Amandine Germon

Jean-Paul Laclau

Agnès Robin

Christophe Jourdan
email: christophe.jourdan@cirad.fr

Deep fine roots in forest ecosystems: why dig deeper?

Keywords: deep rooting, root growth, root traits, carbon sequestration, water uptake, nutrient uptake, deep mycorrhizas

While the number of studies dealing with fine root dynamics in deep soils layers (depth > 1 m) has increased sharply recently, the phenology, the morphology, the anatomy and the role of deep fine roots are still poorly known in forest ecosystems. This review summarizes the current knowledge on fine root production, mortality and longevity in deep soil layers, mycorrhizal association with deep roots, and the role of deep fine roots on carbon, water and nutrient cycling in forest ecosystems. Plant species are known to be more deeply rooted in tropical ecosystems than in temperate and boreal ecosystems, but deep-rooted species are common in a wide range of climates. Deep fine roots are highly plastic in response to changes in environmental conditions and soil resources. Recent studies show that functional traits can be different for deep and shallow roots, with a possible functional specialization of deep fine roots to take up nutrients. With higher vessel diameter and larger tracheid, the anatomy of deep fine roots is also oriented toward water acquisition and transport by increasing the hydraulic conductivity. Deep fine roots can have a great impact on the biogeochemical cycles in many forests (in particular in tropical areas where highly weathered soils are commonly very deep), making it possible to take up water and nutrients over dry periods and contributing to store carbon in the soil. The biogeochemical models in forest ecosystems need to consider the specificity of deep root functioning to better predict carbon, water and nutrient cycling as well as net ecosystem productivity.

Introduction

Roots have an essential role in forest ecosystems through the mechanical function of tree anchorage and the physiological function of absorbing and transporting the amounts of water and nutrients needed for plant development [START_REF] Pregitzer | Fine root architecture of nine North American trees[END_REF][START_REF] Mccormack | Impacts of environmental factors on fine root lifespan[END_REF]. The anchorage function is mainly enabled by physical interactions between the roots and the soil. The absorptive function is more complex as it involves biogeochemical interactions between fine roots, soil particles and soil biota, with sometimes symbioses between fine roots and soil bacteria or fungi. Fine roots, commonly considered as root with a diameter lower than 2 mm [START_REF] Mccormack | Redefining fine roots improves understanding of below ground contributions to terrestrial biosphere processes[END_REF], have the ability to adapt to changing environments to facilitate plant development. Fine root activity can modify physical, chemical and biological soil properties, which can have repercussions at the plant level but also at the ecosystem level [START_REF] Mccormack | Redefining fine roots improves understanding of below ground contributions to terrestrial biosphere processes[END_REF]. Indeed, fine roots play a major role in carbon (C) cycling in forest ecosystems, with large C inputs into the soil through root exudates and necromass production, as well as large C returns to the atmosphere through root respiration and decomposition processes [START_REF] Balesdent | Major contribution of roots to soil carbon storage inferred from maize cultivated soils[END_REF][START_REF] Strand | Irreconcilable differences: fine-root life spans and soil carbon persistence[END_REF]. The great plasticity of root systems, both architecturally and functionally, can be strongly influenced by plant phenology, soil properties and climatic conditions [START_REF] Hodge | Plant root growth, architecture and function[END_REF]. Fine root dynamics have been studied quantifying production and mortality [START_REF] Hendrick | The dynamics of fine root length, biomass, and nitrogen content in two northern hardwood ecosystems[END_REF][START_REF] Mccormack | Impacts of environmental factors on fine root lifespan[END_REF], turnover and survivorship [START_REF] Anderson | Multiple risk factors in root survivorship: A 4 year study in Concord grape[END_REF], senescence [START_REF] Huck | Soybean Root Senescence under Drought Stress 1. Minirhizotron observation tubes: methods and applications for measuring rhizosphere dynamics[END_REF] and elongation rates [START_REF] Germon | Unexpected phenology and lifespan of shallow and deep fine roots of walnut trees grown in a silvoarable Mediterranean agroforestry system[END_REF][START_REF] Lambais | Contrasting phenology of Eucalyptus grandis fine roots in upper and very deep soil layers in Brazil[END_REF]. Fine root dynamics are driven by exogenous factors like soil temperature and water content [START_REF] Coll | Fine root seasonal dynamics, plasticity, and mycorrhization in 2 coexisting Mediterranean oaks with contrasting aboveground phenology[END_REF] and endogenous factors like hormone productions [START_REF] Mcadam | Shoot derived abscisic acid promotes root growth[END_REF] and photosynthate and nutrient allocations within the plant [START_REF] Tierney | Fine root turnover in a northern hardwood forest: a direct comparison of the radiocarbon and minirhizotron methods[END_REF][START_REF] Sloan | Contrasting synchrony in root and leaf phenology across multiple sub Arctic plant communities[END_REF]. [START_REF] Binkley | Ecosystems in four dimensions[END_REF] pointed out the critical need to include depth and timescale of ecological processes below the soil surface in a modern conceptualization of forest ecosystems. The full 'critical zone' concept from Earth science should be included in conventional thinking about ecosystems and deep roots can be a key functional element of the Critical Zone [START_REF] Richter | One physical system': Tansley's ecosystem as Earth's critical zone[END_REF][START_REF] Pierret | Understanding deep roots and their functions in ecosystems: an advocacy for more unconventional research[END_REF]. Shrub and tree roots have the ability to explore huge volumes of soil and can be found at great depths in xeric environments [START_REF] Canadell | Maximum rooting depth of vegetation types at the global scale[END_REF][START_REF] Schenk | Rooting depths, lateral root spreads and below ground/above ground allometries of plants in water limited ecosystems[END_REF]. Deep roots improve tree tolerance to drought [START_REF] Mcdowell | Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought?[END_REF][START_REF] Nardini | Rooting depth, water relations and non structural carbohydrate dynamics in three woody angiosperms differentially affected by an extreme summer drought[END_REF] and store C in deep soil layers [START_REF] Balesdent | Atmosphere-soil carbon transfer as a function of soil depth[END_REF].

Understanding the spatial and temporal variability of fine root functioning in deep soil layers is needed to improve our understanding of biosphere-atmosphere interactions [START_REF] Zeng | The role of root distribution for climate simulation over land[END_REF][START_REF] Kleidon | Assessing the role of deep rooted vegetation in the climate system with model simulations: mechanism, comparison to observations and implications for Amazonian deforestation[END_REF], and the accuracy of terrestrial biosphere models [START_REF] Saleska | Amazon forests green-up during 2005 drought[END_REF][START_REF] Christoffersen | Mechanisms of water supply and vegetation demand govern the seasonality and magnitude of evapotranspiration in Amazonia and Cerrado[END_REF]. Even though the importance of deep root systems has been highlighted in several reviews focused on trees [START_REF] Canadell | Maximum rooting depth of vegetation types at the global scale[END_REF][START_REF] Maeght | How to study deep roots-and why it matters[END_REF][START_REF] Pierret | Understanding deep roots and their functions in ecosystems: an advocacy for more unconventional research[END_REF] or on crops [START_REF] Thorup-Kristensen | Digging Deeper for Agricultural Resources, the Value of Deep Rooting[END_REF], the functional significance of deep fine root dynamics, and their contribution to biogeochemical cycles are still poorly documented. [START_REF] Maeght | How to study deep roots-and why it matters[END_REF] proposed to consider as deep roots the roots growing at a depth of more than 1 m. Even though fine root densities are low at great depths, deep roots are likely to play a key role in many processes of plant physiology, community ecology and biogeochemistry in forest ecosystems. Deep roots are found in many biomes where drought periods can occur [START_REF] Nepstad | The role of deep roots in the hydrological and carbon cycles of Amazonian forests and pastures[END_REF][START_REF] Canadell | Maximum rooting depth of vegetation types at the global scale[END_REF][START_REF] Jackson | Belowground consequences of vegetation change and their treatment in models[END_REF][START_REF] Schenk | Rooting depths, lateral root spreads and below ground/above ground allometries of plants in water limited ecosystems[END_REF]. However, the maximum rooting depth reported in the scientific literature is commonly underestimated because most studies did not sample soils down to the root front, which artificially truncated root distributions [START_REF] Freycon | Tree roots can penetrate deeply in African semi-deciduous rain forests: evidence from two common soil types[END_REF]. In a review paper, [START_REF] Stone | On the maximum extent of tree roots[END_REF] reported 37 examples of root systems observed between 10 and 60 m below the soil surface, indicating that the maximum rooting depth can vary considerably with climatic and soil conditions as well as between tree species. In another review paper, [START_REF] Canadell | Maximum rooting depth of vegetation types at the global scale[END_REF] estimated that roots extend in deep horizons down to 9.5 ± 2.4 m in deserts, 7.3 ± 2.8 m in tropical evergreen forest and 15.0 ± 5.4 m in tropical grassland and savannah, with a maximum rooting depth of 68 m reported for Boscia albitrunca trees in Botswana. [START_REF] Schenk | Rooting depths, lateral root spreads and below ground/above ground allometries of plants in water limited ecosystems[END_REF] showed in a meta-analysis that the maximum rooting depth increased for plants growth forms as their size and life span increased, with the highest values for trees and shrubs (Figure 1).

Distributions and dynamics of deep roots are still poorly documented relative to shallow roots [START_REF] Richter | One physical system': Tansley's ecosystem as Earth's critical zone[END_REF][START_REF] Pierret | Understanding deep roots and their functions in ecosystems: an advocacy for more unconventional research[END_REF]. Despite recent technical innovations, the observation of deep roots remains difficult, time-consuming, expensive and requires a combination of methods to obtain reliable results [START_REF] Maeght | How to study deep roots-and why it matters[END_REF]. Direct and indirect techniques can be used for monitoring deep roots depending on the research aim [START_REF] Vogt | Analysis of some direct and indirect methods for estimating root biomass and production of forests at an ecosystem level[END_REF][START_REF] Hendricks | Assessing the patterns and controls of fine root dynamics: an empirical test and methodological review[END_REF]. Deep root functioning at considerable soil depths has been indirectly studied by quantifying water, nitrogen and carbon budgets of the ecosystem [START_REF] Vogt | Analysis of some direct and indirect methods for estimating root biomass and production of forests at an ecosystem level[END_REF]. Direct methods based on soil excavation, trenches, sequential coring, ingrowth cores, and rhizotron observations have been used to monitor root dynamics in situ [START_REF] Maeght | How to study deep roots-and why it matters[END_REF]. Both indirect and direct approaches can have potential biases leading to overestimate or underestimate root growth and root decomposition. There is no consensus on the most effective and reliable method that should be used to quantify fine root dynamics.

Several attempts in plant root architecture and development modelling were performed so far without considering deep rooting patterns. Some models were based on a continuous formalism through partial derivative equations that simulate root apex density and root interaction through time and space [START_REF] Bastian | Modelling in vitro growth of dense root networks[END_REF][START_REF] Dupuy | Root growth models: towards a new generation of continuous approaches[END_REF][START_REF] Bonneu | A minimal continuous model for simulating growth and development of plant root systems[END_REF]. These types of models enabled direct coupling with water transport models [START_REF] Doussan | Modelling of the hydraulic architecture of root systems: an integrated approach to water absorption-model description[END_REF], or nutrient uptake competition models [START_REF] Bonneu | A minimal continuous model for simulating growth and development of plant root systems[END_REF][START_REF] Mayer | Reactive transport modeling in variably saturated media with min3p: Basic model formulation and model enhancements[END_REF][START_REF] Gérard | Modelling the interactions between root system architecture, root functions and reactive transport processes in soil[END_REF]. Other models were based on a discrete and/or random formalism that simulates root architecture, growth, branching and death processes. Some of them were based on mathematical processes such as L-systems [START_REF] Leitner | A dynamic root system growth model based on L-Systems[END_REF] or fractals [START_REF] Van Noordwijk | Proximal root diameter as predictor of total root size for fractal branching models[END_REF][START_REF] Ozier-Lafontaine | Fractal analysis of the root architecture of Gliricidia sepium for the spatial prediction of root branching, size and mass: model development and evaluation in agroforestry[END_REF], or using combinations of the two [START_REF] Shibusawa | Modelling the branching growth fractal pattern of the maize root system[END_REF], others were derived from direct measurements performed on real plants taking into account root-soil interaction functions [START_REF] Diggle | ROOTMAP-a model in three-dimensional coordinates of the growth and structure of fibrous root systems[END_REF]Jourdan and Rey, 1997a, b;[START_REF] Lynch | SimRoot: modelling and visualization of root systems[END_REF][START_REF] Pagès | Root Typ: a generic model to depict and analyse the root system architecture[END_REF][START_REF] Dunbabin | Modelling root-soil interactions using threedimensional models of root growth, architecture and function[END_REF][START_REF] Pagès | Calibration and evaluation of ArchiSimple, a simple model of root system architecture[END_REF][START_REF] Barczi | DigR: a generic model and its open source simulation software to mimic three-dimensional root-system architecture diversity[END_REF], with water and nutrient uptake [START_REF] Wu | SPACSYS: integration of a 3D root architecture component to carbon, nitrogen and water cycling-model description[END_REF][START_REF] Javaux | Use of a three-dimensional detailed modeling approach for predicting root water uptake[END_REF][START_REF] Leitner | A dynamic root system growth model based on L-Systems[END_REF][START_REF] Postma | OpenSimRoot: widening the scope and application of root architectural models[END_REF]. Most of these models, with the exception of some of them (Jourdan and Rey, 1997a, b;[START_REF] Pagès | Calibration and evaluation of ArchiSimple, a simple model of root system architecture[END_REF][START_REF] Barczi | DigR: a generic model and its open source simulation software to mimic three-dimensional root-system architecture diversity[END_REF], are mainly designed for annual and herbaceous plants, with a short lifespan and a limited rooting depth. For perennial crops, shrubs and trees with longer lifespans and deeper rooting strategies, previous models do not consider possible changes in root architecture, diameter, growth, mortality, or functioning processes depending on (great) soil depth. A first attempt was made with the DigR model, which manages parameter values that may change depending on the position along roots of each type, changing with soil depth or not [START_REF] Barczi | DigR: a generic model and its open source simulation software to mimic three-dimensional root-system architecture diversity[END_REF].

Our paper provides an up-to-date literature review on morphological and phenological traits of fine roots along deep soil profiles in forest ecosystems. The production, mortality rates and longevity of deep fine roots, as well as symbiosis with mycorrhizas, their role in water and nutrient uptake and their influence on belowground C sequestration are reviewed. We addressed the following questions: 1) How can environmental conditions, soil resources and symbiotic association along deep soil profiles influence the functioning of fine roots and their main functional traits? 2) Do we need to take into consideration the specificity of deep fine roots to improve current predictions of C, water and nutrient cycling in forest ecosystems? We proposed a conceptual scheme summarizing how root traits vary between the topsoil and deep 132 soil layers (Figure 2). 133

Morphology and anatomy of deep fine roots

The morphology and architecture of root systems vary greatly between plant species but also within individual species [START_REF] Cannon | A tentative classification of root systems[END_REF][START_REF] Nibau | Branching out in new directions: the control of root architecture by lateral root formation[END_REF]. Biogeochemical processes in forest ecosystems are strongly influenced by root architecture [START_REF] Addo-Danso | Fine-root morphological trait variation in tropical forest ecosystems: an evidence synthesis[END_REF], as well as the ability of plants to survive under stressful conditions [START_REF] Penuelas | Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe[END_REF].

Functional traits of fine roots vary with environmental conditions and resource distribution [START_REF] Ostonen | Specific root length as an indicator of environmental change[END_REF]. Fine roots have been classified depending on their main functions and metabolic activity either in absorptive roots involved in the capture and uptake of soil resources that are extremely fine and are the most distal roots, or in roots involved in the transport of water and nutrients that are larger roots, higher in the branching order, and constitute most of the structural part of the root system [START_REF] Mccormack | Redefining fine roots improves understanding of below ground contributions to terrestrial biosphere processes[END_REF]. The high variability of environmental conditions such as soil moisture and temperature or resource (water and nutrients) availability along soil profiles result in contrasting fine root functional traits with soil depth.

Fine roots have been commonly considered as a coherent "pool" of an arbitrary 0-2 mm root diameter class with the same dynamics, turnover rates, respiration costs and the same rates of water and nutrient uptake [START_REF] Persson | Fine-root production, mortality and decomposition in forest ecosystems[END_REF][START_REF] Jackson | A global budget for fine root biomass, surface area, and nutrient contents[END_REF]. However, an increasing number of recent studies suggest that fine root functions can vary depending on the root order of the branching root system [START_REF] Pregitzer | Relationships among root branch order, carbon, and nitrogen in four temperate species[END_REF][START_REF] Majdi | Longevity of mycorrhizal roots depends on branching order and nutrient availability[END_REF][START_REF] Pregitzer | Fine root architecture of nine North American trees[END_REF][START_REF] Guo | Fine root branch orders respond differentially to carbon source-sink manipulations in a longleaf pine forest[END_REF][START_REF] Wang | Fine root architecture, morphology, and biomass of different branch orders of two Chinese temperate tree species[END_REF][START_REF] Hishi | Heterogeneity of individual roots within the fine root architecture: causal links between physiological and ecosystem functions[END_REF][START_REF] Wang | Variations of fine root diameter with root order in Manchurian ash and Dahurian larch plantations[END_REF][START_REF] Pregitzer | Tree root architecture: form and function[END_REF][START_REF] Valenzuela Estrada | Root anatomy, morphology, and longevity among root orders in Vaccinium corymbosum (Ericaceae)[END_REF][START_REF] Comas | Patterns in root trait variation among 25 co-existing North American forest species[END_REF][START_REF] Fan | Slow decomposition of lower order roots: a key mechanism of root carbon and nutrient retention in the soil[END_REF][START_REF] Rewald | A root is a root is a root? Water uptake rates of Citrus root orders[END_REF][START_REF] Beyer | Fine root morphological and functional traits in Fagus sylvatica and Fraxinus excelsior saplings as dependent on species, root order and competition[END_REF][START_REF] Rewald | Root order-based traits of Manchurian walnut & larch and their plasticity under interspecific competition[END_REF][START_REF] Wada | Variation in the morphology of fine roots in Cryptomeria japonica determined by branch order-based classification[END_REF]. These studies have clearly shown that several fine root traits such as diameter (D), length (L), specific root length (SRL), specific root area (SRA), root length density (RLD), branching density but also number of xylem vessels, tissue density, C/N ratios, phenolic, lignin and suberin contents, mycorrhizal colonization and median lifespans varied depending on the root order. The highest fine root order number, the coarsest root diameter, the highest median lifespan, tissue density, xylem vessel number, lignin and suberin content, and the lowest length, branching density, RLD, SRL, SRA, C/N ratios, and mycorrhizal colonization.

Fine root exploration in deep soil layers represents a high metabolic cost for plants [START_REF] Iversen | Digging deeper: fine root responses to rising atmospheric CO2 concentration in forested ecosystems[END_REF], which may influence fine root traits [START_REF] Prieto | Root functional parameters along a land use gradient: evidence of a community level economics spectrum[END_REF]. Specific root length (SRL) and specific root area (SRA) can be affected by soil depth [START_REF] Maurice | Fine root isotropy in Eucalyptus grandis plantations. Towards the prediction of root length densities from root counts on trench walls[END_REF][START_REF] Prieto | Root functional parameters along a land use gradient: evidence of a community level economics spectrum[END_REF][START_REF] Pinheiro | A fast exploration of very deep soil layers by Eucalyptus seedlings and clones in Brazil[END_REF], while other functional traits (concentrations of C, N, cellulose, lignin,…) seem less sensitive [START_REF] Prieto | Root functional parameters along a land use gradient: evidence of a community level economics spectrum[END_REF]. SRL and SRA values are positively correlated with the soil volume in contact with fine roots, which influences the plant capacity to take up limited soil resources [START_REF] Addo-Danso | Fine-root morphological trait variation in tropical forest ecosystems: an evidence synthesis[END_REF]. Changes in specific root length and specific root area with soil depth have been little investigated and the trends are not clear [START_REF] Makita | Very fine roots respond to soil depth: biomass allocation, morphology, and physiology in a broad leaved temperate forest[END_REF][START_REF] Prieto | Root functional parameters along a land use gradient: evidence of a community level economics spectrum[END_REF][START_REF] Pinheiro | A fast exploration of very deep soil layers by Eucalyptus seedlings and clones in Brazil[END_REF]. [START_REF] Pinheiro | A fast exploration of very deep soil layers by Eucalyptus seedlings and clones in Brazil[END_REF] showed a slight increase in SRL and SRA with soil depth down to 13.5 m for 4 genotypes of several Eucalyptus species in Brazil. [START_REF] Maurice | Fine root isotropy in Eucalyptus grandis plantations. Towards the prediction of root length densities from root counts on trench walls[END_REF] also found that SRL increased with soil depth (down to 3 m) in Eucalyptus plantations of different ages. On the contrary, SRL decreased with soil depth down to 1.2 m in Pinus pinaster plantations in France [START_REF] Bakker | Adaptation of fine roots to annual fertilization and irrigation in a 13-year-old Pinus pinaster stand[END_REF]. [START_REF] Adriano | Deep rooting of rainfed and irrigated orange trees in Brazil[END_REF] found no significant changes in SRL with soil depth down to 8 m in Citrus sinensis plantations, but they observed a tendency toward an increase in mean fine root diameters. [START_REF] Gwenzi | Spatial analysis of fine root distribution on a recently constructed ecosystem in a waterlimited environment[END_REF] also found that fine root thickness tended to increase with soil depth (down to 1.4 m) in Acacia rostellifera and Melaleuca nesophila plantations in Western Australia. [START_REF] Prieto | Root functional parameters along a land use gradient: evidence of a community level economics spectrum[END_REF] measured fine root functional traits in 20 plant communities under tropical climate, montane climate, and sub-humid Mediterranean climate.

They showed that fine roots were thicker in deep soil layers (down to 1.6 m) compared to the topsoil. On the contrary, [START_REF] Sochacki | Accuracy of tree root biomass sampling methodologies for carbon mitigation projects[END_REF] observed that root diameter decreased with depth down to 6 m in Eucalyptus globulus plantations in southwest Australia. Mixing tree species can also greatly influence SRL and SLA but studies comparing fine root traits in mixture with the monospecific stands along deep soil profiles are scarce. [START_REF] Germon | Consequences of mixing Acacia mangium and Eucalyptus grandis trees on soil exploration by fine-roots down to a depth of 17 m[END_REF] showed that SRL and SRA values in mixed-species stands of Acacia mangium and Eucalyptus grandis were 110-150% and 34% higher, respectively, than in their monoculture, and the same pattern was observed between the topsoil and a depth of 6 m. Fast-growing species require a rapid and efficient acquisition of resources above and belowground, which generally translate into higher SRA and SRL values compared to slow-growing species, in particular in deep soil layers [START_REF] Ryser | The mysterious root length[END_REF][START_REF] Reich | The world wide 'fast-slow'plant economics spectrum: a traits manifesto[END_REF][START_REF] Jo | Linking above-and belowground resource use strategies for native and invasive species of temperate deciduous forests[END_REF]. High SRL and thin roots are often associated with a better capacity to capture soil resources [START_REF] Hodge | The plastic plant: root responses to heterogeneous supplies of nutrients[END_REF]. Establishing a deep root system with a high area of contact between soil and fine roots (through high fine root density and SRA values) makes it possible to withdraw water from a large soil volume [START_REF] Jackson | Belowground consequences of vegetation change and their treatment in models[END_REF].

Deep roots are mainly oriented toward water acquisition and transport. [START_REF] Mcelrone | Variation in xylem structure and function in stems and roots of trees to 20 m depth[END_REF] showed that deep roots of Juniperus ashei, Bumelia lanuginosa, Quercus fusiformis and Quercus sinuate had higher vessel diameter and larger tracheid than shallow roots in deep soil layers, down to a depth of 18-20 m, with higher hydraulic conductivity (Figure 3). Similar results were found for eucalypt fine roots in Brazil, where xylem vessels were less abundant but with a larger diameter at depth > 10 m than shallow roots of the same diameter class [START_REF] Perron-Gomide | Anatomy of deep and superficial roots of Eucalyptus grandis trees under rainfall reduction[END_REF]. In line with those results, [START_REF] Pate | Hydraulic architecture and xylem structure of the dimorphic root systems of South-West Australian species of Proteaceae[END_REF] showed that roots at a depth of 2 m had larger xylem conduits, higher SRL and SRA values, as well as hydraulic conductivities up to 15 times higher than roots in shallow layers for tree and shrub species of Proteaceae (Banksia prionotes, Banksia ilicifolia and Adenanthos cygnorum) in Australia. Physiological and anatomical adjustments of fine roots in deep soil layers might be an adaptation of plants to maximize their hydraulic efficiency [START_REF] Mcelrone | Aquaporin mediated changes in hydraulic conductivity of deep tree roots accessed via caves[END_REF]. Even those promising results suggesting that very deep roots, despite their scarcity, could have a key role to take up water during drought periods, studies dealing with fine root morphology and anatomy at great depth are still scarce.

Phenology of deep fine roots

Fine roots in deep and shallow soil layers exhibit contrasting phenology with an asynchrony of growth. [START_REF] Maeght | Seasonal patterns of fine root production and turnover in a mature rubber tree (Hevea brasiliensis Müll. Arg.) stand-differentiation with soil depth and implications for soil carbon stocks[END_REF] showed that shallow fine root growth of Hevea brasiliensis was synchronized with rainfall events and ceased during the dry season. On the contrary, fine root growth occurred at the end of the wet season and continued over the dry season at a depth of more than 2.5 m. [START_REF] Germon | Unexpected phenology and lifespan of shallow and deep fine roots of walnut trees grown in a silvoarable Mediterranean agroforestry system[END_REF] also observed an asynchrony between the growth of shallow and deep roots in an agroforestry system with walnut and durum wheat in the south of France. While the growth of tree roots in the topsoil occurred mainly in summer, root growth during the rainy period (in winter) was mainly observed at a depth of more than 2.5 m. The same behavior has been shown in tropical Eucalyptus plantations growing in very deep soils in Brazil. An asynchrony between shallow and deep root growth was observed, with fine root growth occurring in the topsoil over the rainy summer while it peaked deeper than 3 m at the end of the dry season [START_REF] Lambais | Contrasting phenology of Eucalyptus grandis fine roots in upper and very deep soil layers in Brazil[END_REF]. In another Eucalyptus grandis stand, [START_REF] Germon | Consequences of clear-cutting on the production of fine roots, CO2, CH4 and N2O down to the water table in Eucalyptus grandis stands conducted in coppice in a throughfall-exclusion experiment[END_REF] showed a negative correlation between the amount of extractable water in the topsoil and the flushes of fine root growth in very deep soil layers. In those plantations, fine root growth in deep soil layers seems to be related to the overall water demand of the whole tree and controlled by the need to use increasingly deeper water resources when water becomes scarce in the topsoil, which is consistent with modeling studies [START_REF] Christina | Importance of deep water uptake in tropical eucalypt forest[END_REF][START_REF] Christina | Simulating the effects of different potassium and water supply regimes on soil water content and water table depth over a rotation of a tropical Eucalyptus grandis plantation[END_REF]. Vertical growth rates of trees were almost symmetrical aboveand below-ground in Eucalyptus plantations, reaching 10.4 and 19.2 m in height and a maximum rooting depth of 9.2 and 15.8 m at 1.5 and 3.5 years after planting, respectively [START_REF] Christina | Almost symmetrical vertical growth rates above and below ground in one of the world's most productive forests[END_REF]. Other studies using different methodologies (deep drilling, observations on trench walls, injection of 15 N tracer) in the same area confirmed this velocity of root front displacement (Laclau et al., 2013b;[START_REF] Pinheiro | A fast exploration of very deep soil layers by Eucalyptus seedlings and clones in Brazil[END_REF][START_REF] Pinheiro | Distance from the trunk and depth of uptake of labelled nitrate for dominant and suppressed trees in Brazilian Eucalyptus plantations: Consequences for fertilization practices[END_REF].

The growth rates of Eucalyptus roots observed on minirhizotrons by [START_REF] Lambais | Contrasting phenology of Eucalyptus grandis fine roots in upper and very deep soil layers in Brazil[END_REF] are consistent with this downward speed of exploration, with mean elongation rates increasing with soil depth up to a maximum value of 3.6 cm day -1 over a short period below 3 m. In another Eucalyptus grandis stand, minirhizotron observations confirmed higher fine root elongation rates in deep soil layers than in the topsoil (Figure 4), reaching a maximum of 4.3 cm per day over a short period at depths below 5 m (Laclau et al., 2013b;[START_REF] Germon | Unexpected phenology and lifespan of shallow and deep fine roots of walnut trees grown in a silvoarable Mediterranean agroforestry system[END_REF][START_REF] Lambais | Contrasting phenology of Eucalyptus grandis fine roots in upper and very deep soil layers in Brazil[END_REF][START_REF] Germon | Consequences of clear-cutting and drought on fine root dynamics down to 17 m in coppice-managed eucalypt plantations[END_REF].

Increasing root growth rates with soil depth could be an adaptation to drought [START_REF] Annerose | Approche physiologique de l'adaptation à la sécheresse des espèces cultivées pour l'amélioration de la production en zones sèches[END_REF], providing a rapid access to large amounts of water stored in deep soil layers [START_REF] Christina | Importance of deep water uptake in tropical eucalypt forest[END_REF]. This pattern suggests a positive feedback from root growth downward to shoot growth [START_REF] Friend | Carbon allocation to root and shoot systems of woody plants[END_REF]. Environmental conditions and plant growth regulators may control root exploration of deep soil layers [START_REF] López-Bucio | The role of nutrient availability in regulating root architecture[END_REF]. Soil water contents are commonly higher in deep soil layers and variations of temperature are lower than in the topsoil [START_REF] Du | Linking belowground and aboveground phenology in two boreal forests in Northeast China[END_REF][START_REF] Radville | Root phenology in a changing climate[END_REF]. Climatic factors are buffered in deep soil layers, fluctuating less throughout the day and the seasons than in the upper layers, which influences differentially root phenology along deep soil profiles. Changes in fine root phenology with soil depth might also be controlled by other factors. As deep roots are more distant from the shoot than shallow roots, photosynthates might take more time to reach deep roots.

The longevity of fine roots generally increases with soil depth [START_REF] Hendrick | Temporal and depth-related patterns of fine root dynamics in northern hardwood forests[END_REF][START_REF] Baddeley | Influences of root diameter, tree age, soil depth and season on fine root survivorship in Prunus avium[END_REF] but root behavior at depth may be different in some situations. [START_REF] Wells | Changes in the risk of fine root mortality with age: a case study in peach, Prunus persica (Rosaceae)[END_REF] showed that root longevity of Prunus persica significantly increased with soil depth down to 1.6 m. [START_REF] Germon | Unexpected phenology and lifespan of shallow and deep fine roots of walnut trees grown in a silvoarable Mediterranean agroforestry system[END_REF] showed that the mortality of walnut roots was higher in the topsoil that in deep soil layers with a median life span of 167 days within the first soil meter and 208 days in the 2.5-4.7 m layer in an agroforestry system in the south of France. On the contrary, [START_REF] Maeght | Seasonal patterns of fine root production and turnover in a mature rubber tree (Hevea brasiliensis Müll. Arg.) stand-differentiation with soil depth and implications for soil carbon stocks[END_REF] found that root lifespan decreased with soil depth in a rubber tree plantation in Thailand, from 180-250 days between the depth of 1 and 2.5 m to 120 days between 3 and 4.5 m. [START_REF] Lambais | Contrasting phenology of Eucalyptus grandis fine roots in upper and very deep soil layers in Brazil[END_REF] found no significant differences in the lifespan of Eucalyptus fine roots between the topsoil and a depth of 6 m in Brazil. The relationship between depth and fine root longevity is therefore probably dependent on the ecophysiology of tree species as well as on local environmental parameters (e.g., temperature, water content, N availability, CO2 and probably O2 partial pressure) [START_REF] Vogt | Review of root dynamics in forest ecosystems grouped by climate, climatic forest type and species[END_REF]. There are still major uncertainties about the mechanisms controlling fine root phenology in deep soil layers [START_REF] Radville | Root phenology in a changing climate[END_REF].

Fine root biomass and carbon sequestration in deep soil layers

Soil C storage may be strongly underestimated because most studies have focused on the topsoil [START_REF] Harrison | Deep soil horizons: contribution and importance to soil carbon pools and in assessing whole-ecosystem response to management and global change[END_REF][START_REF] Callesen | Carbon storage and nutrient mobilization from soil minerals by deep roots and rhizospheres[END_REF]. While fine roots play a major role in the global carbon cycle, their contribution on soil C storage in very deep soil layers remains little understood [START_REF] Fontaine | Stability of organic carbon in deep soil layers controlled by fresh carbon supply[END_REF][START_REF] Balesdent | Atmosphere-soil carbon transfer as a function of soil depth[END_REF]. Fine root biomass deeper than 1 m is generally a small proportion of the total biomass in forest ecosystems [START_REF] Schenk | Rooting depths, lateral root spreads and below ground/above ground allometries of plants in water limited ecosystems[END_REF][START_REF] Pierret | Understanding deep roots and their functions in ecosystems: an advocacy for more unconventional research[END_REF]. However, the huge C stocks in deep soil layers worldwide suggest that fine root dynamics could have a strong impact, on the long-term [START_REF] Rumpel | Deep soil organic matter-a key but poorly understood component of terrestrial C cycle[END_REF][START_REF] Stahl | Soil carbon stocks after conversion of Amazonian tropical forest to grazed pasture: importance of deep soil layers[END_REF]. Fine roots account for large C inputs to the soil through the release of exudates and root necromass and large amounts of C return to the atmosphere through root respiration and decomposition processes [START_REF] Balesdent | Major contribution of roots to soil carbon storage inferred from maize cultivated soils[END_REF][START_REF] Strand | Irreconcilable differences: fine-root life spans and soil carbon persistence[END_REF]. Estimating fine root production and turnover throughout the entire soil profile is needed to predict more accurately the potential role of forest ecosystems to mitigate climate change.

Even though fine root densities sharply decrease with soil depth, the root biomass at a depth of more than 1 m depth has probably been underestimated. [START_REF] Maeght | Seasonal patterns of fine root production and turnover in a mature rubber tree (Hevea brasiliensis Müll. Arg.) stand-differentiation with soil depth and implications for soil carbon stocks[END_REF] showed that more than 50% of the total fine root biomass was below 1 m depth in a rubber plantation in Thailand. Fine root biomass between the depths of 1.0 and 4.0 m was 5.8 t ha -1 while it amounted to only 4.8 t ha -1 in the 0-1 m soil layer. Soil coring and measurements of fine root intersects on deep soil trenches showed a similar pattern in Brazil for several Eucalyptus species with about 50% of the total fine root length at a depth of more than 1 m, from 1 to 6 years after planting (Laclau et al., 2013b;[START_REF] Pinheiro | A fast exploration of very deep soil layers by Eucalyptus seedlings and clones in Brazil[END_REF]. In an agroforestry system in the south of France, [START_REF] Cardinael | Competition with winter crops induces deeper rooting of walnut trees in a Mediterranean alley cropping agroforestry system[END_REF] showed that 35% of the total fine root intersects of walnut trees on trench walls were deeper than 2 m. At the same site, using the minirhizotron technique, [START_REF] Germon | Unexpected phenology and lifespan of shallow and deep fine roots of walnut trees grown in a silvoarable Mediterranean agroforestry system[END_REF] measured 25% of the total fine root production deeper than 4 m. [START_REF] Germon | Consequences of mixing Acacia mangium and Eucalyptus grandis trees on soil exploration by fine-roots down to a depth of 17 m[END_REF] showed that the proportion of fine root biomass in the 0-1 m layer relative to the total fine root biomass down to 17 m was 31% in Eucalyptus grandis stands, 52% in Acacia mangium stands and 37% in a mixture with 50% of the two species, at 4 years after planting. The proportion of deep roots increases with stand age in young stands. Fine roots below 1 m represented 10 %, 30% and 42% of the total fine root biomass in 2-, 4-and 12-year-old Ziziphus jujube plantations in China [START_REF] Ma | Effects of drip irrigation on deep root distribution, rooting depth, and soil water profile of jujube in a semiarid region[END_REF]. Fine root intersects on trench walls at a depth of more than 4 m represented 5%, 10% and 15% of total fine roots in 1-, 3.5-and 6-year-old Eucalyptus plantation in Brazil (Laclau et al., 2013b). The rooting depth also increased with stand age down to a maximum of 23.2 m at age 22 years in apple orchards in a sub-humid region of China, and roots deeper than 1 m accounted for 49% of the total fine root biomass at 22 years [START_REF] Li | Deep soil water extraction by apple sequesters organic carbon via root biomass rather than altering soil organic carbon content[END_REF]. However, the increase of root biomass in deep soil layers can decrease water availability in sub-humid or arid climates (Figure 5).

A recent meta-analysis of changes in stable carbon isotope signatures across different climatic zones (at 112 sites) showed that the proportion of carbon allocated deeper than 30 cm was much higher than the proportion of root biomass documented in meta-analyses [START_REF] Balesdent | Atmosphere-soil carbon transfer as a function of soil depth[END_REF]. This pattern could be explained by the contribution of root exudates in addition to root mortality as well as by reduced decay rates at depth. Several interacting processes could contribute to slow down decay rates at depth: scattered microbial biomass, stabilization of soil organic matter by minerals, as well as a reduced stimulation of SOC decomposition by the supply of fresh carbon (priming effect) [START_REF] Fontaine | Stability of organic carbon in deep soil layers controlled by fresh carbon supply[END_REF]. Fine root decomposition rates influence the ability of forest ecosystems to store C and act as a sink for CO2. When roots are decomposed, parts of root tissues are incorporated into the soil organic matter [START_REF] Strand | Irreconcilable differences: fine-root life spans and soil carbon persistence[END_REF]. De [START_REF] De Camargo | Soil carbon dynamics in regrowing forest of eastern Amazonia[END_REF] showed that fine roots can be decomposed at least down to a depth of 5 m in eastern Amazon. [START_REF] Nepstad | The role of deep roots in the hydrological and carbon cycles of Amazonian forests and pastures[END_REF] estimated that C stocks deeper than 1 m exceeded SOC in the 0-1 m layer and the above-ground organic C in an Amazonian tropical forest. The deep root system of this Amazonian forest probably released large amounts of organic C into the soil through root exudation, mycorrhizal associations and fine root mortality [START_REF] Nepstad | The role of deep roots in the hydrological and carbon cycles of Amazonian forests and pastures[END_REF]. Moreover, the microbial biomass is much lower in deep soil layers than in the topsoil, which in combination with oxygen limitations could enhance organic C sequestration as a result of low mineralization rates [START_REF] Taylor | Comparison of microbial numbers and enzymatic activities in surface soils and subsoils using various techniques[END_REF][START_REF] Rumpel | Deep soil organic matter-a key but poorly understood component of terrestrial C cycle[END_REF]. Organic C derived from roots is generally more sequestered in the soil than organic C coming from the aboveground litter, which is more affected by physicochemical processes and has a different structural composition [START_REF] Rasse | Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation[END_REF][START_REF] Schmidt | Persistence of soil organic matter as an ecosystem property[END_REF][START_REF] Menichetti | Contribution of roots and amendments to soil carbon accumulation within the soil profile in a long-term field experiment in Sweden[END_REF]. Further studies investigating the relationships between fine root dynamics, microbial communities and soil environment throughout very deep soil profiles in contrasting pedo-climatic conditions are needed to improve the predictions of soil C storage in deep soil layers under climate change.

Mycorrhizal association with deep roots

Symbiotic association with root systems involving mycorrhizal fungi are common in forest ecosystems [START_REF] Högberg | Extramatrical ectomycorrhizal mycelium contributes one third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil[END_REF][START_REF] Churchland | Specificity of plant-microbe interactions in the tree mycorrhizosphere biome and consequences for soil C cycling[END_REF], with beneficial effects both for plants and fungi. Plants provide carbon to mycorrhizal fungi and in exchange, mycorrhizas greatly increase the volume of soil explored, which makes it possible to increase the amounts of water and nutrients taken up in the soil and transferred to the plants [START_REF] Johnson | Mycorrhizas: symbiotic mediators of rhizosphere and ecosystem processes[END_REF]. Symbiotic associations between deep roots and mycorrhizal fungi are poorly documented and until recently, it was commonly believed that mycorrhizal associations were limited to shallow soil layers. Nevertheless, recent researches on microbial communities have highlighted the value of studying deep soil layers and showed unexpected abundant and diverse microbial communities in subsoils [START_REF] Li | Change in deep soil microbial communities due to long-term fertilization[END_REF][START_REF] Gocke | Disentangling interactions between microbial communities and roots in deep subsoil[END_REF][START_REF] Zheng | Occurrence and abundance of ammonia oxidizing archaea and bacteria from the surface to below the water table, in deep soil, and their contributions to nitrification[END_REF][START_REF] Pereira | Digging deeper to study the distribution of mycorrhizal arbuscular fungi along the soil profile in pure and mixed Eucalyptus grandis and Acacia mangium plantations[END_REF].

Most of research about arbuscular mycorrhizal (AM) fungi depending on soil depth has been carried out in agricultural systems down to a maximum depth of 1 meter. The results were mainly focused on the abundance and diversity of AM spores, with few studies taking into account AM fungi root colonization [START_REF] Kabir | Vertical distribution of arbuscular mycorrhizal fungi under corn (Zea mays L.) in no-till and conventional tillage systems[END_REF][START_REF] Oehl | Community structure of arbuscular mycorrhizal fungi at different soil depths in extensively and intensively managed agroecosystems[END_REF][START_REF] Cuenca | Seasonal variation and distribution at different soil depths of arbuscular mycorrhizal fungi spores in a tropical sclerophyllous shrubland[END_REF][START_REF] Yang | Geographical and plant genotype effects on the formation of arbuscular mycorrhiza in Avena sativa and Avena nuda at different soil depths[END_REF][START_REF] Taniguchi | Colonization and community structure of rootassociated microorganisms of Sabina vulgaris with soil depth in a semiarid desert ecosystem with shallow groundwater[END_REF][START_REF] Shukla | Soil depth: an overriding factor for distribution of arbuscular mycorrhizal fungi[END_REF][START_REF] Becerra | Arbuscular mycorrhizal fungi in saline soils: Vertical distribution at different soil depth[END_REF][START_REF] Gai | Infectivity and community composition of arbuscular mycorrhizal fungi from different soil depths in intensively managed agricultural ecosystems[END_REF]. Nevertheless, some older studies report observations of mycorrhizal associations more deeply, down to a depth of 4 m [START_REF] Virginia | Depth of root symbiont occurrence in soil[END_REF][START_REF] Zajicek | The influence of soil depth on mycorrhizal colonization of forbs in the tallgrass prairie[END_REF]. In tropical agroforests with Faidherbia albida trees, [START_REF] Dalpé | Glomales species associated with surface and deep rhizosphere of Faidherbia albida in Senegal[END_REF] showed that AM propagules were viable in cores taken down to a depth of 34 m, which highlights the importance of improving our knowledge of deep mycorrhizal symbioses. A recent survey showed the presence of AMF fungal spores in deep soil layers down to a depth of 8 m in pure and mixedspecies plantations of Eucalyptus grandis and Acacia mangium in Brazil [START_REF] Pereira | Digging deeper to study the distribution of mycorrhizal arbuscular fungi along the soil profile in pure and mixed Eucalyptus grandis and Acacia mangium plantations[END_REF], with root colonization rates between 6 and 25% for the 0-100 cm soil, and a decrease to about 10% below 1 meter and 5% -6% below 3 m. This weak AMF colonization could be partly due to the age of the trees (over 1 year old) because the symbiosis with AM fungi is commonly known to be substituted gradually by ectomycorrhizal fungi in trees plantations [START_REF] Read | Mycorrhizas in ecosystems[END_REF][START_REF] Bellei | Mycorrhizal succession in young Eucalyptus viminalis plantations in Santa Catarina (southern Brazil)[END_REF][START_REF] Boerner | Spatial patterns of mycorrhizal infectiveness of soils long a successional chronosequence[END_REF].

A vertical structuration of ectomycorrhizal (ECM) symbioses has been shown in numerous studies, with different ECM fungal communities between organic and mineral soil layers [START_REF] Moyersoen | Spatial distribution of ectomycorrhizas and arbuscular mycorrhizas in Korup National Park rain forest, Cameroon, in relation to edaphic parameters[END_REF][START_REF] Dickie | Vertical niche differentiation of ectomycorrhizal hyphae in soil as shown by T RFLP analysis[END_REF][START_REF] Rosling | Vertical distribution of ectomycorrhizal fungal taxa in a podzol soil profile[END_REF][START_REF] Genney | Fine scale distribution of pine ectomycorrhizas and their extramatrical mycelium[END_REF].

Unfortunately, most of the studies do not exceed the depth of 2 m [START_REF] Bakker | Fine root distribution of trees and understory in mature stands of maritime pine (Pinus pinaster) on dry and humid sites[END_REF][START_REF] Clemmensen | Carbon sequestration is related to mycorrhizal fungal community shifts during long term succession in boreal forests[END_REF][START_REF] Rocha | Forest residue maintenance increased the wood productivity of a Eucalyptus plantation over two short rotations[END_REF]. ECM root tips have been observed down to a depth of 4 m in bedrock fissures [START_REF] Bornyasz | Ectomycorrhizae in a soil-weathered granitic bedrock regolith: linking matrix resources to plants[END_REF][START_REF] Querejeta | Hydraulic lift may buffer rhizosphere hyphae against the negative effects of severe soil drying in a California Oak savanna[END_REF]. As for AM fungi, the presence of ECM fungi propagules has been shown in very deep soil layers, down to 10 m [START_REF] Santana | Eucalypt as trap plant to capture associative fungi in soil samples from great depth[END_REF]. [START_REF] Robin | How deep can ectomycorrhizas go? A case study on Pisolithus down to 4 meters in a Brazilian eucalypt plantation[END_REF] demonstrated for the first time using molecular sequencing that ECM symbioses occurred with Eucalyptus grandis roots at a depth of 4 m in Brazil (Figure 6). The intraspecific diversity of the fungus Pisolithus in this study was strongly impacted by the depth, suggesting the presence of a reservoir of biodiversity associated with the deepest roots.

The occurrence of mycorrhizal associations (with both AM and ECM fungi) in deep soil layers can contribute to increasing the volume of soil explored by scarce roots, which can greatly enhance water and nutrient capture during drought periods [START_REF] Lehto | Ectomycorrhizas and water relations of trees: a review[END_REF][START_REF] Begum | Role of Arbuscular Mycorrhizal Fungi in Plant Growth Regulation: Implications in Abiotic Stress Tolerance[END_REF]. Moreover, mycorrhizal fungi have a strong impact on carbon cycling [START_REF] Rillig | Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils[END_REF][START_REF] Tedersoo | Mycorrhizal types differ in ecophysiology and alter plant nutrition and soil processes[END_REF], with possible consequences on C sequestration in deep soil layers. For example, the symbiosis with ECM fungi increases the lifespan of fine roots [START_REF] King | Below ground carbon input to soil is controlled by nutrient availability and fine root dynamics in loblolly pine[END_REF][START_REF] Guo | Influence of root zone nitrogen management and a summer catch crop on cucumber yield and soil mineral nitrogen dynamics in intensive production systems[END_REF][START_REF] Mccormack | Impacts of environmental factors on fine root lifespan[END_REF][START_REF] Lambais | Contrasting phenology of Eucalyptus grandis fine roots in upper and very deep soil layers in Brazil[END_REF], and the fungal biomass of both AM and ECM fungi can represent a significant C sink in forest ecosystems [START_REF] Rillig | Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils[END_REF][START_REF] Wilson | Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long term field experiments[END_REF][START_REF] Cairney | Extramatrical mycelia of ectomycorrhizal fungi as moderators of carbon dynamics in forest soil[END_REF][START_REF] Clemmensen | Carbon sequestration is related to mycorrhizal fungal community shifts during long term succession in boreal forests[END_REF]. The turnover of fungal biomass in deep soil layers can be lower than in the topsoil as a result of the low abundance of predatory organisms [START_REF] Fernandez | The decomposition of ectomycorrhizal fungal necromass[END_REF], which suggests that the contribution of fungi to C storage in the subsoil could be important.

There are serious technical and methodological difficulties to study mycorrhizal associations with deep roots, which explains that mycorrhizal symbioses in deep soil layers are still very little documented. The difficulty to sample a sufficient weight of mycorrhizal fungi in undisturbed soil at large depth is a major challenge. Some authors speculated that they did not sample deeply enough to determine the limits of ECM fine roots [START_REF] Bakker | Fine root distribution of trees and understory in mature stands of maritime pine (Pinus pinaster) on dry and humid sites[END_REF]. The minirhizotron method is well suited for root observations and has already been used to study the dynamics of ECM fungi [START_REF] Allen | In situ high frequency observations of mycorrhizas[END_REF][START_REF] Mccormack | Production dynamics of Cenococcum geophilum ectomycorrhizas in response to long-term elevated CO2 and N fertilization[END_REF]. A recent study using minirhizotrons showed typical ECM structures associated with deep roots down to 6 m in a Brazilian eucalypt plantation [START_REF] Lambais | Contrasting phenology of Eucalyptus grandis fine roots in upper and very deep soil layers in Brazil[END_REF]. However, the method itself could affect mycorrhization, especially in deep soil layers (transport of spores, modification of the environment near the tube…) and might create a favorable environment for fungi growth. These interesting observations, despite their limitations, suggest the urgent need to combine several methods making it possible to study in situ simultaneously the dynamics of roots and mycorrhizal symbioses. We also need to go beyond diversity approaches and to study more the functional aspects of these symbioses. Although a growing body of evidence suggests that biological activity in deep soil layers is a major scientific lock poorly investigated and important to resolve to improve our understanding of the biogeochemistry of forest ecosystems, it remains a major methodological and technical challenge [START_REF] Gocke | Disentangling interactions between microbial communities and roots in deep subsoil[END_REF].

Water and nutrient uptake in deep soil layers

The role of deep roots on water uptake by trees is well documented [START_REF] Phillips | A belowground perspective on the drought sensitivity of forests: Towards improved understanding and simulation[END_REF].

Deep roots are essential to sustain high tree transpiration over dry seasons, which strongly influences the Amazonian climate [START_REF] Kleidon | Assessing the role of deep rooted vegetation in the climate system with model simulations: mechanism, comparison to observations and implications for Amazonian deforestation[END_REF][START_REF] Saleska | Amazon forests green-up during 2005 drought[END_REF]. Soil water content monitoring throughout soil profiles as well as studies using hydrogen and oxygen isotopes at specific dates make it possible to estimate at which depth water is taken up by tree roots [START_REF] Guderle | Using measured soil water contents to estimate evapotranspiration and root water uptake profiles-a comparative study[END_REF][START_REF] Beyer | A deuterium-based labeling technique for the investigation of rooting depths, water uptake dynamics and unsaturated zone water transport in semiarid environments[END_REF][START_REF] Koeniger | Review on soil water isotope based groundwater recharge estimations[END_REF][START_REF] Trogisch | Spatio-temporal water uptake patterns of tree saplings are not altered by interspecific interaction in the early stage of a subtropical forest[END_REF][START_REF] Beyer | Examination of deep root water uptake using anomalies of soil water stable isotopes, depth-controlled isotopic labeling and mixing models[END_REF]. [START_REF] Stahl | Depth of soil water uptake by tropical rainforest trees during dry periods: does tree dimension matter?[END_REF] showed that 46% of the trees were extracting water at a depth of at least 1.2 m in a tropical rainforest. Trees have developed efficient strategies for the acquisition of water resources in deep soil layers, which can also help sustain shallow root functioning during drought through hydraulic redistribution [START_REF] Burgess | The redistribution of soil water by tree root systems[END_REF][START_REF] Domec | Native root xylem embolism and stomatal closure in stands of Douglas fir and ponderosa pine: mitigation by hydraulic redistribution[END_REF][START_REF] Bleby | Water uptake and hydraulic redistribution across large woody root systems to 20 m depth[END_REF]. [START_REF] Burgess | Tree roots: conduits for deep recharge of soil water[END_REF] have demonstrated that Eucalyptus species have the capacity to redistribute water from wetter deep layers into shallow soil layers through vertical and horizontal roots. Hydraulic redistribution has now been demonstrated for many tree species and modeling approaches showed that this process can strongly influence the evapotranspiration and the net carbon exchange of the ecosystem [START_REF] Domec | Hydraulic redistribution of soil water by roots affects whole stand evapotranspiration and net ecosystem carbon exchange[END_REF]. Water uptake in very deep soil layers is highly dynamic in response to changes in atmospheric demand and soil water contents in the upper layers [START_REF] Christina | Importance of deep water uptake in tropical eucalypt forest[END_REF]. A modeling approach showed that the occurrence of rainfall events, changing from a week to another, had a strong impact on which depth water uptake occurs (Figure 7). It has also been shown that tree nutrition can greatly influence water withdrawal by roots in very deep soil layers [START_REF] Christina | Simulating the effects of different potassium and water supply regimes on soil water content and water table depth over a rotation of a tropical Eucalyptus grandis plantation[END_REF]. Recently, [START_REF] Li | Deep soil water extraction by apple sequesters organic carbon via root biomass rather than altering soil organic carbon content[END_REF] showed that the extraction of water in deep soil layers by the root system of apple stands between 15 and 22 years of age was mainly occurring at depths below 12 m in a sub-humid region of China.

They also suggested that roots in the 1-12 m layer remained alive to transport the water taken up below 12 m as they were probably unable to extract additional water in the upper 12 m.

The access of roots to a very deep water table can dramatically change tree functioning and the net C exchanges in forest ecosystems [START_REF] Roupsard | Reverse phenology and dry season water uptake by Faidherbia albida (Del.) A. Chev. in an agroforestry parkland of Sudanese west Africa[END_REF][START_REF] Carter | Plasticity in the Huber value contributes to homeostasis in leaf water relations of a mallee Eucalypt with variation to groundwater depth[END_REF][START_REF] Zolfaghar | Transpiration of Eucalyptus woodlands across a natural gradient of depth-to-groundwater[END_REF]. To improve soil-vegetation-atmosphere transfer models in tropical forest ecosystems, we need a better understanding of the potential of very deep roots to withdraw water stored in the subsoil [START_REF] Akkermans | Validation and comparison of two soil vegetation atmosphere transfer models for tropical Africa[END_REF].

The contribution of deep roots to supply tree requirements has been much less studied for nutrients than for water. A safety net of tree roots reducing the losses of nutrients by deep leaching is well known in agroforestry systems [START_REF] Allen | Safety-net role of tree roots: evidence from a pecan (Carya illinoensis K. Koch)-cotton (Gossypium hirsutum L.) alley cropping system in the southern United States[END_REF]. Monitoring soil solution chemistry throughout very deep soil profiles showed that Eucalyptus roots take up most of the nutrients dissolved in the gravitational solutions before leaching at great depth [START_REF] Laclau | Biogeochemical cycles of nutrients in tropical Eucalyptus plantations: main features shown by intensive monitoring in Congo and Brazil[END_REF][START_REF] Mareschal | Nutrient leaching and deep drainage under Eucalyptus plantations managed in short rotations after afforestation of an African savanna: two 7-year time series[END_REF], with a very quick uptake by a root mat during the decomposition processes in the forest floor [START_REF] Laclau | The function of the superficial root mat in the biogeochemical cycles of nutrients in Congolese Eucalyptus plantations[END_REF]. Sr and Ca cycling were also very conservative in a tropical rainforest in French Guyana, with very little Sr contribution from deep soil layers for tree species differing by their rooting depth, which supported the theory that Sr and Ca uptake and cycling are mostly superficial in tropical rainforests [START_REF] Poszwa | Do deep tree roots provide nutrients to the tropical rainforest?[END_REF]. Recent studies using markers suggest that a functional specialization of fine roots could also influence their ability to take up nutrients depending on the depth. Comparing oak, European beech and Norway spruce monocultures in Denmark, [START_REF] Göransson | Estimating the relative nutrient uptake from different soil depths in Quercus robur, Fagus sylvatica and Picea abies[END_REF] showed that the distribution of roots and mycelia was not a reliable indicator of nutrient uptake capacity by tree roots at different soil depths. The uptake capacity from deep soil layers was higher than expected from the root distribution for most of the markers compared with the topsoil, which might be explained by an overlap of the uptake zones around the roots and mycorrhizal hyphae in the topsoil [START_REF] Göransson | Estimating the relative nutrient uptake from different soil depths in Quercus robur, Fagus sylvatica and Picea abies[END_REF]. Injection of 15 NO3 -, Rb + (K + analog) and Sr 2+ (Ca 2+ analog) markers at the depths of 10, 50, 150 and 300 cm in Brazilian Ferralsol soils also suggested a functional specialization of fine roots with a higher capacity to take up cations in deep soil layers, in 2-and 6-year-old Eucalyptus grandis plantations [START_REF] Da Silva | Functional specialization of Eucalyptus fine roots: contrasting potential uptake rates for nitrogen, potassium and calcium tracers at varying soil depths[END_REF][START_REF] Bordron | Fertilization increases the functional specialization of fine roots in deep soil layers for young Eucalyptus grandis trees[END_REF]. Trees exhibit a great flexibility in their capability to adjust their root development and the uptake of soil resource in the layers where they are available [START_REF] Jackson | Rapid physiological adjustment of roots to localized soil enrichment[END_REF][START_REF] Hutchings | Foraging in plants: the role of morphological plasticity in resource acquisition[END_REF][START_REF] Robinson | Resource capture by localized root proliferation: why do plants bother?[END_REF]. A recent study in a rainfall exclusion experiment showed that eucalypt fine root functioning can be considerably altered as a response to drought in deep soil profiles [START_REF] Pradier | Rainfall reduction impacts rhizosphere biogeochemistry in eucalypts grown in a deep Ferralsol in Brazil[END_REF].

Whereas H3O + and exchangeable K + concentrations were not influenced by the drought treatment (37% of rainfall exclusion) in the bulk soil, they were significantly higher in the rhizosphere than in the bulk soil in plots with reduced rainfall, notably at a depth of more than 2 m. This study suggested that root-induced weathering of K-bearing minerals contributed to increasing rhizosphere acidification and K bioavailability at great depth.

Influence of soil environment and resource availability

Deep roots are highly plastic in response to heterogeneous resource distributions [START_REF] Hodge | Plant root growth, architecture and function[END_REF]. Plants have the ability to adapt their root system to changing soil water contents, nutrient availabilities, soil physical properties, and soil atmosphere composition. The variability of environmental factors affecting root growth are buffered in deep soil layers compared to the topsoil [START_REF] Voroney | The soil habitat[END_REF]. Changes in fine root structure, architecture, and production with soil depth can be influenced by the spatial heterogeneity of soil resources and soil microclimate [START_REF] Addo-Danso | Fine-root morphological trait variation in tropical forest ecosystems: an evidence synthesis[END_REF]. Root ingrowth bags installed down to a depth of 6 m in mixed-species plantations of Acacia mangium and Eucalyptus grandis showed a remarkable capacity of very deep roots to explore resource-rich soil patches despite their low density in the soil [START_REF] Germon | Consequences of mixing Acacia mangium and Eucalyptus grandis trees on soil exploration by fine-roots down to a depth of 17 m[END_REF]. A high plasticity of fine roots has also been shown through a vertical segregation of fine roots in mixed-species forests making it possible to explore more intensively deep soil profiles than monospecific stands [START_REF] Schenk | Spatial root segregation: are plants territorial? In[END_REF]. Some studies in agroforestry systems and forest ecosystems suggest that fine roots of the weakest competitor can be partially excluded from soil horizons where the resources limiting tree growth are concentrated [START_REF] Schmid | Root distribution of Norway spruce in monospecific and mixed stands on different soils[END_REF][START_REF] Mulia | Unusual fine root distributions of two deciduous tree species in southern France: What consequences for modelling of tree root dynamics?[END_REF]Laclau et al., 2013a).

Plant species use a large range of rooting patterns to cope with periodic drought, from "drought tolerant strategies" with fine roots surviving in periodically dry soil to "drought avoiding strategies" shedding fine roots from dry soil horizons while rapidly developing roots in moister areas [START_REF] Brunner | How tree roots respond to drought[END_REF][START_REF] Vries | Grassland species root response to drought: consequences for soil carbon and nitrogen availability[END_REF][START_REF] Bristiel | Coping with drought: root trait variability within the perennial grass Dactylis glomerata captures a trade-off between dehydration avoidance and dehydration tolerance[END_REF]. Soil water content is a major driver of root growth and production in deep soil layers. [START_REF] Adriano | Deep rooting of rainfed and irrigated orange trees in Brazil[END_REF] showed that fine root mass of Citrus sinensis were higher in deep soil layers (between the depths of 5 m and 8 m) for rainfed trees than for irrigated trees. However, changes in SRL and SRA along soil profiles were unclear in those Citrus plantations, whatever the water supply regime. [START_REF] Schenk | Rooting depths, lateral root spreads and below ground/above ground allometries of plants in water limited ecosystems[END_REF] showed that the maximum rooting depth in tropical ecosystems was positively correlated with the length of the dry season and negatively correlated with the annual precipitation. [START_REF] Wang | Root tip morphology, anatomy, chemistry and potential hydraulic conductivity vary with soil depth in three temperate hardwood species[END_REF] also found a highly negative correlation between root mass and soil water content down to a depth of 21 m in grasslands and shrublands in China. Drought periods commonly increase the proportion of fine roots in deep soil layers as well as specific root areas [START_REF] Markesteijn | Seedling root morphology and biomass allocation of 62 tropical tree species in relation to drought and shade tolerance[END_REF][START_REF] Ma | Evolutionary history resolves global organization of root functional traits[END_REF][START_REF] Zhou | Drought induced changes in root biomass largely result from altered root morphological traits: evidence from a synthesis of global field trials[END_REF]. In a survey of 62 tropical tree species, [START_REF] Markesteijn | Seedling root morphology and biomass allocation of 62 tropical tree species in relation to drought and shade tolerance[END_REF] showed that trees increase the belowground biomass and the proportion of deep roots in response to dry conditions. [START_REF] Germon | Consequences of clear-cutting and drought on fine root dynamics down to 17 m in coppice-managed eucalypt plantations[END_REF] showed an increase in SRL and SRA down to a depth of 16 m in response to throughfall exclusion for Eucalyptus trees in Brazil.

Fine root dynamics can also be influenced by the depth of the water table. [START_REF] Li | Optimal root system strategies for desert phreatophytic seedlings in the search for groundwater[END_REF] showed that the displacement of the root front of Alhagi sparsifolia was 0.66 cm d -1 when the water table was at a depth of 0.8 m and 1.5 cm d -1 when the water table was at a depth of 2.2 m. [START_REF] Canham | Dynamics of phreatophyte root growth relative to a seasonally fluctuating water table in a Mediterranean-type environment[END_REF] showed a seasonal distribution of fine root biomass in deep soil layers in response to the fluctuations of the depth of the water table in southwest Australia.

Although the physiological mechanisms remain little understood, some studies investigating the relationships between changes in water table depth and fine root dynamics suggest that an increase in water table depth could promote an increase in root elongation rates downwards [START_REF] Stave | Seedling growth of Acacia tortilis and Faidherbia albida in response to simulated groundwater tables[END_REF][START_REF] Canham | The response of Banksia roots to change in water table level in a Mediterranean-type environment[END_REF].

The influence of soil texture on fine root distributions remains unclear. Fine root distributions were shallower in sandy soils than in clayey soils in a tropical evergreen forest [START_REF] Schenk | Rooting depths, lateral root spreads and below ground/above ground allometries of plants in water limited ecosystems[END_REF]. However, roots of Haloxyolon ammodendron reached a depth of 10 m in a sandy soil and only 3 m in a heavy soil [START_REF] Xu | Rooting depth and leaf hydraulic conductance in the xeric tree Haloxyolon ammodendron growing at sites of contrasting soil texture[END_REF]. Comparing root distributions for Entandrophragma cylindricum Sprague (Meliaceae) in African semi-deciduous rainforests, [START_REF] Freycon | Tree roots can penetrate deeply in African semi-deciduous rain forests: evidence from two common soil types[END_REF] showed that fine root densities down to a depth of 6 m were lower in a coarse-textured Arenosol soil than in a fine-textured Ferralsol soil. The same pattern was showed by Laclau et al. (2013b) comparing fine root densities down to a depth of 10 m in sandy and clayey Ferralsol soils in the same Eucalyptus stand. Similarly, [START_REF] Robinson | Soil water depletion by Eucalyptus spp. integrated into dryland agricultural systems[END_REF] in Australia reported that eucalypt species can reach 8-10 m deep and withdraw deep soil water (Figure 8) despite a high bulk density (up to 2.0 g cm -3 ) in clayey subsoil. [START_REF] Canadell | Maximum rooting depth of vegetation types at the global scale[END_REF] cited some examples of roots reaching great depths in rocky soils, using cracks and macropores at the vicinity of rocks to grow with low mechanical constraints.

Nutrient availability can also influence fine root traits throughout deep soil profiles. Studying fine roots and nutrient distributions down to a depth of 10 m in five semi-arid and arid forests in the southwestern USA, [START_REF] Mcculley | Nutrient uptake as a contributing explanation for deep rooting in arid and semi-arid ecosystems[END_REF] showed morphological and physiological adjustments of fine roots in response to nutrient availability. The fate of tracers injected at various depth in a Ferralsol soil suggested that NPK fertilization increased the capacity of Eucalyptus grandis fine roots to take up nutrients down to a depth of 3 m [START_REF] Bordron | Fertilization increases the functional specialization of fine roots in deep soil layers for young Eucalyptus grandis trees[END_REF]. Moreover, NPK fertilization increased fine root density, specific root length and specific root area throughout the soil profile. However, N fertilization did not influence the fine root biomass down to a depth of 3 m in another E. grandis stand at the same site in Brazil [START_REF] Jourdan | Fine root production and turnover in Brazilian Eucalyptus plantations under contrasting nitrogen fertilization regimes[END_REF]. The relationships between nutrient availability throughout deep soil profiles, fine root dynamics and fine root traits are difficult to disentangle from changes in environmental conditions and further studies are needed to gain insight into the specific effect of soil nutrient contents.

Even though the consequences of elevated CO2 concentrations in the atmosphere on plant growth has been studied in many FACE experiments, fine root responses are still little documented for trees. In a review paper, [START_REF] Iversen | Digging deeper: fine root responses to rising atmospheric CO2 concentration in forested ecosystems[END_REF] showed that high atmospheric CO2 concentrations tend to increase root depth in forest ecosystems. However, most of the studies dealing with fine roots in FACE experiments were carried out in the upper soil layers. Fine root traits influence tree functioning [START_REF] Prieto | Root functional parameters along a land use gradient: evidence of a community level economics spectrum[END_REF][START_REF] Addo-Danso | Fine-root morphological trait variation in tropical forest ecosystems: an evidence synthesis[END_REF] but the scarcity of information on the influence of the rise of atmospheric CO2 concentrations on fine roots traits at depths of more than 30 cm limits our understanding of the response of forests to climate change on huge areas. Studies dealing with the influence of elevated CO2 concentrations on root distributions and fine root traits in deep soil layers are therefore urgently needed for tree species.

Modeling approaches to gain insight into the functioning of deep fine roots

Modeling architecture development and dynamics of the deep fine roots is hindered by the limited data available in the literature, yet necessary to parametrize and evaluate the models.

Root number, root diameter, root volume, and root radial distances are the main parameters of root system biomechanics [START_REF] Nicoll | Adaptive growth of tree root systems in response to wind action and site conditions[END_REF][START_REF] Dorval | Anchorage failure of young trees in sandy soils is prevented by a rigid central part of the root system with various designs[END_REF], varying considerably with soil layers. Soil depth strongly influences the root system architecture due to the heterogeneity of its environment. Root architectural models could simulate accurately spatial and temporal dynamics through a simulation of the root system in 3D. Integrating a vertically discretized soil into a model is particularly important as shallow and deep roots present different spatial and temporal dynamics. Model parametrization needs to consider shallow and deep-rooted systems behaving differently according to the environmental factors and soil conditions. These models can be parametrized according to the definition of root types (e.g. RootTyp from [START_REF] Pagès | Root Typ: a generic model to depict and analyse the root system architecture[END_REF]; or DigR (Figure 9) from [START_REF] Barczi | DigR: a generic model and its open source simulation software to mimic three-dimensional root-system architecture diversity[END_REF]) or by branching order (e.g. OpenSimRoot from [START_REF] Postma | OpenSimRoot: widening the scope and application of root architectural models[END_REF]) or through parametric Lsystem modeling [START_REF] Leitner | A dynamic root system growth model based on L-Systems[END_REF], which also might vary with soil layers. Such a model without discretized processes by soil layers is not capable to simulate accurately the impact of environmental conditions and soil resources on root development. Models devoted to simulating water and nutrient uptake dynamics need to integrate the functional specialization of deep roots and root growth plasticity in response to environmental conditions, in particular in deep soil layers. However, most root functioning rules are still not completely understood, especially at great depth as a result of the difficulty of measuring those processes in situ.

Therefore, model calibration must cope with this knowledge and experimental limits.

Architectural models can also be coupled with models simulating nutrient uptake [START_REF] Mayer | A numerical model for multicomponent reactive transport in variably saturated porous media[END_REF][START_REF] Bonneu | A minimal continuous model for simulating growth and development of plant root systems[END_REF][START_REF] Mayer | Reactive transport modeling in variably saturated media with min3p: Basic model formulation and model enhancements[END_REF], water transport [START_REF] Doussan | Modelling of the hydraulic architecture of root systems: an integrated approach to water absorption-model description[END_REF], rhizospheric processes [START_REF] Kim | A mathematical model for pH patterns in the rhizospheres of growth zones[END_REF], or even reactive transport models [START_REF] Mayer | A numerical model for multicomponent reactive transport in variably saturated porous media[END_REF][START_REF] Mayer | Reactive transport modeling in variably saturated media with min3p: Basic model formulation and model enhancements[END_REF][START_REF] Gérard | Modelling the interactions between root system architecture, root functions and reactive transport processes in soil[END_REF]. Nevertheless, it can be convenient to simulate accurately the overall architecture and any specialized functions of deep roots compared to shallow roots. Furthermore, deep roots have a strong influence on deep carbon stocks, which accounts for a significant amount of carbon [START_REF] Jobbágy | Groundwater use and salinization with grassland afforestation[END_REF] and can be partially renewed at the 10-year scale [START_REF] Baisden | Bomb 14 C enrichment indicates decadal C pool in deep soil?[END_REF][START_REF] Koarashi | Dynamics of decadally cycling carbon in subsurface soils[END_REF]. Models predicting soil organic carbon stocks through a single soil layer modeling approach [START_REF] Hansen | Simulation of nitrogen dynamics and biomass production in winter wheat using the Danish simulation model DAISY[END_REF][START_REF] Sallih | Modelling of soil carbon forms after organic amendment under controlled conditions[END_REF][START_REF] Petersen | CN-SIM-a model for the turnover of soil organic matter. I. Long-term carbon and radiocarbon development[END_REF][START_REF] Pansu | Modeling organic transformations by microorganisms of soils in six contrasting ecosystems: Validation of the MOMOS model[END_REF][START_REF] Oelbermann | An evaluation of the century model to predict soil organic carbon: examples from Costa Rica and Canada[END_REF] are therefore not considering adequately deep roots that play an active role in carbon cycling. In recent years, an awareness of the importance of deep carbon stocks by the modeling community has led to the development of different discretized models depending on the soil depth [START_REF] Braakhekke | SOMPROF: A vertically explicit soil organic matter model[END_REF][START_REF] Braakhekke | Modeling the vertical soil organic matter profile using Bayesian parameter estimation[END_REF][START_REF] Guenet | The relative importance of decomposition and transport mechanisms in accounting for soil organic carbon profiles[END_REF][START_REF] Taghizadeh-Toosi | C-TOOL: A simple model for simulating whole-profile carbon storage in temperate agricultural soils[END_REF]. However, modeling accurately deep root dynamics and their active role in C fluxes in forest ecosystems, as well as nutrient and water uptake throughout tree growth remains a major challenge for the next decades.

Conclusion

Deep roots are a major component of forest ecosystems that can greatly influence the biogeochemistry of the Critical Zone. Their anatomical, morphological and functional root traits may be different from those of shallow roots (Figure 2

Figure 1 .

 1 Figure 1. Maximum rooting depths of plant growth forms. Geometric means marked by different letters were significantly different according to one-way ANOVAs. Source: Schenk and Jackson (2002), used by permission.

Figure 2 .

 2 Figure 2. Conceptual scheme of root trait variations between the topsoil and deep soil layers. The larger the size of the text, the higher the value of the root trait considered. The main tendencies in the literature (indicated in Appendix 1) are shown here, but the behavior of certain plant species can be different. RLD for root length density, SRL for specific root length, SRA for specific root density and RTD for root tissue density. Images of root anatomy and ectomycorrhizal symbiosis where adapted from Perron-Gomide et al. (Com. Pers. 2020) and Robin et al. (2019), respectively.

Figure 3 .

 3 Figure 3. Scanning electron micrographs of shallow roots (top row) and deep roots (bottom row, depth of 18-20 m) for Quercus fusiformis, Juniperus ashei, Quercus sinuata and Bumelia lanuginosa tree species from the Edward's Plateau region of central Texas. The white line in each sub-figure shows the scale for a length of 50 μm for Juniperus ashei, 300 μm for Quercus sinuata and Quercus fusiformis, and 200 μm for Bumelia lanuginosa. Adapted from McElrone et al. (2004), used by permission.

Figure 4 .

 4 Figure 4. Images of Eucalyptus fine roots in the topsoil (A), and at depth of 11.5 m (B) in minirhizotron tubes installed in deep permanent pits in Brazil showing great differences in branching density of very fine roots. The velocity of exploration of deep soil layer in this stand (C) is shown scanning the same 1.8-m long minirhizotron tube inserted at a depth of 11.5 m from September 20, 2017 to November 16, 2017. Adapted from Germon (2019).

Figure 5 .

 5 Figure 5. Relationship between root biomass carbon storage and water storage loss relative to long-term cultivated farmlands between the depths of 1m and 23.2 m in a chronosequence of 8-, 11-, 15-, 18-, and 22-year-old afforested apple (Malus pumila Mill.) orchard stands in a sub-humid region of the Chinese Loess Plateau. The standard deviations are indicated (n = 3). Adapted from Li et al. (2019), used by permission.

Figure 6 .

 6 Figure 6. Ectomycorrhizal root tips originated from 4-m deep pits in a Eucalyptus grandis plantation in Brazil. The yellow morphotype (a-f) was identified molecularly as Pisolithus spp. and the white morphotype (g-k) as Scleroderma spp. In each image, the scale bar corresponds to 1 mm. Adapted from Robin et al. (2019), used by permission.

Figure 7 .

 7 Figure7. Daily simulated actual evapotranspiration (AETsim) using MAESPA model (A) and time series of root length density (RLD, cm dm -3 ) (B) over 5 years after planting Eucalyptus trees in Brazil. The AETsim (A) is represented as a function of the depth of root water uptake (RWUsim, red gradient) or uptake from the capillary fringe above the water table (WT, blue), and the evaporation from the soil surface and from the wet canopy is represented in brown. Vertical lines (B) indicate the days when root profiles were measured, and the green line is the maximum measured rooting depth. Adapted from[START_REF] Christina | Importance of deep water uptake in tropical eucalypt forest[END_REF], used by permission.

Figure 8 .

 8 Figure 8. Soil water content (g g -1 ) of transects drilled to depths of up to 10 m perpendicular to eucalypt tree belts at 4 locations across south-west Western Australia (A-D). Dry areas show indirectly where eucalypt roots take up water. Adapted from Robinson et al. (2006), used by permission.

Figure 9 .

 9 Figure 9. Simulation of Eucalyptus root system by DigR model. Side view of a 5-year-old seedling (main) and detail (black rectangle) of shallow roots (bottom right). Different root types are shown: taproot (red), distal secondary taproot (light blue), plagiotropic secondary root (blue), cable-like root (yellow), long fine root (blue), medium fine root (purple), short fine root (red). DigR logo represents 2 × 2 m scale for the whole root system. Adapted from Barczi et al. (2018), used by permission.

McElroneet al. (2004)

Acknowledgments

Appendix 1: Main changes in fine root traits in deep soil layers compared to the topsoil. indicates an upward trend, indicates a downward trend and indicates predominantly no effect. Categories of root traits and individual root traits are adapted from [START_REF] Brunner | How tree roots respond to drought[END_REF], [START_REF] Brunner | Morphological and physiological responses of Scots pine fine roots to water supply in a dry climatic region in Switzerland[END_REF], [START_REF] Mccormack | Predicting fine root lifespan from plant functional traits in temperate trees[END_REF] and [START_REF] Prieto | Root functional parameters along a land use gradient: evidence of a community level economics spectrum[END_REF].

Root traits categories

Fine root traits