Breeding for Economically and Environmentally Sustainable Wheat Varieties: An Integrated Approach from Genomics to Selection.

There is currently a strong societal demand for sustainability, quality, and safety in bread wheat production. To address these challenges, new and innovative knowledge, resources, tools, and methods to facilitate breeding are needed. This starts with the development of high throughput genomic tools including single nucleotide polymorphism (SNP) arrays, high density molecular marker maps, and full genome sequences. Such powerful tools are essential to perform genome-wide association studies (GWAS), to implement genomic and phenomic selection, and to characterize the worldwide diversity. This is also useful to breeders to broaden the genetic basis of elite varieties through the introduction of novel sources of genetic diversity. Improvement in varieties particularly relies on the detection of genomic regions involved in agronomical traits including tolerance to biotic (diseases and pests) and abiotic (drought, nutrient deficiency, high temperature) stresses. When enough resolution is achieved, this can result in the identification of candidate genes that could further be characterized to identify relevant alleles. Breeding must also now be approached through in silico modeling to simulate plant development, investigate genotype × environment interactions, and introduce marker-trait linkage information in the models to better implement genomic selection. Breeders must be aware of new developments and the information must be made available to the world wheat community to develop new high-yielding varieties that can meet the challenge of higher wheat production in a sustainable and fluctuating agricultural context. In this review, we compiled all knowledge and tools produced during the BREEDWHEAT project to show how they may contribute to face this challenge in the coming years.

Interactions Between Environment and Genetic Diversity in Perennial Grass Phenology: A Review of Processes at Plant Scale and Modeling.

In perennial grasses, the reproductive development consists of major phenological stages which highly determine the seasonal variations of grassland biomass production in terms of quantity and quality. The reproductive development is regulated by climatic conditions through complex interactions subjected to high genetic diversity. Understanding these interactions and their impact on plant development and growth is essential to optimize grassland management and identify the potential consequences of climate change. Here, we review the main stages of reproductive development, from floral induction to heading, i.e., spike emergence, considering the effect of the environmental conditions and the genetic diversity observed in perennial grasses. We first describe the determinants and consequences of reproductive development at individual tiller scale before examining the interactions between plant tillers and their impact on grassland perenniality. Then, we review the available grassland models through their ability to account for the complexity of reproductive development and genetic × environmental interactions. This review shows that (1) The reproductive development of perennial grasses is characterized by a large intraspecific diversity which has the same order of magnitude as the diversity observed between species or environmental conditions. (2) The reproductive development is determined by complex interactions between the processes of floral induction and morphogenesis of the tiller. (3) The perenniality of a plant is dependent on the reproductive behavior of each tiller. (4) Published models only partly explain the complex interactions between morphogenesis and climate on reproductive development. (5) Introducing more explicitly the underlying processes involved in reproductive development in models would improve our ability to anticipate grassland behavior in future growth conditions.

Leaf elongation response to blue light is mediated by stomatal-induced variations in transpiration in Festuca arundinacea.

Reduced blue light irradiance is known to enhance leaf elongation rate (LER) in grasses, but the mechanisms involved have not yet been elucidated. We investigated whether leaf elongation response to reduced blue light could be mediated by stomata-induced variations of plant transpiration. Two experiments were carried out on tall fescue in order to monitor LER and transpiration under reduced blue light irradiance. Additionally, LER dynamics were compared with those observed in the response to vapour pressure deficit (VPD)-induced variations of transpiration. Finally, we developed a model of water flow within a tiller to simulate the observed short-term response of LER to various transpiration regimes. LER dramatically increased in response to blue light reduction and then reached new steady states, which remained higher than the control. Reduced blue light triggered a simultaneous stomatal closure which induced an immediate decrease of leaf transpiration. The hydraulic model of leaf elongation accurately predicted the LER response to blue light and VPD, resulting from an increase in the growth-induced water potential gradient in the leaf growth zone. Our results suggest that the blue light signal is sensed by stomata of expanded leaves and transduced to the leaf growth zone through the hydraulic architecture of the tiller.

A functional structural model of grass development based on metabolic regulation and coordination rules.

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.

Towards intercrop ideotypes: non-random trait assembly can promote overyielding and stability of species proportion in simulated legume-based mixtures.

BACKGROUNDS AND AIMS: A major challenge when supporting the development of intercropping systems remains the design of efficient species mixtures. The ecological processes that sustain overyielding of legume-based mixtures compared to pure crops are well known, but their links to plant traits remain to be unravelled. A common assumption is that enhancing trait divergence among species for resource acquisition when assembling plant mixtures should increase species complementarity and improve community performance. METHODS: The Virtual Grassland model was used to assess how divergence in trait values between species on four physiological functions (namely light and mineral N acquisition, temporal development, and C-N use efficiency) affected overyielding and mixture stability in legume-based binary mixtures. A first step allowed us to identify the model parameters that were most important to interspecies competition. A second step involved testing the impact of convergent and divergent parameter (or trait) values between species on virtual mixture performance. RESULTS: Maximal overyielding was achieved in cases where trait values were divergent for the physiological functions controlling N acquisition and temporal development but convergent for light interception. It was also found that trait divergence should not affect competitive abilities of legume and non-legumes at random. Indeed, random trait combinations frequently led to reduced mixture yields when compared to a perfectly convergent neutral model. Combinations with the highest overyielding also tended to be associated with mixture instability and decreasing legume biomass proportion. Achieving both high overyielding and mixture stability was only found to be possible under low or moderate N levels, using combinations of traits adapted to each environment. CONCLUSIONS: No simple assembly rule based on trait divergence could be confirmed. Plant models able to infer plant-plant interactions can be helpful for the identification of major interaction traits and the definition of ideotypes adapted to a targeted intercropping system.

WALTer: a three-dimensional wheat model to study competition for light through the prediction of tillering dynamics.

BACKGROUND AND AIMS: Branching is a main morphogenetic process involved in the adaptation of plants to the environment. In grasses, tillering is divided into three phases: tiller emergence, cessation of tillering and tiller regression. Understanding and prediction of the tillering process is a major challenge to better control cereal yields. In this paper, we present and evaluate WALTer, an individual-based model of wheat built on simple self-adaptive rules for predicting the tillering dynamics at contrasting sowing densities. METHODS: WALTer simulates the three-dimensional (3-D) development of the aerial architecture of winter wheat. Tillering was modelled using two main hypotheses: (H1) a plant ceases to initiate new tillers when a critical Green Area Index (GAIc) is reached, and (H2) the regression of a tiller occurs if its interception of light is below a threshold (PARt). The development of vegetative organs follows descriptive rules adapted from the literature. A sensitivity analysis was performed to evaluate the impact of each parameter on tillering and GAI dynamics. WALTer was parameterized and evaluated using an initial dataset providing an extensive description of GAI dynamics, and another dataset describing tillering dynamics under a wide range of sowing densities. KEY RESULTS: Sensitivity analysis indicated the predominant importance of GAIc and PARt. Tillering and GAI dynamics of expt 1 were well fit by WALTer. Once calibrated based on the agronomic density of expt 2, tillering parameters allowed an adequate prediction of tillering dynamics at contrasting sowing densities. CONCLUSIONS: Using simple rules and a small number of parameters, WALTer efficiently simulated the wheat tillering dynamics observed at contrasting densities in experimental data. These results show that the definition of a critical GAI and a threshold of PAR is a relevant way to represent, respectively, cessation of tillering and tiller regression under competition for light.

Investigation of complex canopies with a functional-structural plant model as exemplified by leaf inclination effect on the functioning of pure and mixed stands of wheat during grain filling.

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.

CN-Wheat, a functional-structural model of carbon and nitrogen metabolism in wheat culms after anthesis. I. Model description.

Background and Aims Improving crops requires better linking of traits and metabolic processes to whole plant performance. In this paper, we present CN-Wheat, a comprehensive and mechanistic model of carbon (C) and nitrogen (N) metabolism within wheat culms after anthesis. Methods The culm is described by modules that represent the roots, photosynthetic organs and grains. Each of them includes structural, storage and mobile materials. Fluxes of C and N among modules occur through a common pool and through transpiration flow. Metabolite variations are represented by differential equations that depend on the physiological processes occurring in each module. A challenging aspect of CN-Wheat lies in the regulation of these processes by metabolite concentrations and the environment perceived by organs. Key Results CN-Wheat simulates the distribution of C and N into wheat culms in relation to photosynthesis, N uptake, metabolite turnover, root exudation and tissue death. Regulation of physiological activities by local concentrations of metabolites appears to be a valuable feature for understanding how the behaviour of the whole plant can emerge from local rules. Conclusions The originality of CN-Wheat is that it proposes an integrated view of plant functioning based on a mechanistic approach. The formalization of each process can be further refined in the future as knowledge progresses. This approach is expected to strengthen our capacity to understand plant responses to their environment and investigate plant traits adapted to changes in agronomical practices or environmental conditions. A companion paper will evaluate the model.

CN-Wheat, a functional-structural model of carbon and nitrogen metabolism in wheat culms after anthesis. II. Model evaluation.

Background and Aims Simulating resource allocation in crops requires an integrated view of plant functioning and the formalization of interactions between carbon (C) and nitrogen (N) metabolisms. This study evaluates the functional-structural model CN-Wheat developed for winter wheat after anthesis. Methods In CN-Wheat the acquisition and allocation of resources between photosynthetic organs, roots and grains are emergent properties of sink and source activities and transfers of mobile metabolites. CN-Wheat was calibrated for field plants under three N fertilizations at anthesis. Model parameters were taken from the literature or calibrated on the experimental data. Key Results The model was able to predict the temporal variations and the distribution of resources in the culm. Thus, CN-Wheat accurately predicted the post-anthesis kinetics of dry masses and N content of photosynthetic organs and grains in response to N fertilization. In our simulations, when soil nitrates were non-limiting, N in grains was ultimately determined by availability of C for root activity. Dry matter accumulation in grains was mostly affected by photosynthetic organ lifespan, which was regulated by protein turnover and C-regulated root activity. Conclusions The present study illustrates that the hypotheses implemented in the model were able to predict realistic dynamics and spatial patterns of C and N. CN-Wheat provided insights into the interplay of C and N metabolism and how the depletion of mobile metabolites due to grain filling ultimately results in the cessation of resource capture. This enabled us to identify processes that limit grain mass and protein content and are potential targets for plant breeding.

Assessing the effects of architectural variations on light partitioning within virtual wheat-pea mixtures.

BACKGROUND AND AIMS: Predicting light partitioning in crop mixtures is a critical step in improving the productivity of such complex systems, and light interception has been shown to be closely linked to plant architecture. The aim of the present work was to analyse the relationships between plant architecture and light partitioning within wheat-pea (Triticum aestivum-Pisum sativum) mixtures. An existing model for wheat was utilized and a new model for pea morphogenesis was developed. Both models were then used to assess the effects of architectural variations in light partitioning. METHODS: First, a deterministic model (L-Pea) was developed in order to obtain dynamic reconstructions of pea architecture. The L-Pea model is based on L-systems formalism and consists of modules for 'vegetative development' and 'organ extension'. A tripartite simulator was then built up from pea and wheat models interfaced with a radiative transfer model. Architectural parameters from both plant models, selected on the basis of their contribution to leaf area index (LAI), height and leaf geometry, were then modified in order to generate contrasting architectures of wheat and pea. KEY RESULTS: By scaling down the analysis to the organ level, it could be shown that the number of branches/tillers and length of internodes significantly determined the partitioning of light within mixtures. Temporal relationships between light partitioning and the LAI and height of the different species showed that light capture was mainly related to the architectural traits involved in plant LAI during the early stages of development, and in plant height during the onset of interspecific competition. CONCLUSIONS: In silico experiments enabled the study of the intrinsic effects of architectural parameters on the partitioning of light in crop mixtures of wheat and pea. The findings show that plant architecture is an important criterion for the identification/breeding of plant ideotypes, particularly with respect to light partitioning.

Comparison of the morphogenesis of three genotypes of pea (Pisum sativum) grown in pure stands and wheat-based intercrops.

Cereal-legume intercrops represent a promising way of combining high productivity and agriculture sustainability. The benefits of cereal-legume mixtures are highly affected by species morphology and functioning, which determine the balance between competition and complementarity for resource acquisition. Studying species morphogenesis, which controls plant architecture, is therefore of major interest. The morphogenesis of cultivated species has been mainly described in mono-specific growing conditions, although morphogenetic plasticity can occur in multi-specific stands. The aim of the present study was therefore to characterize the variability of the morphogenesis of pea plants grown either in pure stands or mixed with wheat. This was achieved through a field experiment that included three pea cultivars with contrasting earliness (hr and HR type) and branching patterns. Results show that most of the assessed parameters of pea morphogenesis (phenology, branching, final number of vegetative organs and their kinetics of appearance) were mainly dependent on the considered genotype, which highlights the importance of the choice of cultivars in intercropping systems. There was however a low variability of pea morphogenesis between sole and mixed stands except for plant height and branching of the long-cycle cultivar. The information provided in the present study at stand and plant scale can be used to build up structural-functional models. These models can contribute to improving the understanding of the functioning of cereal-legume intercrops and also to the definition of plant ideotypes adapted to the growth in intercrops.

How does pea architecture influence light sharing in virtual wheat-pea mixtures? A simulation study based on pea genotypes with contrasting architectures.

BACKGROUND AND AIMS: Light interception is a key factor driving the functioning of wheat-pea intercrops. The sharing of light is related to the canopy structure, which results from the architectural parameters of the mixed species. In the present study, we characterized six contrasting pea genotypes and identified architectural parameters whose range of variability leads to various levels of light sharing within virtual wheat-pea mixtures. METHODOLOGY: Virtual plants were derived from magnetic digitizations performed during the growing cycle in a greenhouse experiment. Plant mock-ups were used as inputs of a radiative transfer model in order to estimate light interception in virtual wheat-pea mixtures. The turbid medium approach, extended to well-mixed canopies, was used as a framework for assessing the effects of leaf area index (LAI) and mean leaf inclination on light sharing. PRINCIPAL RESULTS: THREE GROUPS OF PEA GENOTYPES WERE DISTINGUISHED: (i) early and leafy cultivars, (ii) late semi-leafless cultivars and (iii) low-development semi-leafless cultivars. Within open canopies, light sharing was well described by the turbid medium approach and was therefore determined by the architectural parameters that composed LAI and foliage inclination. When canopy closure started, the turbid medium approach was unable to properly infer light partitioning because of the vertical structure of the canopy. This was related to the architectural parameters that determine the height of pea genotypes. Light capture was therefore affected by the development of leaflets, number of branches and phytomers, as well as internode length. CONCLUSIONS: This study provides information on pea architecture and identifies parameters whose variability can be used to drive light sharing within wheat-pea mixtures. These results could be used to build up the architecture of pea ideotypes adapted to multi-specific stands towards light competition.

How good is the turbid medium-based approach for accounting for light partitioning in contrasted grass--legume intercropping systems?

BACKGROUND AND AIMS: Most studies dealing with light partitioning in intercropping systems have used statistical models based on the turbid medium approach, thus assuming homogeneous canopies. However, these models could not be directly validated although spatial heterogeneities could arise in such canopies. The aim of the present study was to assess the ability of the turbid medium approach to accurately estimate light partitioning within grass-legume mixed canopies. METHODS: Three contrasted mixtures of wheat-pea, tall fescue-alfalfa and tall fescue-clover were sown according to various patterns and densities. Three-dimensional plant mock-ups were derived from magnetic digitizations carried out at different stages of development. The benchmarks for light interception efficiency (LIE) estimates were provided by the combination of a light projective model and plant mock-ups, which also provided the inputs of a turbid medium model (SIRASCA), i.e. leaf area index and inclination. SIRASCA was set to gradually account for vertical heterogeneity of the foliage, i.e. the canopy was described as one, two or ten horizontal layers of leaves. KEY RESULTS: Mixtures exhibited various and heterogeneous profiles of foliar distribution, leaf inclination and component species height. Nevertheless, most of the LIE was satisfactorily predicted by SIRASCA. Biased estimations were, however, observed for (1) grass species and (2) tall fescue-alfalfa mixtures grown at high density. Most of the discrepancies were due to vertical heterogeneities and were corrected by increasing the vertical description of canopies although, in practice, this would require time-consuming measurements. CONCLUSIONS: The turbid medium analogy could be successfully used in a wide range of canopies. However, a more detailed description of the canopy is required for mixtures exhibiting vertical stratifications and inter-/intra-species foliage overlapping. Architectural models remain a relevant tool for studying light partitioning in intercropping systems that exhibit strong vertical heterogeneities. Moreover, these models offer the possibility to integrate the effects of microclimate variations on plant growth.

What determines the complex kinetics of stomatal conductance under blueless PAR in Festuca arundinacea? Subsequent effects on leaf transpiration.

Light quality and, in particular, its content of blue light is involved in plant functioning and morphogenesis. Blue light variation frequently occurs within a stand as shaded zones are characterized by a simultaneous decrease of PAR and blue light levels which both affect plant functioning, for example, gas exchange. However, little is known about the effects of low blue light itself on gas exchange. The aims of the present study were (i) to characterize stomatal behaviour in Festuca arundinacea leaves through leaf gas exchange measurements in response to a sudden reduction in blue light, and (ii) to test the putative role of Ci on blue light gas exchange responses. An infrared gas analyser (IRGA) was used with light transmission filters to study stomatal conductance (gs), transpiration (Tr), assimilation (A), and intercellular concentration of CO(2) (Ci) responses to blueless PAR (1.80 mumol m(-2) s(-1)). The results were compared with those obtained under a neutral filter supplying a similar photosynthetic efficiency to the blueless PAR filter. It was shown that the reduction of blue light triggered a drastic and instantaneous decrease of gs by 43.2% and of Tr by 40.0%, but a gradual stomatal reopening began 20 min after the start of the low blue light treatment, thus leading to new steady-states. This new stomatal equilibrium was supposed to be related to Ci. The results were confirmed in more developed plants although they exhibited delayed and less marked responses. It is concluded that stomatal responses to blue light could play a key role in photomorphogenetic mechanisms through their effect on transpiration.