [START_REF] Tissut | Ecoremediation. Cooperation between plants and soil microorganisms, molecular aspects and limits[END_REF]). In the case of heavy metals, a prior chelation phase is needed [START_REF] Mendoza-Cózatl | Tonoplast-localized Abc2 transporter mediates phytochelatin accumulation in vacuoles and confers cadmium tolerance[END_REF]. As regards organic pollutants, three phases are often described: 1) biotransformation that converts xenobiotics into more polar compounds (in some cases, this phase is not necessary), 2) conjugation that adds to the xenobiotics sugars, amino acids, or peptides to facilitate their metabolism, and 3) sequestration of conjugated molecules into vacuoles or their fixation to the cell wall components [START_REF] Tissut | Ecoremediation. Cooperation between plants and soil microorganisms, molecular aspects and limits[END_REF].

Excretion of toxic molecules

Many halophytes were shown to have trichomes or salt glands controlling salt accumulation in plant tissues. Salt glands are embedded in the leaf epidermis. They can be multicellular, as observed in Dicots (Plumbaginaceae and Tamaricaceae), or bicellular, as reported in Monocots (Poaceae; [START_REF] Barhoumi | Ultrastructure of Aeluropus littoralis leaf salt glands under NaCl stress[END_REF]. Trichomes are composed of two parts: i) a stalk embedded in the epidermis bearing ii) a unicellular bladder cell with a huge vacuole, a well-reduced cytoplasm pushed close to the wall, and only a few organelles [START_REF] Smaoui | Localization of potential ion transport pathways in vesicular trichome cells of Atriplex halimus L[END_REF]. In some cases, salt excretion is performed by leaf cuticle as described in Suaeda fruticosa (Chenopodiaceae), a species with no excreting glands or trichomes [START_REF] Labidi | Salt excretion in Suaeda fruticosa[END_REF]. Hence, salt excretion is a phenomenon by which halophytes eliminate excess salt reaching their leaves (Sobrado 2002) in a highly-selective way, secreting mostly NaCl and thus contributing to maintain a suitable K + /Na + ratio of cell cytoplasm. However, other ions such as K + , Mg 2+ , Ca 2+ , and SO4 2-can be excreted [START_REF] Sobrado | Leaf secretion composition of the mangrove species Avicennia germinans (L.) in relation to salinity: a case study by using total-reflection X-ray fluorescence analysis[END_REF] if they are in excess in leaf tissues. [START_REF] Manousaki | Halophytes an emerging trend in phytoremediation[END_REF] reported also that salt glands and trichomes on leaf surfaces of some halophytes (such as Tamarix smyrnensis, Atriplex halimus, Armeria maritime, Avicennia marina, Avicennia germinans, and Spartina alterniflora) can excrete excess metals as a possible detoxification mechanism.

Nutrient homeostasis

Nutrient homeostasis is one of the major factors allowing halophytes to survive under extreme saline conditions.

It is based on two main strategies: nutrient uptake efficiency and nutrient use efficiency. Since the most abundant salt is NaCl, the former strategy relies on cation/Na + selectivity and anion/Cl -one that increase to mitigate the salt-induced reduction in nutrient uptake efficiency [START_REF] Hafsi | Interactive effects of salinity and potassium availability on growth, water status, and ionic composition of Hordeum maritimum[END_REF]Rabhi et al. 2010c). However, K + /Na + selectivity is the most studied one as this macronutrient is often more affected by salinity than other nutrients.

Although nutrient/salt selectivity is often described in halophytes in response to salt stress, it is not sufficient to maintain nutrient uptake efficiency at the level of the control. This is why high use efficiency is needed [START_REF] Hafsi | Interactive effects of salinity and potassium availability on growth, water status, and ionic composition of Hordeum maritimum[END_REF]Rabhi et al. 2010c). Mineral nutrition is imbalanced by several stresses other than salinity. For instance, the two halophytic Aeluropus species A. lagopoides and A. littoralis displayed an increase in K + and Na + concentrations under drought stress [START_REF] Vaziri | Physiological and biochemical responses of Aeluropus lagopoides and Aeluropus littoralis to drought stress[END_REF]. This is important for osmotic adjustment during water stress as inorganic osmolytes increase osmotic potential. [START_REF] Gulzar | Salt tolerance of a coastal salt marsh grass[END_REF] who observed an enhancement in K + level in A. lagopoides tissues attributed such a response to drought stress to a high selectivity for K + by retaining higher Cl -and Mg 2+ ions in roots. Heavy metal stress is also a factor of nutrition disturbances and plants able to maintain their nutrient homeostasis under this stress are thought to overcome it. For instance, the two halophytes Sesuvium portulacastrum and Mesembryanthemum crystallinum experienced different potassium and calcium status as subjected to a range of cadmium (Cd) concentrations (0, 50, 100, 200, and 300 µM), the former being more able to maintain its nutrient homeostasis than the latter [START_REF] Ghnaya | Effects of Cd 2+ on K + , Ca 2+ and N uptake in two halophytes Sesuvium portulacastrum and Mesembryanthemum crystallinum: consequences on growth[END_REF]. This was due to the fact that S. portulacastrum displayed a higher aptitude to produce biomass and to limit Cd uptake even under severe stress conditions than M. crystallynum [START_REF] Ghnaya | Effects of Cd 2+ on K + , Ca 2+ and N uptake in two halophytes Sesuvium portulacastrum and Mesembryanthemum crystallinum: consequences on growth[END_REF], which is probably due to its higher Ca 2+ and K + selectivity over Cd 2+ . In addition, recently, [START_REF] Zhan | Mitochondrial alterations during Al-induced PCD in peanut root tips[END_REF] found that a K + influx/H + efflux reaction is coupled with the transport of the Polycyclic Aromatic Hydrocarbon (PAH) phenanthrene into root cells, which constitutes a new insight into its uptake by plant roots. This also opens new perspectives on the role of nutrient homeostasis in plant tolerance to organic pollutants, in particular in halophytes.

Membrane integrity

Plant cells contain many membrane systems that are not considered as simple barriers delimiting different compartments; they are specialized to particular functions undertaken by their lipid components and membraneassociated proteins [START_REF] Komatsu | The proteomics of plant cell membranes[END_REF]). Hence, almost all plant responses to environmental stresses directly or indirectly require membrane integrity to be maintained, although stresses themselves cause significant intracellular restructuring [START_REF] Buchanan | Biochemistry and molecular biology of plants[END_REF]. The most studied membranes under abiotic stress conditions are plasmalemma, tonoplast, and thylakoid membranes. Plasmalemma plays structural and communicating (interface with the extracellular environment exchanging information and substances) roles. Hence, it constitutes the site of signal processing in response to stresses [START_REF] Komatsu | The proteomics of plant cell membranes[END_REF]). To estimate membrane integrity under stress, some usual parameters are often used: i) malondialdehyde (MDA) concentration that constitutes an indirect measurement of lipid peroxidation (for all membranes), ii) electrolyte leakage that indicates the degree of the plasmalemma permeability and therefore its inaptitude to retain electrolytes (for plasmalemma since it is the last membrane to be crossed, iii) the correlation between excessive salts within a tissue and its water content to estimate the degree of their sequestration into vacuoles (for tonoplast), and iv) chloroplast ultrastructure that illustrates the degree of damage in grana (for thylakoid membranes). In halophytes, as in all plants, the use of these parameters among others have shown that a variety of severe abiotic stresses induce membrane damages [START_REF] Hassine | Abscisic acid has contrasting effects on salt excretion and polyamine concentrations of an inland and a coastal population of the Mediterranean xero-halophyte species Atriplex halimus[END_REF][START_REF] Parida | Physiological and biochemical responses reveal the drought tolerance efficacy of the halophyte Salicornia brachiata[END_REF], which is due to the generation of Reactive Oxygen Species (ROS) responsible for oxidative stress [START_REF] Bose | ROS homeostasis in halophytes in the context of salinity stress tolerance[END_REF]). Hence, ROS homeostasis is one of the major factors allowing halophytes higher salt tolerance in comparison with glycophytes [START_REF] Bose | ROS homeostasis in halophytes in the context of salinity stress tolerance[END_REF]).

ROS overproduction was described in halophyte responses to several abiotic stresses as reviewed by [START_REF] Jithesh | Antioxidative response mechanisms in halophytes: their role in stress defence[END_REF]. It is initiated by the univalent reduction of O2 or the transfer of excess excitation energy to O2. The transfer of one, two, or three electrons generates respectively superoxide radicals (O2 .-), hydrogen peroxide (H2O2), or hydroxyl radical (HO . ) [START_REF] Mittler | Oxidative stress, antioxidants and stress tolerance[END_REF]. Nevertheless, plants are equipped with two antioxidant systems that can scavenge ROS and therefore protect cell membranes and molecules from damages.

The non-enzymatic system groups a variety of molecules such as tocopherol, carotenoids, ascorbate, and glutathione, whereas the enzymatic one groups several enzymes, namely superoxide dismutase, catalase, ascorbate peroxidase, monohydroascorbate reductase, dehydroascorbate reductase, and glutathione reductase [START_REF] Jithesh | Antioxidative response mechanisms in halophytes: their role in stress defence[END_REF].

Chloroplast (thylakoid membrane) is one of the main targets of ROS. Its protection is therefore a priority in halophytes under stress conditions. Rabhi et al. (2010b) showed that the halophyte Sesuvium portulacastrum is able to protect thylakoid membranes and proteins even at 400 mM NaCl. Similar results were also found in the halophyte Sulla carnosa under magnesium deficiency conditions [START_REF] Farhat | Starch and sugar accumulation in Sulla carnosa leaves upon Mg 2+ starvation[END_REF][START_REF] Farhat | Preferential damaging effects of limited magnesium bioavailability on photosystem I in Sulla carnosa plants[END_REF] as well as under individual and combined effects of salinity and iron deficiency (Unpublished data).

Biochemical and molecular mechanisms of cross-tolerance

Gene duplication and promoter adaptation

Gene duplication is a kind of genome adaptive mechanisms to environment fluctuations [START_REF] Kondrashov | Gene duplication as a mechanism of genomic adaptation to a changing environment[END_REF]. The identification of copy-number variations (CNVs) in response to stressful or changing conditions may help understand gene duplications as an adaptive mechanism. Studies of 80 Arabidopsis thaliana ecotypes showed that natural selection has led to CNVs covering 2.2 Mb of the reference genome [START_REF] Cao | Whole-genome sequencing of multiple Arabidopsis thaliana populations[END_REF]). The genomes of A. thaliana and its halophyte relative Thellungiella parvula have approximately 10% of their total genes in tandem duplicates [START_REF] Dassanayake | The genome of the extremophile crucifer Thellungiella parvula[END_REF], and they are clearly involved in the species dramatically different stress tolerance strategies. This is exemplified by the amplification of NHX8 homologs, known to encode a putative Li + transporter in A. thaliana [START_REF] An | AtNHX8, a member of the monovalent cation: proton antiporter-1 family in Arabidopsis thaliana, encodes a putative Li + /H + antiporter[END_REF]). The duplication led to a constitutively higher expression in T. parvula than in A. thaliana. This was probably responsible for the improvement of T. parvula tolerance to high Li + concentrations in its natural biotope. Some other examples were also reported such as the duplications of CBL10 orthologs, encoding a calcium sensor, AVP1, encoding a vacuolar proton transporter in T. parvula, and HKT, present in a single copy in A. thalina and in three ones in T. parvula [START_REF] Dassanayake | The genome of the extremophile crucifer Thellungiella parvula[END_REF].

Based on molecular and genomic studies, several key transcription factors were identified to be induced under several abiotic stress conditions. Among them, DREB and ABF are well characterized transcription factors known to play an important role in regulating gene expression in response to abiotic stresses through both ABAindependent and dependent pathways. In parallel, many salt-induced promoters are not specific to salinity.

Promoters of the stress-induced genes contain cis-regulatory elements such as DRE/CRT, ABRE, MYC recognition sequence (MYCRS), and MYB recognition sequence (MYBRS), which are regulated by various upstream transcriptional factors [START_REF] Mahajan | Cold, salinity and drought stresses: an overview[END_REF][START_REF] Zhu | Salt and drought stress signal transduction in plants[END_REF]). [START_REF] Nawaz | Expression levels and promoter activities of candidate salt tolerance genes in halophytic and glycophytic Brassicaceae[END_REF] compared expression levels and promoter activities of candidate salt tolerance genes in the halophyte T. salsuginea and the glycophyte A. thaliana using promoter swap experiments. They showed that SOS1 and VATD promoters were respectively five-fold and two-fold more active in T. salsuginea than in A. thaliana. These observations were supported by an expression of a higher number of gene families nonspecific to salt stress in the halophyte than in the glycophyte [START_REF] Wu | Insights into salt tolerance from the genome of Thellungiella salsuginea[END_REF]. [START_REF] Wu | Insights into salt tolerance from the genome of Thellungiella salsuginea[END_REF] found that 21 transcription factor families were expanded in T. salsuginea genome as compared to that of A. thaliana. These expansions may be associated with the adaptation of T. salsuginea to extreme environments, as individual members of some A. thaliana factor families have been shown to be related to stress tolerance. For example, the RAV gene family that has been reported to respond to several stresses, including salinity [START_REF] Fowler | Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock[END_REF][START_REF] Sohn | Expression and functional roles of the pepper pathogen-induced transcription factor RAV1 in bacterial disease resistance, and drought and salt stress tolerance[END_REF], expanded from six members to nine, respectively in A. thaliana and T. salsuginea [START_REF] Wu | Insights into salt tolerance from the genome of Thellungiella salsuginea[END_REF]). In the extreme halophyte Salicornia brachiata, transcript profiling revealed an abundance of SbUSP (an uncharacterized universal stress protein gene) transcripts in response to salt stress as well as to drought, heat, and cold stresses. Heterologous expression of this gene conferred salt and osmotic tolerance to E. coli (Udawat et al. 2013). Some other salt-responsive genes cloned from this halophyte experienced also elevated expression under abiotic stress conditions in the host plant. For instance, SbMT-2 gene was up-regulated by salinity, drought, and heat stresses and its expression increased with treatment time [START_REF] Chaturvedi | Cloning and transcript analysis of type 2 metallothionein gene (SbMT-2) from extreme halophyte Salicornia brachiata and its heterologous expression in E. coli[END_REF]. The peroxisomal ascorbate peroxidase gene (SbpAPX) was also strongly induced by cold [START_REF] Singh | Over-expression of the peroxisomal ascorbate peroxidase (SbpAPX) gene cloned from halophyte Salicornia brachiate confers salt and drought stress tolerance in transgenic tobacco[END_REF]). In addition, pAPX gene cloned from Avicenia marina was up-regulated by salinity, H2O2, prolonged light, and ferric citrate treatment [START_REF] Kavitha | An oxidative and salinity stress induced peroxisomal ascorbate peroxidase from Avicennia marina: molecular and functional characterization[END_REF]). In the same context, a SUMO conjugating (Small Ubiquitin related Modifier) enzyme gene 'SaSce9' from experienced induced transcripts under salinity, drought, cold, and exogenously supplied ABA conditions in leaves as well as in roots of the halophytic grass Spartina alterniflora. Its constitutive overexpression in A. thaliana improved its tolerance to salinity and drought [START_REF] Karan | A stress inducible SUMO conjugating enzyme gene (SaSce9) from a grass halophyte Spartina alterniflora enhances salinity and drought stress tolerance in Arabidopsis[END_REF]. In the halophyte Limoniastrum monopetalum, [START_REF] El-Bakatoushi | Identification and characterization of up-regulated genes in the halophyte Limoniastrum monopetalum (L.) Boiss grown under crude oil pollution[END_REF] showed that crude oil exposure over-expressed salt and drought genes.

Wide genome transcriptional adaptation to abiotic stresses

Proteomic analysis revealed the induction of several non specific-stress-and defense-related proteins

While addressing the key pathways regulating abiotic stress plant adaptation, comprehensive data presented confirmed that proteins are relevant tools to confer tolerance. Therefore, it has been found out that salinity induces more proteomic changes in A. thaliana than in T. salsuginea [START_REF] Oliver | Proteome analysis of leaves of the desiccation-tolerant grass, Sporobolus stapfianus, in response to dehydration[END_REF][START_REF] Gechev | Molecular mechanisms of desiccation tolerance in resurrection plants[END_REF][START_REF] Dooki | Proteomic responses of rice young panicles to salinity[END_REF]). The former displayed 88 differentially abundant protein spots versus 37 ones in T. salsuginea as compared to their controls [START_REF] Dooki | Proteomic responses of rice young panicles to salinity[END_REF]. Therefore, salinity changes more the proteomic profile of A. thaliana as compared to that of T. salsuginea since the latter is able to maintain enough photosynthetic activity and ATP production for stress adjustment. A proteomic study of Suaeda salsa under individual and combined effects of salinity and heat shock showed that out of 80 proteins whose levels were increased by salt stress and 70 proteins whose levels were reduced by heat shock, an overlap of only 17 proteins was detected. In addition, out of 112 proteins accumulated by the combined effects, only 43 were salt-elevated and 30 were heat shockelevated [START_REF] Li | Construction of rice site-specific chloroplast transformation vector and transient expression of EGFP gene in Dunaliella salina[END_REF]). Hence, among 124 induced proteins (during salinity, heat shock, or their combination), only 14 were common in the three treatments [START_REF] Li | Construction of rice site-specific chloroplast transformation vector and transient expression of EGFP gene in Dunaliella salina[END_REF]. Interestingly, the authors found an overexpression of STO5 not only by salt stress but also by heat shock and their combination, which can lead to higher salt tolerance in transgenic plants [START_REF] Nagaoka | Salt tolerance-related protein STO binds to a Myb transcription factor homologue and confers salt tolerance in Arabidopsis[END_REF]). An aluminum-induced protein-like protein (AIPLP) that has been shown to be involved not only in aluminum stress response but also in other metal, wounding [START_REF] Snowden | Aluminum-induced genes: induction by toxic metals, low calcium, and wounding and pattern of expression in root tips[END_REF], and drought stress responses [START_REF] Oztürk | Monitoring large-scale changes in transcript abundance in drought-and salt-stressed barley[END_REF], was induced in Puccinellia tenuiflora under 95 mM Na2CO3 treatment, which suggests that it might also contribute to its tolerance to Na2CO3 stress [START_REF] Yu | Comparative proteomic analysis of Puccinellia tenuiflora leaves under Na2CO3 stress[END_REF]). In addition, a developmentally-regulated plasma membrane polypeptide (DREPPPM)-like protein that has been shown to be involved in cold acclimation and salt stress, increased under Na2CO3 stress. This protein may be associated with the Ca 2+ signal transduction pathway in the seedlings of Puccinellia tenuiflora under Na2CO3 stress [START_REF] Yu | Comparative proteomic analysis of Puccinellia tenuiflora leaves under Na2CO3 stress[END_REF]).

Cross-tolerance-enhanced abundance of protective proteins involved in photosynthesis activation and protein biosynthesis

Abiotic stresses negatively affect photosynthesis at different levels, altering both photochemichal and nonphotochemical processes [START_REF] Saibo | Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses[END_REF]). Nevertheless, plants have developed many adaptive strategies allowing them to cope with severe conditions [START_REF] Zhu | Salt and drought stress signal transduction in plants[END_REF][START_REF] Saibo | Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses[END_REF]). Identification of photosynthesisrelated proteins that are differentially abundant under drought and severe salt stress is very important. So far, many photosynthesis-related proteins exhibited an increase or decrease in response to these two stresses [START_REF] Oliver | Proteome analysis of leaves of the desiccation-tolerant grass, Sporobolus stapfianus, in response to dehydration[END_REF][START_REF] Vanhove | Screening the banana biodiversity for drought tolerance: can an in vitro growth model and proteomics be used as a tool to discover tolerant varieties and understand homeostasis[END_REF][START_REF] Aranjuelo | Plant physiology and proteomics reveals the leaf response to drought in alfalfa (Medicago sativa L.)[END_REF]). The comparison between halophyte and glycophyte proteins under salt stress reviewed by [START_REF] Kosová | Proteome analysis of cold response in spring and winter wheat (Triticum aestivum) crowns reveals similarities in stress adaptation and differences in regulatory processes between the growth habits[END_REF] reported an increase in PsbP, ferredoxin-NADPH reductase, OEE2, RubisCO activase, TPI, GAPDH, and Glucose-6-P dehydrogenase in glycophytes and an increase in LHC, OEE2, RubisCO LSU and SSU, RubisCO activase, D2, CP24, CP47, PSI subunit IV, carbonic anhydrase; SBP, and PGK. In response to salinity, non-salt-specific proteins can be accumulated. For instance, [START_REF] Chen | Salinity-induced changes in protein expression in the halophytic plant Nitraria sphaerocarpa[END_REF] found an enhanced abundance in eleven heat-shock proteins (HSPs) in the halophyte Nitraria sphaerocarpa under saline conditions. Based on literature and their own results, the authors suggested an HSP/chaperone network in plants that responds to salinity. As subjected to salt stress, the halophytic plant Puccinellia tenuiflora exhibited an increased abundance of tocopherol cyclase, a crucial enzyme in the biosynthesis of α-tocopherol in plants [START_REF] Yu | Physiological and proteomic analysis of salinity tolerance in Puccinellia tenuiflora[END_REF]) conferring it higher stress tolerance. It is also known that free metal ions can catalyze ROS formation. Therefore, responses leading to the elimination of free metal ions were observed in salt-stressed plants [START_REF] Kosová | Proteome analysis of cold response in spring and winter wheat (Triticum aestivum) crowns reveals similarities in stress adaptation and differences in regulatory processes between the growth habits[END_REF]. Stress also results in an accumulation of several protective proteins as chaperones from HSP90 family, HSP70 family, and Hsc70 (heat-shock cognate) [START_REF] Kosová | Proteome analysis of cold response in spring and winter wheat (Triticum aestivum) crowns reveals similarities in stress adaptation and differences in regulatory processes between the growth habits[END_REF]. Other stress-protective proteins, such as osmotin and osmotin-like proteins, are involved in enhancing osmotic stress responses. PR-10 proteins respond not only to biotic, but also to abiotic stresses, such as drought, salt, cold, and oxidative stresses, and UV-irradiation [START_REF] Agarwal | A study on the influence of different promoter and 5'UTR (URM) cassettes from Arabidopsis thaliana on the expression level of the reporter gene βglucuronidase in tobacco and cotton[END_REF].

Abiotic-stress-commonly-induced alterations in carbohydrate nutritional status

Sugar metabolism is a very dynamic process and its metabolic fluxes and concentrations highly fluctuate with development stage and in response to environmental stresses [START_REF] Rolland | Sugar sensing and signaling in plants: conserved and novel mechanisms[END_REF]. Under abiotic stress, glucose has an important role as osmolytes in maintaining cell turgor, stabilizing cell membranes, and decreasing protein degradation [START_REF] Sharp | Root growth maintenance during water deficits: physiology to functional genomics[END_REF]). Non-reducing disaccharides such as trehalose can accumulate with higher levels in tolerant plants. Other sugars with no energetic role, such as the oligosaccharides raffinose and stachyose were accumulated in response to abiotic stress conditions such as drought, salinity, and extreme temperatures [START_REF] Kaplan | Exploring the temperature-stress metabolome of Arabidopsis[END_REF]. Relevant physiological studies have shown that soluble carbohydrates, like glucose, fructose, sucrose, or fructans, significantly contribute to the mechanisms of adaptation to salt stress [START_REF] Parida | NaCl stress causes changes in photosynthetic pigments, proteins and other metabolic components in the leaves of a true mangrove, Bruguiera parviflora, in hydroponic cultures[END_REF]. [START_REF] Gil | Soluble carbohydrates as osmolytes in several halophytes from a Mediterranean salt marsh[END_REF] studied sugar accumulation in five halophytes (Juncus acutus, Juncus maritimus, Plantago crassifolia, Inula crithmoides, and Sarcocornia fruticosa) and found that sucrose, and at a lower level, glucose and fructose were the most abundant sugars in J. acutus and J. maritimus, and sorbitol the only soluble sugar accumulated in P. crassifolia. In addition to their involvement in osmotic adjustment, soluble carbohydrates stabilize also proteins and membrane structure and protect plant cell against ROS, especially in halophyte species [START_REF] Szabados | Proline: a multifunctional amino acid[END_REF][START_REF] Boriboonkaset | Regulation of some carbohydrate metabolism-related genes, starch and soluble sugar contents, photosynthetic activities and yield attributes of two contrasting rice genotypes subjected to salt stress[END_REF]. Polyols and sugar alcohols like mannitol or sorbitol were also accumulated and linked to abiotic stress tolerance [START_REF] Arbona | Antioxidant enzymatic activity is linked to waterlogging stress tolerance in citrus[END_REF]. In addition to all cited roles, sucrose, fructose, and glucose play also pivotal roles as signaling molecules to abiotic stresses [START_REF] Koch | Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development[END_REF][START_REF] Rolland | Sugar sensing and signaling in plants: conserved and novel mechanisms[END_REF][START_REF] Ruan | Sucrose metabolism: gateway to diverse carbon use and sugar signaling[END_REF].

Enhanced biosynthesis of organic osmolytes, phenolic compounds, and lignin

Under abiotic stresses, plants synthesize osmolytes like soluble sugars and amino acids that contribute to turgor maintaining by osmotic adjustment [START_REF] Arbona | Enzymatic and non-enzymatic antioxidant responses of Carrizo citrange, a salt-sensitive citrus rootstock, to different levels of salinity[END_REF][START_REF] Arbona | Antioxidant enzymatic activity is linked to waterlogging stress tolerance in citrus[END_REF]. In this context, it is interesting to follow the synthesis and levels of osmolytes involved in stress tolerance such as amino acids, secondary metabolites, and regulatory metabolites [START_REF] Arbona | Metabolomics as a tool to investigate abiotic stress tolerance in plants[END_REF]. Indeed, increases in Proline (Pro) content have been reported in response to a variety of abiotic stress conditions like salt stress [START_REF] Yoshiba | Characterization of a cDNA clone encoding 23 kDa polypeptide of the oxygen-evolving complex of photosystem II in rice[END_REF][START_REF] Arbona | Antioxidant enzymatic activity is linked to waterlogging stress tolerance in citrus[END_REF]), soil flooding (De Campos et al. 2011), drought [START_REF] Arbona | Antioxidant enzymatic activity is linked to waterlogging stress tolerance in citrus[END_REF], and extreme temperatures [START_REF] Kaplan | Exploring the temperature-stress metabolome of Arabidopsis[END_REF]). The target enzyme is a pyrroline-5-caboxylate synthetase (P5CS) [START_REF] Arbona | Antioxidant enzymatic activity is linked to waterlogging stress tolerance in citrus[END_REF]. Pro plays also a role in ROS scavenging [START_REF] Arbona | Enzymatic and non-enzymatic antioxidant responses of Carrizo citrange, a salt-sensitive citrus rootstock, to different levels of salinity[END_REF] as well as in DNA, membrane, and protein stabilization [START_REF] Arbona | Antioxidant enzymatic activity is linked to waterlogging stress tolerance in citrus[END_REF]. Polyamines (PA) also have protective ROS scavenging roles [START_REF] Alet | New insights into the role of spermine in Arabidopsis thaliana under long-term salt stress[END_REF]. A variety of abiotic stresses were shown to induce PA accumulation that was found to positively correlate with stress tolerance [START_REF]Conjugated polyamines and reproductive development: Biochimical, molecular and physiological approaches[END_REF][START_REF] Bitrián | Polyamines under abiotic stress: metabolic crossroads and hormonal cross talks in plants[END_REF]. Putrescine (Put), spermidine (Spd), and spermine (Spm) are the most abundant PAs found in higher plants [START_REF] Arbona | Metabolomics as a tool to investigate abiotic stress tolerance in plants[END_REF]. It has been recently reported that, in nonadapted Thellungiella salsuginea accessions, sugars and polyamines could be involved in the mechanisms of cold adaptation [START_REF] Colinet | Exploring the plastic response to cold acclimation through metabolomics[END_REF]. However, the most described and important compounds are sugars, sugar alcohols, and nitrogenous compounds with low molecular weight (in particular Pro and glycinebetaine). Their accumulation in adapted plants is thought to be involved in their tolerance to stresses [START_REF] Witt | Metabolic and phenotypic responses of greenhouse-grown maize hybrids to experimentally controlled drought stress[END_REF]. Under heavy metal stress, to reduce metal accumulation in photosynthetic organs is considered as a tolerance trait like phytochelatin biosynthesis and glutathione metabolism [START_REF] Arbona | Metabolomics as a tool to investigate abiotic stress tolerance in plants[END_REF].

It is known that heat induces PAL activity and phenolic production and reduces, at the same time, their oxidation, contributing to heat stress acclimation [START_REF] Arbona | Metabolomics as a tool to investigate abiotic stress tolerance in plants[END_REF]. The precursors of lignins, phenylpropanoids are also involved in stress defense mechanisms, in particular in roots where they can adjust cell wall composition and stiffness [START_REF] Van Poecke | Herbivore-induced volatile production by Arabidopsis thaliana leads to attraction of the parasitoid Cotesia rubecula: chemical, behavioral, and gene-expression analysis[END_REF][START_REF] D'auria | The secondary metabolism of Arabidopsis thaliana: growing like a weed[END_REF].

Carotenoids and xanthophylls are lipophilic compounds synthesized in plants from isopentenyl pyrophosphate (IPP) via the plastidial methyl erythritol phosphate (MEP) pathway. The role of carotenoids is not restricted to cell protection from UV radiation under stress conditions. Indeed, it was demonstrated that the overexpression of phytoene synthase gene in transgenic tobacco plants resulted in a higher osmotic and salt tolerance, but through channeling carotenoid flux to ABA biosynthesis which resulted in an enhancement of ABA levels [START_REF] Cidade | Ectopic expression of a fruit phytoene synthase from Citrus paradisi Macf. promotes abiotic stress tolerance in transgenic tobacco[END_REF].

The following diagram (Figure ) summarizes specific and non-specific responses to combined stresses.

Figure.

Schematic diagram showing the possible cross-talk involved in the response of halophytes to multiple stresses. The signal pathways resulting from several stresses induce specific and non-specific genes that can confer stress-tolerance. The latter are responsible for cross-tolerance. GPCR: G-protein-coupled receptor; RLK: receptor-like kinase; CBL: calcineurin B-like interacting protein kinase; CPK: calcium-dependent protein kinase; MAPK: mitogen-activated protein kinase; ROS: reactive oxygen species; TFs: transcription factors.

Cross-tolerance between salinity and organic pollutants: application for phytoremediation

Compartmentalization and subcellular sequestration are common mechanisms involved in salinity and organic pollutant tolerance

As heavy metals and salts, organic pollutants constitute one of the major hazardous chemicals that contaminate soils today (El-Bakatoushi 2011). The uptake of toxic organics in plant cells and/or their sequestration or metabolism are essential for detoxification of the rhizosphere and in turn for phytoremediation. Therefore, organic pollutants such phenanthrene may passively penetrate the plasmalemma of root and shoot cells [START_REF] Alkio | Stress responses to polycyclic aromatic hydrocarbons in Arabidopsis include growth inhibition and hypersensitive response-like symptoms[END_REF]. [START_REF] Wild | A novel analytical approach for visualizing and tracking organic chemicals in plants[END_REF] traced the movement of anthracene in maize leaves and showed that it was localized on the leaf surface; it diffused into the cytoplasm within 72 h. This finding was supported by [START_REF] Alkio | Stress responses to polycyclic aromatic hydrocarbons in Arabidopsis include growth inhibition and hypersensitive response-like symptoms[END_REF] who showed that phenanthrene can diffuse in Arabidopsis through direct contact with the tissue as well as from the air. Also, [START_REF] Zhan | Dynamics of active organic carbon in a paddy soil under different rice farming modes[END_REF] found in wheat two modes of phenanthrene transport; a simple diffusion and an active absorption by a transporter. In the same context, [START_REF] Cobbett | Arabidopsis and the genetic potential for the phytoremediation of toxic elemental and organic pollutants[END_REF] reported that the uptake of organic xenobiotics into the plant cell is often mediated by an ABC transport protein. A subclass of the ABC transporters, originally named the multi drug resistance proteins (MRPs) in reference to animal cells and bacteria, is the best-characterized family of plant proteins that carry organics across membranes. MRPs are involved in the uptake, efflux, and sequestration of toxic compounds and xenobiotics [START_REF] Tommasini | An ABC-transporter of Arabidopsis thaliana has both glutathione-conjugate and chlorophyll catabolite transport activity[END_REF]. In literature, little is known about the mechanisms of Polycyclic Aromatic Hydrocarbon (PAH) metabolism and accumulation in plants. All authors used the green lever model to explain plant cell internalization, degradation, and sequestration of organic compounds such as PAHs (Sandermann 1992). In plants, the metabolism of xenobiotics can be divided into three phases leading to the neutralization of the organic pollutant: transformation (Phase I), conjugation (Phase II), and compartmentalization (Phase III) (Sandermann 1992). The first two phases are similar to those used by animals. During phase I, the compound is transformed by oxidation (frequently), reduction, or hydrolysis, creating one or more functional groups on the molecule (Komives and Güllner 2005).

The hydrophobic character of organic pollutants like PAHs suggests hydroxylation by specific enzymes to transform them into hydro-soluble compounds in cytoplasm. Hence, in phase II, one or more substituents are attached onto endogenous or existing active sites formed during Phase I. The main reactions include conjugation of glycosides, glutathione, amino acid, or malonic acid. During phase III, the soluble compounds are either stored in the vacuole or incorporated into lignin or other cell wall components of becoming non-extractable. Due to its similarity with the hepatic detoxification mechanisms in animals, the term "green liver" has been adopted for the operation of plant cells during xenobiotic metabolism [START_REF] Hjr | Higher plant metabolism of xenobiotics: the "green liver" concept[END_REF]. This concept was supported by [START_REF] Alkio | Stress responses to polycyclic aromatic hydrocarbons in Arabidopsis include growth inhibition and hypersensitive response-like symptoms[END_REF] who demonstrated that in A. thaliana, phenanthrene was detected and sequestrated in particular cell "trichomes" and after higher amount of PAHs it was diffused to basal unclear cells, with increased the levels of particular mono-or dioxygenases that allow increased tolerance and transform PAHs to non-toxic intermediate compounds during phase I [START_REF] Cerniglia | Fungal metabolism of polycyclic aromatic hydrocarbons: past, present and future applications in bioremediation[END_REF][START_REF] Kanaly | Biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons by bacteria[END_REF].

Similarly, since monovalent ions, used by halophytes and salt-tolerant glycophytes for osmotic adjustment, are toxic at the required concentrations, Na + and Cl -are predominantly vaculole-compartmentalized to maintain their concentrations in the cytoplasm within tolerable limits (Whyn Jones and Gorham 2002).

Although the evidence is limited, Na + /H + exchange and the activity of one or more of the PMF-generating enzymes appear to play a role in the accumulation of Na + as they increase under saline conditions. However, ion transport across tonoplast is not sufficient for efficient compartmentalization; their retention within vacuoles is also required and was shown to be correlated with low tonoplast fluidity [START_REF] Leach | Quantitatively determined self-incompatibility: 2. Outcrossing in Borago officinaux[END_REF]). Hence, one can speculate that since halophytes are more efficient in saline ion compartmentalization than glycophytes, they are theoretically more able to sequester any other toxic ion or compound.

3.2. ROS accumulation and signaling are common features shared between stresses induced by salinity and organic pollutants [START_REF] Liu | An oxidative stress response to polycyclic aromatic hydrocarbon exposure is rapid and complex in Arabidopsis thaliana[END_REF] suggested that phenanthrene oxidized by mono-or di-oxygenases, like the CYP, increased ROS level, which induces oxidative stress. However, it cannot be confirmed if oxidative stress is a consequence of phenanthrene detoxification activities or of its own or derivative phytotoxicity [START_REF] Liu | An oxidative stress response to polycyclic aromatic hydrocarbon exposure is rapid and complex in Arabidopsis thaliana[END_REF]. ROS production is an unavoidable event for all organisms exposed to oxygen and Na + and Cl -accumulation in the cytosol increased ROS production (Allakhverdiev et al. 2002). The result of hydroxylation of organic pollutant by cytochrome P450 generated also ROS production. A higher antioxidant capacity in halophytes than in glycophytes has been suggested to confer them a higher tolerance to stresses such as salinity [START_REF] Flowers | Salinity tolerance in halophytes[END_REF][START_REF] Kosová | Proteome analysis of cold response in spring and winter wheat (Triticum aestivum) crowns reveals similarities in stress adaptation and differences in regulatory processes between the growth habits[END_REF]) and phenanthrene toxicity [START_REF] Shiri | The halophytic model plant Thellungiella salsuginea exhibited increased tolerance to phenanthrene-induced stress in comparison with the glycophitic one Arabidopsis thaliana: Application for phytoremediation[END_REF]. [START_REF] Mittler | Abiotic stress, the field environment and stress combination[END_REF] reported that the exposure of a plant to a combination of several abiotic stresses will co-activate different stress-response pathways. The results of stress combination have a synergistic or antagonistic effect. This suggests that a crosstalk between co-activated pathways is likely to be mediated at different levels. These could involve a variety of transcription factor networks, mitogen-activated protein kinases (MAPK) [START_REF] Cardinale | Convergence and divergence of stress-induced mitogenactivated protein kinase signaling pathways at the level of two distinct mitogen-activated protein kinase kinases[END_REF][START_REF] Xiong | Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase[END_REF], a multitude of stress hormones (ethylene, jasmonic acid, and abscisic acid) [START_REF] Anderson | Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis[END_REF]), calcium and/or ROS signaling [START_REF] Mittler | Reactive oxygen gene network of plants[END_REF][START_REF] Bowler | The role of calcium and activated oxygens as signals for controlling cross-tolerance[END_REF] as well as numerous receptors and signaling complexes [START_REF] Casal | Environmental cues affecting development[END_REF].

The stress tolerance by increasing antioxidant activity is attractive to explain a high tolerance in halophytes to organic pollutants that generated an oxidative stress [START_REF] Liu | An oxidative stress response to polycyclic aromatic hydrocarbon exposure is rapid and complex in Arabidopsis thaliana[END_REF]. Therefore, the higher levels of enzymatic antioxidants in halophytes, in particular that of SOD, suggest that the crucial role to rapid conversion of O2 .-to H2O2 may be essential for early defense signaling. Halophyte species induced rapidly H2O2 levels, then they have higher SOD level 'in stock' [START_REF] Bose | Role of magnesium in alleviation of aluminium toxicity in plants[END_REF]. Secondly, high levels of APX and CAT may interfere with H2O2 signaling and decrease its positive role. However, only OH . is highly reactive and causes significant damage to cell structures and is the major compound resulting from hydroxylation of PAHs, it is also known to activate directly a range of Na + , K + , and Ca 2+ -permeable cation channels [START_REF] Demidchik | Arabidopsis root K + -efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death[END_REF][START_REF] Zepeda-Jazo | Polyamines interact with hydroxyl radicals in activating Ca (2+) and K (+) transport across the root epidermal plasma membranes[END_REF]) disturbing K + /Na + ratio within cytoplasm and inducing programmed cell death (PCD) [START_REF] Shabala | Expression of animal CED-9 anti-apoptotic gene in tobacco modifies plasma membrane ion fluxes in response to salinity and oxidative stress[END_REF][START_REF] Shabala | Salinity and programmed cell death: unravelling mechanisms for ion specific signaling[END_REF][START_REF] Demidchik | Arabidopsis root K + -efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death[END_REF].

The understanding of salinity and organic pollutant tolerance may help improve phytoremediation

Phytoremediation is known as a green technology using plants to remediate contaminated-environments. It is cheap, non-instructive, and effective means of pollutant cleanup. In literature, little is known about halophyte use in phytoremediation of organic pollutants. The majority of the examples of phytoremediation by halophytes was reported in salt marshes, their natural habitats [START_REF] Howes Keiffer | Germination and establishment of halophytes on brine-affected soils[END_REF][START_REF] Sorkhoh | Oil phytoremediation potential of hypersaline coasts of the Arabian Gulf using rhizosphere technology[END_REF][START_REF] Masciandaro | Phytoremediation of dredged marine sediment: monitoring of chemical and biochemical processes contributing to sediment reclamation[END_REF][START_REF] Ribeiro | Potential of phytoremediation for the removal of petroleum hydrocarbons in contaminated salt marsh sediments[END_REF]). Salt marshes constitute important ecosystems severely exposed to risks due to the oil spills resulting from accidental discharges, leakage from boats, industrial wastewater discharges, and urban runoff [START_REF] Ribeiro | Potential of phytoremediation for the removal of petroleum hydrocarbons in contaminated salt marsh sediments[END_REF]. Phytoremediation of organic pollutants is based on the observation that planted contaminated soil versus unplanted soil showed on acceleration of organic pollutant degradation in the presence of plants (Burken and Schonoor 1996;[START_REF] Masciandaro | Phytoremediation of dredged marine sediment: monitoring of chemical and biochemical processes contributing to sediment reclamation[END_REF]. There are two different strategies of phytoremediation: direct and explanta phytoremediation [START_REF] Salt | Phytoremediation[END_REF]). The first one consists of pollutant uptake by analogy to phytoextraction of heavy metals. However, the availability of organic pollutants depends on their physicochemical properties and their concentration in soil [START_REF] Wenzel | Phytoremediation: a plant-microbe-based remediation system[END_REF]). The second one is based on exudates synthesized by roots like enzymes involved in the degradation of organic pollutants and other compounds stimulating fungi and bacteria growth that use pollutants as carbon source.

In this context, phytoremediation of organic pollutants remains unexplored enough. The majority of investigations in this field focused on the interaction between microorganisms and roots to improve the degradation of organic pollutants in soil. Some studies reported that PAHs can be taken up by plant leaves from air or by their roots from soil [START_REF] Simonich | Vegetation-atmosphere partitioning of polycyclic aromatic hydrocarbons[END_REF][START_REF] Kipopoulou | Bioconcentration of polycyclic aromatic hydrocarbons in vegetables grown in an industrial area[END_REF][START_REF] Fismes | Soil-to-root transfer and translocation of polycyclic aromatic hydrocarbons by vegetables grown on industrial contaminated soils[END_REF]. Indeed, because of their high lipophily, they are adsorbed either on leaf cuticle and passed through it by solubilization in waxes or on root suberine cortical zones and absorbed by root cells [START_REF] Simonich | Vegetation-atmosphere partitioning of polycyclic aromatic hydrocarbons[END_REF][START_REF] Kipopoulou | Bioconcentration of polycyclic aromatic hydrocarbons in vegetables grown in an industrial area[END_REF][START_REF] Fismes | Soil-to-root transfer and translocation of polycyclic aromatic hydrocarbons by vegetables grown on industrial contaminated soils[END_REF]. The halophyte Halocnemum strobilaceum naturally inhabiting hypersaline soils was shown to remediate soil contaminated by aromatic hydrocarbon in the Arabian Gulf [START_REF] Sorkhoh | Oil phytoremediation potential of hypersaline coasts of the Arabian Gulf using rhizosphere technology[END_REF]. A 'phytoremediation' culture of Cakile maritima on sterilized sand (without microorganisms) contaminated with phenanthrene significantly decreased its phytotoxicity in a subsequent culture of Thellungiella salsuginea [START_REF] Shiri | The halophyte Cakile maritima reduces phenanthrene phytotoxicity[END_REF]. [START_REF] Meudec | Uptake of four PAHs occurring into aerial plant tissue artificially exposed to heavy fuel oil in Salicornia[END_REF] investigated also the uptake of fuel oil PAHs by the halophytic plant Salicornia fragilis and the bioaccumulation of these compounds into shoot tissues in the upper aerial part of the plant. This finding proves that plants are able to take up and to accumulate PAHs in their biomass. This bioaccumulation depends on the time and dose of exposure to fuel oil in the sediment. In this example of halophytic plant, the uptake by roots of PAHs seems to be the main pathway. The particular morphology of Salicornia plants (no real leaf) and the absence of PAHs in control also suggest that PAHs detected are not originated from atmospheric contamination. The different PAH distribution suggests that low molecular weight PAHs, like phenanthrene and pyrene due to their higher solubility, are transported more easily in the phloem than high molecular weight PAHs like benzo(a)pyrene. [START_REF] Fismes | Soil-to-root transfer and translocation of polycyclic aromatic hydrocarbons by vegetables grown on industrial contaminated soils[END_REF] reported that the transport of low molecular weight PAHs from root to aerial parts could be passive and driven by transpiration flux.

Concluding remarks

Halophytes are of significant interest since they naturally occur in environments with excess toxic ions and research findings suggest that they also tolerate other abiotic stresses through cross-tolerance mechanisms that allow them tolerance to several stresses in addition to salt stress tolerance. In this review, we focused on crosstolerance mechanisms in halophytes at the physiological, genomic, transcriptomic, proteomic, and metabolomic levels with an emphasis on their cross-tolerance to salinity and organic pollutants. Their powerful subcellular sequestration of toxic ions and compounds and their high activities of antioxidant enzymes constitute key traits in their high tolerance to both salinity and organic pollutant stresses. However, data about halophyte use in the phytoremediation of organic pollutant-contaminated soils are scarce. Comparative studies between halophyte and glycophyte responses to these pollutants are encouraged. In addition, the effects of optimal salinity levels on halophyte phytoremediation potential of organic pollutants are particularly required.