Laboratoire d'Ecophysiologie des Plantes sous Stress environnementaux

Significance Agricultural production is vulnerable to climate change. Understanding climate change, especially the temperature impacts, is critical if policymakers, agriculturalists, and crop breeders are to ensure global food security. Our study, by compiling extensive published results from four analytical methods, shows that independent methods consistently estimated negative temperature impacts on yields of four major crops at the global scale, generally underpinned by similar impacts at country and site scales. Multimethod analyses improved the confidence in assessments of future climate impacts on global major crops, with important implications for developing crop- and region-specific adaptation strategies to ensure future food supply of an increasing world population.

Stomatal control of species with contrasting stomatal behaviours have been investigated under natural fluctuations of evaporative demand and soil water status. Sunflower and barley (anisohydric behaviour) have a daytime leaf water potential (ΨI) which markedly decreases with evaporative demand during the day and is lower in droughted than in watered plants. In contrast, maize and poplar (isohydric behaviour) maintain a nearly constant ΨI during the day at a value which does not depend on soil water status until plants are close to death. Plants were also subjected to a range of soil water potentials under contrasting air vapour pressure deficits (VPD, from 0.5 to 3 kPa) in the field, in the greenhouse or in a growth chamber. Finally, plants or detached leaves were fed with varying concentrations of artificial ABA. Stomatal conductance of well-watered plants had no response to VPD when plants were grown in natural soils, suggesting that the opposite result observed in many laboratory experiments might be linked to the low unsaturated hydraulic conductivity of usual potting substrates. The response of stomatal conductance of all studied species to the concentration of ABA in pressurized xylem sap ([ABA]xyl) was the same whether ABA had an endogenous origin (droughted plants) or was artificially fed. However stomatal response of maize and poplar to [ABA]xyl markedly changed with varying evaporative demand or ΨI, whereas this was not the case in sunflower or barley. This suggests that isohydric behaviour is linked to an interaction between hydraulic and chemical information, while anisohydric behaviour is linked to an absence of interaction. In all cases, [ABA]xyl was related to soil water status with common relationships for different experimental conditions, but with markedly different responses among species. Diurnal variations of [ABA]xyl with evaporative demand were small in all studied species. Results are synthesized in a model which accounts for observed behaviours of gs, ΨI and [ABA]xyl in fluctuating conditions and for several species. The validity of this model, in particular the physiological meaning of [ABA]xyl, is discussed.

In plants, carbon (C) molecules provide building blocks for biomass production, fuel for energy, and exert signalling roles to shape development and metabolism. Accordingly, plant growth is well correlated with light interception and energy conversion through photosynthesis. Because water deficits close stomata and thus reduce C entry, it has been hypothesised that droughted plants are under C starvation and their growth under C limitation. In this review, these points are questioned by combining literature review with experimental and modelling illustrations in various plant organs and species. First, converging evidence is gathered from the literature that water deficit generally increases C concentration in plant organs. The hypothesis is raised that this could be due to organ expansion (as a major C sink) being affected earlier and more intensively than photosynthesis (C source) and metabolism. How such an increase is likely to interact with C signalling is not known. Hence, the literature is reviewed for possible links between C and stress signalling that could take part in this interaction. Finally, the possible impact of water deficit-induced C accumulation on growth is questioned for various sink organs of several species by combining published as well as new experimental data or data generated using a modelling approach. To this aim, robust correlations between C availability and sink organ growth are reported in the absence of water deficit. Under water deficit, relationships weaken or are modified suggesting release of the influence of C availability on sink organ growth. These results are interpreted as the signature of a transition from source to sink growth limitation under water deficit.

Stomata play a key role in plant adaptation to changing environmental conditions as they control both water losses and CO(2) uptake. Particularly, in the context of global change, simulations of the consequences of drought on crop plants are needed to design more efficient and water-saving cropping systems. However, most of the models of stomatal conductance (g(s)) developed at the leaf level link g(s) to environmental factors or net photosynthesis (A(net)), but do not include satisfactorily the effects of drought, impairing our capacity to simulate plant functioning in conditions of limited water supply. The objective of this review was to draw an up-to-date picture of the g(s) models, from the empirical to the process-based ones, along with their mechanistic or deterministic bases. It focuses on models capable to account for multiple environmental influences with emphasis on drought conditions. We examine how models that have been proposed for well-watered conditions can be combined with those specifically designed to deal with drought conditions. Ideas for future improvements of g(s) models are discussed: the issue of co-regulation of g(s) and A(net); the roles of CO(2), absissic acid and H(2)O(2); and finally, how to better address the new challenges arising from the issue of global change.

The improvement of crop yield has been possible through the indirect manipulation of quantitative trait loci (QTLs) that control heritable variability of the traits and physiological mechanisms that determine biomass production and its partitioning. This article surveys how QTL-based approaches contribute to a better understanding of the genetic basis of crop performance under environmentally constrained conditions and critically analyzes how this knowledge can assist breeders accelerate the release of cultivars better able to cope with abiotic constraints.

Drought tolerance involves mechanisms operating at different spatial and temporal scales, from rapid stomatal closure to maintenance of crop yield. We review how short-term mechanisms are controlled for stabilizing shoot water potential and how long-term processes have been constrained by evolution or breeding to fit into acclimation strategies for specific drought scenarios. These short- or long-term feedback processes participate in trade-offs between carbon accumulation and the risk of deleterious soil water depletion. Corresponding traits and alleles may therefore have positive or negative effects on crop yield depending on drought scenarios. We propose an approach that analyzes the genetic architecture of traits in phenotyping platforms and of yield in tens of field experiments. A combination of modeling and genomic prediction is then used to estimate the comparative interests of combinations of alleles depending on drought scenarios. Hence, drought tolerance is understood probabilistically by estimating the benefit and risk of each combination of alleles.

Abstract Wheat grain protein concentration is an important determinant of wheat quality for human nutrition that is often overlooked in efforts to improve crop production. We tested and applied a 32‐multi‐model ensemble to simulate global wheat yield and quality in a changing climate. Potential benefits of elevated atmospheric CO 2 concentration by 2050 on global wheat grain and protein yield are likely to be negated by impacts from rising temperature and changes in rainfall, but with considerable disparities between regions. Grain and protein yields are expected to be lower and more variable in most low‐rainfall regions, with nitrogen availability limiting growth stimulus from elevated CO 2 . Introducing genotypes adapted to warmer temperatures (and also considering changes in CO 2 and rainfall) could boost global wheat yield by 7% and protein yield by 2%, but grain protein concentration would be reduced by −1.1 percentage points, representing a relative change of −8.6%. Climate change adaptations that benefit grain yield are not always positive for grain quality, putting additional pressure on global wheat production.

Most traits associated with drought tolerance have a dual effect, positive in very severe scenarios and negative in milder scenarios, or the opposite trend. Their effects also depend on other climatic conditions such as evaporative demand or light, and on management practices. This is the case for processes associated with cell protection and with avoidance, but also for the maintenance of growth or photosynthesis, high water use efficiency, large root systems or reduced abortion rate under water deficit. Therefore, spectacular results obtained in one drought scenario may have a limited interest for improving food security in other geographical areas with water scarcity. The most relevant questions on drought tolerance are probably, 'Does a given allele confer a positive effect on yield in an appreciable proportion of years/scenarios in a given area or target population of environment (TPE)?'; 'In a given site or TPE, what is the trade-off between risk avoidance and maintained performance?'; and 'Will a given allele or trait have an increasingly positive effect with climate change?' Considerable progress has already occurred in drought tolerance. Nevertheless, explicitly associating traits for tolerance to drought scenarios may have profound consequences on the genetic strategies, with a necessary involvement of modelling.

• The high-throughput phenotypic analysis of Arabidopsis thaliana collections requires methodological progress and automation. Methods to impose stable and reproducible soil water deficits are presented and were used to analyse plant responses to water stress. • Several potential complications and methodological difficulties were identified, including the spatial and temporal variability of micrometeorological conditions within a growth chamber, the difference in soil water depletion rates between accessions and the differences in developmental stage of accessions the same time after sowing. Solutions were found. • Nine accessions were grown in four experiments in a rigorously controlled growth-chamber equipped with an automated system to control soil water content and take pictures of individual plants. One accession, An1, was unaffected by water deficit in terms of leaf number, leaf area, root growth and transpiration rate per unit leaf area. • Methods developed here will help identify quantitative trait loci and genes involved in plant tolerance to water deficit.

Land plant aerial organs are covered by a hydrophobic layer called the cuticle that serves as a waterproof barrier protecting plants against desiccation, ultraviolet radiation, and pathogens. Cuticle consists of a cutin matrix as well as cuticular waxes in which very-long-chain (VLC) alkanes are the major components, representing up to 70% of the total wax content in Arabidopsis (Arabidopsis thaliana) leaves. However, despite its major involvement in cuticle formation, the alkane-forming pathway is still largely unknown. To address this deficiency, we report here the characterization of the Arabidopsis ECERIFERUM1 (CER1) gene predicted to encode an enzyme involved in alkane biosynthesis. Analysis of CER1 expression showed that CER1 is specifically expressed in the epidermis of aerial organs and coexpressed with other genes of the alkane-forming pathway. Modification of CER1 expression in transgenic plants specifically affects VLC alkane biosynthesis: waxes of TDNA insertional mutant alleles are devoid of VLC alkanes and derivatives, whereas CER1 overexpression dramatically increases the production of the odd-carbon-numbered alkanes together with a substantial accumulation of iso-branched alkanes. We also showed that CER1 expression is induced by osmotic stresses and regulated by abscisic acid. Furthermore, CER1-overexpressing plants showed reduced cuticle permeability together with reduced soil water deficit susceptibility. However, CER1 overexpression increased susceptibility to bacterial and fungal pathogens. Taken together, these results demonstrate that CER1 controls alkane biosynthesis and is highly linked to responses to biotic and abiotic stresses.

Growth and carbon (C) fluxes are severely altered in plants exposed to soil water deficit. Correspondingly, it has been suggested that plants under water deficit suffer from C shortage. In this study, we test this hypothesis in Arabidopsis (Arabidopsis thaliana) by providing an overview of the responses of growth, C balance, metabolites, enzymes of the central metabolism, and a set of sugar-responsive genes to a sustained soil water deficit. The results show that under drought, rosette relative expansion rate is decreased more than photosynthesis, leading to a more positive C balance, while root growth is promoted. Several soluble metabolites accumulate in response to soil water deficit, with K(+) and organic acids as the main contributors to osmotic adjustment. Osmotic adjustment costs only a small percentage of the daily photosynthetic C fixation. All C metabolites measured (not only starch and sugars but also organic acids and amino acids) show a diurnal turnover that often increased under water deficit, suggesting that these metabolites are readily available for being metabolized in situ or exported to roots. On the basis of 30 enzyme activities, no in-depth reprogramming of C metabolism was observed. Water deficit induces a shift of the expression level of a set of sugar-responsive genes that is indicative of increased, rather than decreased, C availability. These results converge to show that the differential impact of soil water deficit on photosynthesis and rosette expansion results in an increased availability of C for the roots, an increased turnover of C metabolites, and a low-cost C-based osmotic adjustment, and these responses are performed without major reformatting of the primary metabolism machinery.

Ecophysiological models predict quantitative traits of one genotype in any environment, whereas quantitative trait locus (QTL) models predict the contribution of alleles to quantitative traits under a limited number of environments. We have combined both approaches by dissecting into effects of QTLs the parameters of a model of maize (Zea mays) leaf elongation rate (LER; H. Ben Haj Salah, F. Tardieu [1997] Plant Physiol 114: 893-900). Response curves of LER to meristem temperature, water vapor pressure difference, and soil water status were established in 100 recombinant inbred lines (RILs) of maize in six experiments carried out in the field or in the greenhouse. All responses were linear and common to different experiments, consistent with the model. A QTL analysis was carried out on the slopes of these responses by composite interval mapping confirmed by bootstrap analysis. Most QTLs were specific of one response only. QTLs of abscisic acid concentration in the xylem sap colocalized with QTLs of response to soil water deficit and conferred a low response. Each parameter of the ecophysiological model was computed as the sum of QTL effects, allowing calculation of parameters for 11 new RILs and two parental lines. LERs were simulated and compared with measurements in a growth chamber experiment. The combined model accounted for 74% of the variability of LER, suggesting that it has a general value for any RIL under any environment.

Abstract Understanding the drivers of yield levels under climate change is required to support adaptation planning and respond to changing production risks. This study uses an ensemble of crop models applied on a spatial grid to quantify the contributions of various climatic drivers to past yield variability in grain maize and winter wheat of European cropping systems (1984–2009) and drivers of climate change impacts to 2050. Results reveal that for the current genotypes and mix of irrigated and rainfed production, climate change would lead to yield losses for grain maize and gains for winter wheat. Across Europe, on average heat stress does not increase for either crop in rainfed systems, while drought stress intensifies for maize only. In low-yielding years, drought stress persists as the main driver of losses for both crops, with elevated CO 2 offering no yield benefit in these years.

The development of functional-structural plant models requires an increasing amount of computer modelling. All these models are developed by different teams in various contexts and with different goals. Efficient and flexible computational frameworks are required to augment the interaction between these models, their reusability, and the possibility to compare them on identical datasets. In this paper, we present an open-source platform, OpenAlea, that provides a user-friendly environment for modellers, and advanced deployment methods. OpenAlea allows researchers to build models using a visual programming interface and provides a set of tools and models dedicated to plant modelling. Models and algorithms are embedded in OpenAlea 'components' with well defined input and output interfaces that can be easily interconnected to form more complex models and define more macroscopic components. The system architecture is based on the use of a general purpose, high-level, object-oriented script language, Python, widely used in other scientific areas. We present a brief rationale that underlies the architectural design of this system and we illustrate the use of the platform to assemble several heterogeneous model components and to rapidly prototype a complex modelling scenario.

The classical view that the drought-related hormone ABA simply acts locally at the guard cell level to induce stomatal closure is questioned by differences between isolated epidermis and intact leaves in stomatal response to several stimuli. We tested the hypothesis that ABA mediates, in addition to a local effect, a remote effect in planta by changing hydraulic regulation in the leaf upstream of the stomata. By gravimetry, porometry to water vapour and argon, and psychrometry, we investigated the effect of exogenous ABA on transpiration, stomatal conductance and leaf hydraulic conductance of mutants described as ABA-insensitive at the guard cell level. We show that foliar transpiration of several ABA-insensitive mutants decreases in response to ABA. We demonstrate that ABA decreases stomatal conductance and down-regulates leaf hydraulic conductance in both the wildtype Col-0 and the ABA-insensitive mutant ost2-2. We propose that ABA promotes stomatal closure in a dual way via its already known biochemical effect on guard cells and a novel, indirect hydraulic effect through a decrease in water permeability within leaf vascular tissues. Variability in sensitivity of leaf hydraulic conductance to ABA among species could provide a physiological basis to the isohydric or anisohydric behaviour.

Increasing the accuracy of crop productivity estimates is a key element in planning adaptation strategies to ensure global food security under climate change. Process-based crop models are effective means to project climate impact on crop yield, but have large uncertainty in yield simulations. Here, we show that variations in the mathematical functions currently used to simulate temperature responses of physiological processes in 29 wheat models account for >50% of uncertainty in simulated grain yields for mean growing season temperatures from 14 °C to 33 °C. We derived a set of new temperature response functions that when substituted in four wheat models reduced the error in grain yield simulations across seven global sites with different temperature regimes by 19% to 50% (42% average). We anticipate the improved temperature responses to be a key step to improve modelling of crops under rising temperature and climate change, leading to higher skill of crop yield projections.

We have known for many years that the dehydration of plant cells can lead to accumulation of the plant growth regulator ABA. Application of this compound to well-watered plants mimics many of the effects of soil drymg on gene expression, physiology, growth, and development, making this compound a strong candidate for a role in the droughted plant. Dehydration of leaves can result in massive accumulations of ABA, and roots also synthesize the compound in increased amounts as they are exposed to drier and drier soil. Davies and Zhang (1991) argued that an important component of the drought responses of many plants can be an ABA signal moving from the roots to the shoots to regulate physiology and development as a function of soil water status/availability. Many recent reports show relationships between stomatal conductance and soil water status or xylem ABA concentration, which seem to support this view. Nevertheless, critica1 examination of the ABA-signaling hypothesis must show that enough extra ABA moves in the transpiration stream to the shoots to account for the changes in functioning that are recorded. Many other chemicals moving in the xylem to shoots can also provide shoots with 'information conceming root functioning, and we must consider the nature of such signals. We should also be concemed with the nature of the information that might be transmitted by a root signal (eg. a measure of soil water status or soil water availability) and the form that such a chemical signal might take (e.g. the concentration of the signal molecule in the transpiration stream or the flux of signal molecules to the site of action in the leaf).

Summary Leaf growth is the central process facilitating energy capture and plant performance. This is also one of the most sensitive processes to a wide range of abiotic stresses. Because hydraulics and metabolics are two major determinants of expansive growth (volumetric increase) and structural growth (dry matter increase), we review the interaction nodes between water and carbon. We detail the crosstalks between water and carbon transports, including the dual role of stomata and aquaporins in regulating water and carbon fluxes, the coupling between phloem and xylem, the interactions between leaf water relations and photosynthetic capacity, the links between Lockhart's hydromechanical model and carbon metabolism, and the central regulatory role of abscisic acid. Then, we argue that during leaf ontogeny, these interactions change dramatically because of uncoupled modifications between several anatomical and physiological features of the leaf. We conclude that the control of leaf growth switches from a metabolic to a hydromechanical limitation during the course of leaf ontogeny. Finally, we illustrate how taking leaf ontogeny into account provides insights into the mechanisms underlying leaf growth responses to abiotic stresses that affect water and carbon relations, such as elevated CO 2 , low light, high temperature and drought. Contents Summary 349 I. Leaf growth: volume, structures, water and carbon 349 II. Coupling water and carbon limitations through the Lockhart model? 350 III. ABA signalling pathway as a hub to coordinate water and carbon relations 353 IV. Leaf venation: just a two‐way pipe network? 354 V. Leaf ontogeny orchestrates the actors involved in the control of leaf growth 355 VI. The growing leaf in a changing world 360 VII. Conclusion 361 Acknowledgements 362 References 362

Global climate change is predicted to increase temperatures, alter geographical patterns of rainfall and increase the frequency of extreme climatic events. Such changes are likely to alter the timing and magnitude of drought stresses experienced by crops. This study used new developments in the classification of crop water stress to first characterize the typology and frequency of drought-stress patterns experienced by European maize crops and their associated distributions of grain yield, and second determine the influence of the breeding traits anthesis-silking synchrony, maturity and kernel number on yield in different drought-stress scenarios, under current and future climates. Under historical conditions, a low-stress scenario occurred most frequently (ca. 40%), and three other stress types exposing crops to late-season stresses each occurred in ca. 20% of cases. A key revelation shown was that the four patterns will also be the most dominant stress patterns under 2050 conditions. Future frequencies of low drought stress were reduced by ca. 15%, and those of severe water deficit during grain filling increased from 18% to 25%. Despite this, effects of elevated CO2 on crop growth moderated detrimental effects of climate change on yield. Increasing anthesis-silking synchrony had the greatest effect on yield in low drought-stress seasonal patterns, whereas earlier maturity had the greatest effect in crops exposed to severe early-terminal drought stress. Segregating drought-stress patterns into key groups allowed greater insight into the effects of trait perturbation on crop yield under different weather conditions. We demonstrate that for crops exposed to the same drought-stress pattern, trait perturbation under current climates will have a similar impact on yield as that expected in future, even though the frequencies of severe drought stress will increase in future. These results have important ramifications for breeding of maize and have implications for studies examining genetic and physiological crop responses to environmental stresses.

Every year thousands of experiments are conducted using plants grown under more-or-less controlled environmental conditions. The aim of many such experiments is to compare the phenotype of different species or genotypes in a specific environment, or to study plant performance under a range of suboptimal conditions. Our paper aims to bring together the minimum knowledge necessary for a plant biologist to set up such experiments and apply the environmental conditions that are appropriate to answer the questions of interest. We first focus on the basic choices that have to be made with regard to the experimental setup (e.g. where are the plants grown; what rooting medium; what pot size). Second, we present practical considerations concerning the number of plants that have to be analysed considering the variability in plant material and the required precision. Third, we discuss eight of the most important environmental factors for plant growth (light quantity, light quality, CO2, nutrients, air humidity, water, temperature and salinity); what critical issues should be taken into account to ensure proper growth conditions in controlled environments and which specific aspects need attention if plants are challenged with a certain a-biotic stress factor. Finally, we propose a simple checklist that could be used for tracking and reporting experimental conditions.