Rhizodeposition, i.e. the release of organic matters by roots, constitutes a significant fraction of the plant carbon (C) budget and plays a key role in plant-soil interactions. However, its spatial and temporal dynamics remain poorly understood. We developed RhizoDep, a new functional-structural root model that simulates 3D root growth, respiration, and rhizodeposition based on C balance and root morphology at the individual root segment level. Our model successfully reproduced the dynamics of belowground C flows observed in a previous pulse-labelling field experiment on spring wheat. Our simulations revealed that root C exudation largely dominated over mucilage secretion and cap cells sloughing in terms of C release. The spatial distribution of exudation rate along the roots was driven by the preferential unloading of sugars to support root elongation and emergence, and was modulated by the formation of apoplastic barriers. Furthermore, our results demonstrated that, for a given C allocation flow to roots, variations in root hairs or lateral root number had minimal effects on rhizodeposition, whereas changes in root tissue density had a significant impact. RhizoDep offers a new opportunity to explore the dynamics of C exchange at the plant-soil interface and to identify traits and environmental conditions that favor rhizodeposition.

Introduction Rhizodeposits, defined here as any organic materials released by living roots, can represent up to 15% of net amount of carbon (C) photosynthesized by a plant (Pausch and Kuzyakov, 2018). Rhizodeposits have been shown to play an important role in plant growth through various mechanisms (e.g. by favoring water uptake through mucilage secretion, or nutrient uptake through the exudation of soluble compounds), and to represent a major contributor to the formation of stable soil organic matter and thus to the mitigation of climate change through soil C sequestration. Decomposing rhizodeposition into its elementary processes (e.g. exudation, mucilage secretion, cells sloughing) is required for a better understanding of the response of rhizodeposition to various environmental constraints and of its associatedbenefits. While many works have attempted to quantify the exudation of soluble organic compounds at the scale of a plant or the net rhizodeposition of C in soils, very few studies have been able to estimate the amount of mucilage or sloughed cells released by a whole root system over time. Consequently, while it has been claimed that the amount of soluble organic C is much higher than the amount of C released as mucilage or sloughed cells by roots (Nguyen, 2003; Rees et al. 2005), the relative importance of distinct rhizodeposition processes in plant’s and soil’s C balance remains largely unknown. While the comparison of mucilage secretion and citrate exudation within a FSPM has been recently attempted (Landl et al. 2021), no model has been developed so far for simulating such rhizodeposition processes as part of plant’s C management. The present work aimed to give a better assessment of the contribution of distinct rhizodeposition processes to the total amount of organic C released by roots, for different plant species, growth stages and environments.

Although widely used in ecology, trait-based approaches are seldom used to study agroecosystems. In particular, there is a need to evaluate how functional trait variability among varieties of a crop species compares to the variability among wild plant species and how variety selection can modify trait syndromes. Here, we quantified 18 above- and below-ground functional traits for 57 varieties of common wheat representative of different modern selection histories. We compared trait variability among varieties and among Pooideae species, and analyzed the effect of selection histories on trait values and trait syndromes. For traits under strong selection, trait variability among varieties was less than 10% of the variability observed among Pooideae species. However, for traits not directly selected, such as root N uptake capacity, the variability was up to 75% of the variability among Pooideae species. Ammonium absorption capacity by roots was counter-selected for conventional varieties compared with organic varieties and landraces. Artificial selection also altered some trait syndromes classically reported for Pooideae. Identifying traits that have high or low variability among varieties and characterizing the hidden effects of selection on trait values and syndromes will benefit the selection of varieties to be used especially for lower N input agroecosystems.

Phenotypic plasticity-the ability of one genotype to produce different phenotypes depending on growth conditions-is a core aspect of the interactions between plants and the environment. The model CN-Wheat simulates the functioning of a grass culm and the construction of traits as properties emerging from the feedback loops between morphogenesis, the environmental factors and source-sink activities. The plant is seen as a self-regulated system where leaf growth is driven by carbon and nitrogen metabolism within each leaf and by coordination rules between successive leaves. Here, we investigated the ability of this approach to simulate realistic grass phenotypic plasticity and explored plant behaviour in a wide range of growth conditions. The growth of grass monoculms, with traits similar to a wheat stem, was simulated for highly contrasting conditions of soil nitrogen concentration, incident light and planting density. The monoculms were kept vegetative and produced similar to 15 mature leaves at the end of the simulations. The model simulated highly contrasting phenotypes. Overall, the simulated trends and the magnitude of responses of leaf and plant traits to growth conditions were consistent with the literature on grass species. These results demonstrate that integrating plant functioning at organ scale can simulate, as an emergent property, the phenotypic plasticity of plants in contrasting light and nitrogen conditions. Besides, simulations of the internal variables of plants gave access to plant trophic status across plant ontogeny and plant environments. In conclusion, this framework is a significant step towards better integration of the genotype-environment interactions.

Canopy light interception determines the amount of energy captured by a crop, and is thus critical to modeling crop growth and yield, and may substantially contribute to the prediction uncertainty of crop growth models (CGMs). We thus analyzed the canopy light interception models of the 26 wheat (Triticum aestivum) CGMs used by the Agricultural Model Intercomparison and Improvement Project (AgMIP). Twenty-one CGMs assume that the light extinction coefficient (K) is constant, varying from 0.37 to 0.80 depending on the model. The other models take into account the illumination conditions and assume either that all green surfaces in the canopy have the same inclination angle (theta) or that theta distribution follows a spherical distribution. These assumptions have not yet been evaluated due to a lack of experimental data. Therefore, we conducted a field experiment with five cultivars with contrasting leaf stature sown at normal and double row spacing, and analyzed theta distribution in the canopies from three-dimensional canopy reconstructions. In all the canopies, theta distribution was well represented by an ellipsoidal distribution. We thus carried out an intercomparison between the light interception models of the AgMIP-Wheat CGMs ensemble and a physically based K model with ellipsoidal leaf angle distribution and canopy clumping (K-ell(C)). Results showed that the K-ell(C) model outperformed current approaches under most illumination conditions and that the uncertainty in simulated wheat growth and final grain yield due to light models could be as high as 45%. Therefore, our results call for an overhaul of light interception models in CGMs.

Simulating leaf development from initiation to maturity opens new possibilities to model plant-environment interactions and the plasticity of plant architecture. This study analyses the dynamics of leaf production and extension along a maize (Zea mays) shoot to assess important modelling choices. Maize plants from two cultivars originating from the same inbred line, yet differing in the length of mature leaves were used in this study. We characterized the dynamics of the blade and sheath lengths of all phytomers by dissecting plants every 2-3 days. We analysed how differences in leaf size were built up and we examined the coordination between the emergence of organs and phases of their extension. Leaf extension rates were higher in the cultivar with longer leaves than in the cultivar with shorter leaves; no differences were found in other aspects. We found that (i) first post-embryonic leaves were initiated at a markedly higher rate than upper leaves; (ii) below ear position, sheaths were initiated at a time intermediate between tip emergence and appearance, while above the ear position, sheaths were initiated at a high rate, such that the time interval between the blade and sheath initiations decreased for these leaves; and (iii) ear position also marked a change in the correlation in size between successive phytomers with little correlation of size between upper and lower leaves. Our results identified leaf extension rate as the reason for the difference in size between the two cultivars. The two cultivars shared the same pattern for the timing of initiation events, which was more complex than previously thought. The differences described here may explain some inaccuracies reported in functional-structural plant models. We speculate that genotypic variation in behaviour for leaf and sheath initiation exists, which has been little documented in former studies.

Introduction - Rhizodeposition, i.e. the release of organic materials by roots, represents a significant portion of plant's carbon (C) budget, ranging from 5% to 15% of net photosynthesized C (Pausch and Kuzyakov, 2018). Various rhizodeposits can be released by roots, e.g. soluble exudates, secreted mucilage, sloughed cells, or volatile organic compounds. Despite their short lifetime, some of these products have been shown to favor plant growth, e.g. by increasing water and nutrient uptake. Among rhizodeposition processes, exudation has been suggested to depend on the concentration of carbohydrates inside the roots (Personeni et al., 2007). However, rhizodeposition not only depends on the availability of C in the roots, but also on the architecture of the root system, and many have shown that rhizodeposits are more concentrated in specific areas, such as root tips. Consequently, a Functional-Structural Plant Model (FSPM) would theoretically represent the best framework for simulating the spatial and temporal dynamics of rhizodeposition, as it can describe the evolution of both the metabolism and the architecture of the plant. The objective of this work is to create such a framework by coupling a whole-plant FSPM, a 3D root architectural model, and a new model simulating rhizodeposition. Modelling approach - Our strategy has been to combine the FSPM CN-Wheat (Barillot et al., 2016), which describes the main processes of C and nitrogen (N) acquisition and transformation by an individual wheat plant and the 3D growth and development of its aerial organs, with the model ArchiSimple (Pages et al., 2014) that simulates the development of the 3D root architecture for a range of plant species, and the new model RhizoDep, which calculates a full C balance in each part of a root system in order to simulate local rhizodeposition fluxes. The complementarity of the three models is illustrated in Figure 1: i) CN-Wheat is used to calculate the amount of C allocated from the shoots to the roots, ii) ArchiSimple provides the 3D structure of the root system, and iii) RhizoDep distributes the C provided by the shoots within the 3D root system and simulates the actual growth, respiration and rhizodeposition of each root element based on C availability. The major link between the three models lies in the exchange of C between aboveground and belowground tissues, which is driven by gradients of sucrose concentration in the different compartments of the plant. Preliminary results & short-term perspectives - The coupling of the three models has been started using the OpenAlea platform and its Multiscale Tree Graph formalism (Pradal et al., 2008). First simulations were done using the allocation of C to the roots simulated by CN-Wheat as an input to the root model based on the effective coupling of ArchiSimple and RhizoDep. These simulations show how rhizodeposition is intrinsically dependent on the architecture of the root system and on the total amount of available C. For completing the coupling, several issues still need to be tackled, e.g. how N uptake and metabolism should be spatialized in a 3D root system, how it may be regulated by local C and N availability, and how rhizodeposition can modify soil N availability. However, this modelling approach has already led to a first prototype able to simulate rhizodeposition processes on a dynamic, 3D root system that is fully integrated within the functioning of the whole plant. Its refinement will offer unique opportunities to study the possible link between rhizodeposition and the environmental factors affecting plant growth, e.g. atmospheric CO2 concentration or soil N availability.

Shoot architecture is a key component of the interactions between plants and their environment. We present a novel model of grass, which fully integrates shoot morphogenesis and the metabolism of carbon (C) and nitrogen (N) at organ scale, within a three-dimensional representation of plant architecture. Plant morphogenesis is seen as a self-regulated system driven by two main mechanisms. First, the rate of organ extension and the establishment of architectural traits are regulated by concentrations of C and N metabolites in the growth zones and the temperature. Second, the timing of extension is regulated by rules coordinating successive phytomers instead of a thermal time schedule. Local concentrations are calculated from a model of C and N metabolism at organ scale. The three-dimensional representation allows the accurate calculation of light and temperature distribution within the architecture. The model was calibrated for wheat (Triticum aestivum) and evaluated for early vegetative stages. This approach allowed the simulation of realistic patterns of leaf dimensions, extension dynamics, and organ mass and composition. The model simulated, as emergent properties, plant and agronomic traits. Metabolic activities of growing leaves were investigated in relation to whole-plant functioning and environmental conditions. The current model is an important step towards a better understanding of the plasticity of plant phenotype in different environments.

Background and Aims The dynamics of plant architecture is a central aspect of plant and crop models. Most models assume that whole shoot development is orchestrated by the leaf appearance rate, which follows a thermal time schedule. However, leaf appearance actually results from leaf extension and taking it as an input hampers our ability to understand shoot construction. The objective of the present study was to assess a modelling framework for grasses, in which the emergence of leaves and other organs is explicitly calculated as a result of their extension. Methods The approach builds on a previous model, which uses a set of rules co-ordinating the timing of development within and between phytomers. We first assessed rule validity for four experimental datasets. including different cultivars, planting densities and environments, and accordingly revised the equations driving the extension of the upper leaves and of internodes. We then fitted model parameters for each dataset and evaluated the ability to simulate the measured phenotypes across time. Finally, we carried out a sensitivity analysis to identify the parameters that had the greatest impact and to investigate model behaviour. Key Results The modified version of the model simulated correctly the contrasting maize phenotypes. Co-ordination rules accounted for the observations in all studied cultivars. Factors with major impact on model output included extension rates, the time of tassel initiation and initial conditions. A large diversity of phenotypes could be simulated. Conclusions This work provides direct experimental evidence for co-ordination rules and illustrates the capacity of the model to represent contrasting phenotypes. These rules play an important role in patterning shoot architecture and some of them need to be assessed further, considering contrasting growth conditions. To make the model more predictive, several parameters could be considered in the future as internal variables driven by plant status.

Introduction - Phenotypic plasticity - the ability of one genotype to produce different phenotypes depending on growth conditions - is a core aspect of the interactions between plants and their environment. For instance, leaf traits define the ability of plants to capture light, as well as their exposition and responses to various signals and stresses. In turn, leaf traits such as dimensions, composition and mass are highly regulated by growth conditions. The explicit description of shoot architecture in functional-structural models (FSPM) open new possibilities to express these feedback loops, which regulate plant fitness and productivity. However, formalizing into models the processes that build the plastic responses of traits to growth conditions is a major bottleneck to date. Most FSPMs that address the coupling between resources availability and growth consider only carbon (C) and drive resource allocation by sink priorities defined from empirical relations. Besides, the determinism of traits such as the areal density, which links mass growth with dimension growth, are poorly understood, so that these traits are frequently approximated as constant, while they have been shown to vary widely with growth conditions. Finally, the lack of process-based formalisms of existing models impairs our ability to simulate morphogenesis under contrasting growth conditions. As a step toward more mechanistic approaches to simulate shoot morphogenesis, we propose a plantscale FSPM of C and nitrogen (N) economy of the growing grass in which the morphogenesis is fully integrated with the plant metabolism. Model description - The model represents the plant as a collection of tillers made of several growing and mature shoot phytomers (identifying lamina, sheath and internode mature tissues and growth zones), a single roots compartment and a shared pool mimicking the phloem. Each compartment has a structural mass and concentrations in mobile and storage metabolites. The plant is seen as a self-regulated system which relies on two processes: i) local C and N concentrations in the growth zones drive organ elongation rate, specific structural mass and width, ii) coordination rules link the timing of extension of the organs between successive phytomers. These processes were implemented into CN-Wheat (Barillot et al., 2016ab), a detailed FSPM of C and N metabolism previously developed for a culm with a static architecture. The new version of CN-Wheat presented here is the coupling of (i) a model of leaf, internode and root growth, (ii) a dynamic representation of the 3D geometry of plants which builds on the ADEL-Wheat model (Fournier et al., 2003), (iii) a model of light distribution (Chelle and Andrieu, 1998), and finally (iv) a model simulating photosynthesis, N acquisition, synthesis and allocation of C and N metabolites, and senescence at the organ level, which extends the initial version of CN-Wheat. All above mentionned processes are regulated, at organ scale, by the environmental conditions and the concentrations in C and N metabolites. Results and Discussion - The model was calibrated for wheat during the vegetative stages (from seedling emergence to the beginning of stem extension). First, the model was evaluated in field conditions representative of North-Western Europe, which resulted in realistic patterns of leaf dimensions, extension and senescence dynamics, organ mass and composition. A key result was the ability of the model to simulate, as emerging properties, key plant and agronomic traits e.g. the phyllochron, shoot/roots ratio dynamic, N dilution and radiation use efficiency. Then, we evaluated the model's ability to simulate plant plasticity under different scenarios of plant density, incoming light and soil nitrate concentration. The model simulated realistic responses of leaf traits such as dimensions, specific leaf area and specific leaf N; the figure illustrates the simulated variations of lamina dimensions and N vertical gradient with N resources. Conclusion - Our model is innovative by the high level of explicitation of the processes underlying shoot morphogenesis, which provides new possibilities to link the phenotypic plasticity of plants to their C and N metabolic status at the place and time where traits are built. The approach could be extended to include other factors involved in plasticity, such as hormones or direct responses to the environment perceived. The genericity of the modelling frame makes it also applicable to explore shoot morphogenesis in other grass species.

BACKGROUND AND AIMS Because functional-structural plant models (FSPMs) take plant architecture explicitly into consideration, they constitute a promising approach for unravelling plant-plant interactions in complex canopies. However, existing FSPMs mainly address competition for light. The aim of the present work was to develop a comprehensive FSPM accounting for the interactions between plant architecture, environmental factors and the metabolism of carbon (C) and nitrogen (N). METHODS We developed an original FSPM by coupling models of (1) 3-D wheat architecture, (2) light distribution within canopies and (3) C and N metabolism. Model behaviour was evaluated by simulating the functioning of theoretical canopies consisting of wheat plants of contrasting leaf inclination, arranged in pure and mixed stands and considering four culm densities and three sky conditions. KEY RESULTS As an emergent property of the detailed description of metabolism, the model predicted a linear relationship between absorbed light and C assimilation, and a curvilinear relationship between grain mass and C assimilation, applying to both pure stands and each component of mixtures. Over the whole post-anthesis period, planophile plants tended to absorb more light than erectophile plants, resulting in a slightly higher grain mass. This difference was enhanced at low plant density and in mixtures, where the erectophile behaviour resulted in a loss of competitiveness. CONCLUSION The present work demonstrates that FSPMs provide a framework allowing the analysis of complex canopies such as studying the impact of particular plant traits, which would hardly be feasible experimentally. The present FSPM can help in interpreting complex interactions by providing access to critical variables such as resource acquisition and allocation, internal metabolic concentrations, leaf life span and grain filling. Simulations were based on canopies identically initialized at flowering; extending the model to the whole cycle is thus required so that all consequences of a trait can be evaluated.

Achieving novel improvements in crop management may require changing interrow distance in cultivated fields. Such changes would benefit from a better understanding of plant responses to the spatial heterogeneity in their environment. Our work investigates the architectural plasticity of wheat plants in response to increasing row spacing and evaluates the hypothesis of a foraging behavior in response to neighboring plants. A field experiment was conducted with five commercial winter wheat cultivars possessing unique architectures, grown under narrow (NI, 17.5 cm) or wide interrows (WI, 35 cm) at the same population density (170 seeds/m2). We characterized the development (leaf emergence, tillering), the morphology (dimension of organs, leaf area index), and the geometry (ground cover, leaf angle, organ spreading, and orientation). All cultivars showed a lower number of emerged tillers in WI compared to NI, which was later partly compensated by lower tiller mortality. Besides, the upper leaf blades were larger in WI. Finally the leaf area index at flowering showed little difference between WI and NI treatments. The rate of leaf emergence and the final leaf number were higher in WI compared to NI, except for one cultivar. Around the start of stem elongation, pseudo-stems were more erect in WI, while around the time of flowering, stems were more inclined and leaves were more planophile. Cultivars differed in their degrees of responses, with one appearing to prospect more specifically within the interrow space in WI treatment. Altogether, our results suggest that altering interrow distance leads to changes in the perceived extent of competition by plants, with responses first mimicking the effect of a higher plant density and later the effect of a lower plant density. Only one cultivar showed responses that suggested a perception of the heterogeneity of the environment. These findings improve our understanding of plant responses to spatial heterogeneity and provide novel information to simulate light capture in plant 3D models, depending on cultivar behavior.

The extraction of desirable heritable traits for crop improvement from high-throughput phenotyping (HTP) observations remains challenging. We developed a modeling workflow named "Digital Plant Phenotyping Platform" (D3P), to access crop architectural traits from HTP observations. D3P couples the Architectural model of DEvelopment based on L-systems (ADEL) wheat (Triticum aestivum) model (ADEL-Wheat), which describes the time course of the three-dimensional architecture of wheat crops, with simulators of images acquired with HTP sensors. We demonstrated that a sequential assimilation of the green fraction derived from Red-Green-Blue images of the crop into D3P provides accurate estimates of five key parameters (phyllochron, lamina length of the first leaf, rate of elongation of leaf lamina, number of green leaves at the start of leaf senescence, and minimum number of green leaves) of the ADEL-Wheat model that drive the time course of green area index and the number of axes with more than three leaves at the end of the tillering period. However, leaf and tiller orientation and inclination characteristics were poorly estimated. D3P was also used to optimize the observational configuration. The results, obtained from in silico experiments conducted on wheat crops at several vegetative stages, showed that the accessible traits could be estimated accurately with observations made at 0° and 60° zenith view inclination with a temporal frequency of 100 °Cd (degree day). This illustrates the potential of the proposed holistic approach that integrates all the available information into a consistent system for interpretation. The potential benefits and limitations of the approach are further discussed.

Structural 3D plant models aim at mimicking the dynamics of plant and crop structure based on experimental data. Such models can be interfaced with physical models to investigate plant-environment interactions. This work aimed at defining functions that represent the leaf and tiller development of individual wheat plants, and that could be fitted to the specific traits produced in a broad range of situations. A dataset of the dynamics of wheat plant (Triticum aestivum) architecture was collected for 55 experimental situations, including 11 growing seasons, three sowing densities, three sowing dates, and 13 commercial cultivars. Data were analysed to identify conserved patterns in the dynamics of leaf emergence and of tiller emergence and senescence. The broad range of conditions tested allowed us to evaluate the robustness of relationships proposed in previous studies and to identify novel patterns. Amongst them, we observed: (i) that leaf emergence dynamics may follow either a linear or a bilinear pattern for the same genotype. When a change in phyllochron occurred, it coincided with the initiation of the flag leaf; (ii) the delay between leaf and tiller emergence was not constant, but increased very regularly for successive phytomers; (iii) the number of leaves emerged at tillering cessation decreased with plant density but depended also on the final number of leaves on the main stem (MS) and marked differences existed between cultivars. Finally, we defined functions representing leaf and tiller dynamics with parameters that have a simple botanical interpretation and are easy to derive from field measurements. Assessing plant density, crop leaf stage at 5-6 dates and tiller population at 2 dates during the cycle provide the required data. This study defines a rationale to analyse and represent the dynamics of the architecture of individual wheat plants. The method can be used to determine the dynamics of architecture in 3D models and should be transposable to a wide range of cereal species.

The development of plant FSPMs requires to define how phytomers extend and reach their mature size. Both the rate and duration of organ extension are impacted by environmental conditions. However, the second point is rarely considered in plant growth models. Our work relied on an existing model based on the formalisation of coordination rules for maize, which allows flexibility in plant growth timing. However, the validation of this model was based up to now on a single experiment with one genotype, and did not include a direct evaluation of the coordination rules. The objective of the present work was to get a deeper view of the ability of modelling approaches based on coordination rules to simulate shoot development in maize. First we assessed the validity of coordination rules for two genotypes with contrasted number of leaves and grown in contrasted environments. Second we adjusted the model on both genotypes. Some formalisms were adapted to best represent both genotypes. Finally, our results show that a same set of coordination rules could represent precisely the development of maize genotypes of contrasted architectures. This bring support to the idea that coordination rules could be used in FSPM models as an alternative to a fixed thermal time schedule.