Angélique Christophe

Arabidopsis Plants Acclimate to Water Deficit at Low Cost through Changes of Carbon Usage: An Integrated Perspective Using Growth, Metabolite, Enzyme, and Gene Expression Analysis

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.

A model-based analysis of the dynamics of carbon balance at the whole-plant level in Arabidopsis thaliana

Arabidopsis thaliana (L.) Heynh. is used as a model plant in many research projects. However, few models simulate its growth at the whole-plant scale. The present study describes the first model of Arabidopsis growth integrating organogenesis, morphogenesis and carbon-partitioning processes for aerial and subterranean parts of the plant throughout its development. The objective was to analyse competition among sinks as they emerge from patterns of plant structural development. The model was adapted from the GreenLab model and was used to estimate organ sink strengths by optimisation against biomass measurements. Dry biomass production was calculated by a radiation use efficiency-based approach. Organogenesis processes were parameterised based on experimental data. The potential of this model for growth analysis was assessed using the Columbia ecotype, which was grown in standard environmental conditions. Three phases were observed in the overall time course of trophic competition within the plant. In the vegetative phase, no competition was observed. In the reproductive phase, competition increased with a strong increase when lateral inflorescences developed. Roots and internodes and structures bearing siliques were strong sinks and had a similar impact on competition. The application of the GreenLab model to the growth analysis of A. thaliana provides new insights into source-sink relationships as functions of phenology and morphogenesis.

Influence of intra-shoot trophic competition on shoot development in two grapevine cultivars (Vitis vinifera)

The effect of trophic competition between vegetative sources and reproductive sinks on grapevine (Vitis vinifera L.) shoot development was analyzed. Two international cultivars (Grenache N and Syrah) grown in pots, which were well watered, were studied. A large range of trophic competition levels was obtained by modifying the cluster loads per plant. An analytical breakdown of the branching system was used to analyze the effects of trophic competition. Phytomer production on the primary axis and the probability and timing of axillary budburst were not affected by trophic competition. However, the duration of development and leaf production rate for secondary axes were both significantly affected. The impact of trophic competition differed within the P0-P1-P2 architectural module, locally within the shoot and between cultivars. Trophic competition reduced the organogenesis of secondary axes most strongly close to clusters, on P1-P2 phytomers and in Grenache N. Based on these results, a modeling approach simulating sink strength variation and the local effects of sink proximity would be more relevant than a model considering only development as a function of thermal time or the global distribution of available biomass.

Comparison of three approaches to model grapevine organogenesis in conditions of fluctuating temperature, solar radiation and soil water content.

BACKGROUND AND AIMS There is increasing interest in the development of plant growth models representing the complex system of interactions between the different determinants of plant development. These approaches are particularly relevant for grapevine organogenesis, which is a highly plastic process dependent on temperature, solar radiation, soil water deficit and trophic competition. METHODS The extent to which three plant growth models were able to deal with the observed plasticity of axis organogenesis was assessed. In the first model, axis organogenesis was dependent solely on temperature, through thermal time. In the second model, axis organogenesis was modelled through functional relationships linking meristem activity and trophic competition. In the last model, the rate of phytomer appearence on each axis was modelled as a function of both the trophic status of the plant and the direct effect of soil water content on potential meristem activity. KEY RESULTS The model including relationships between trophic competition and meristem behaviour involved a decrease in the root mean squared error (RMSE) for the simulations of organogenesis by a factor nine compared with the thermal time-based model. Compared with the model in which axis organogenesis was driven only by trophic competition, the implementation of relationships between water deficit and meristem behaviour improved organogenesis simulation results, resulting in a three times divided RMSE. The resulting model can be seen as a first attempt to build a comprehensive complete plant growth model simulating the development of the whole plant in fluctuating conditions of temperature, solar radiation and soil water content. CONCLUSIONS We propose a new hypothesis concerning the effects of the different determinants of axis organogenesis. The rate of phytomer appearance according to thermal time was strongly affected by the plant trophic status and soil water deficit. Furthermore, the decrease in meristem activity when soil water is depleted does not result from source/sink imbalances.

Quantifying physiological determinants of genetic variation for yield potential in sunflower. SUNFLO: a model-based analysis

Present work focussed on improving the description of organogenesis, morphogenesis and metabolism in a biophysical plant model (SUNFLO) applied to sunflower (Helianthus annuus L.). This first version of the model is designed for potential growth conditions without any abiotic or biotic stresses. A greenhouse experiment was conducted to identify and estimate the phenotypic traits involved in plant productivity variability of 26 sunflower genotypes. The ability of SUNFLO to discriminate the genotypes was tested on previous results of a field survey aimed at evaluating the genetic progress since 1960. Plants were phenotyped in four directions; phenology, architecture, photosynthesis and biomass allocation. Twelve genotypic parameters were chosen to account for the phenotypic variability. SUNFLO was built to evaluate their respective contribution to the variability of yield potential. A large phenotypic variability was found for all genotypic parameters. SUNFLO was able to account for 80% of observed variability in yield potential and to analyse the phenotypic variability of complex plant traits such as light interception efficiency or seed yield. It suggested that several ways are possible to reach high yields in sunflower. Unlike classical statistical analysis, this modelling approach highlights some efficient parameter combinations used by the most productive genotypes. The next steps will be to evaluate the genetic determinisms of the genotypic parameters.

Reduced nighttime transpiration is a relevant breeding target for high water-use efficiency in grapevine

Significance Breeding crops with more biomass produced per drop of water transpired is a key challenge in the context of climate change. However, the tight coupling between transpiration and carbon assimilation during the day makes it challenging to decrease water loss without altering photosynthesis and reducing crop yield. We tested whether reducing transpiration at night when photosynthesis is inactive could substantially reduce water loss without altering growth—a hypothesis that, to our knowledge, has never been genetically addressed in any species. By studying a whole progeny in grapevine, a major crop for drought-prone areas, we identified genomic regions where selection could be operated to reduce transpiration at night and maintain growth. This opens new horizons for breeding crops with higher water-use efficiency. Increasing water scarcity challenges crop sustainability in many regions. As a consequence, the enhancement of transpiration efficiency (TE)—that is, the biomass produced per unit of water transpired—has become crucial in breeding programs. This could be achieved by reducing plant transpiration through a better closure of the stomatal pores at the leaf surface. However, this strategy generally also lowers growth, as stomatal opening is necessary for the capture of atmospheric CO2 that feeds daytime photosynthesis. Here, we considered the reduction in transpiration rate at night (En) as a possible strategy to limit water use without altering growth. For this purpose, we carried out a genetic analysis for En and TE in grapevine, a major crop in drought-prone areas. Using recently developed phenotyping facilities, potted plants of a cross between Syrah and Grenache cultivars were screened for 2 y under well-watered and moderate soil water deficit scenarios. High genetic variability was found for En under both scenarios and was primarily associated with residual diffusion through the stomata. Five quantitative trait loci (QTLs) were detected that underlay genetic variability in En. Interestingly, four of them colocalized with QTLs for TE. Moreover, genotypes with favorable alleles on these common QTLs exhibited reduced En without altered growth. These results demonstrate the interest of breeding grapevine for lower water loss at night and pave the way to breeding other crops with this underexploited trait for higher TE.

Phenotypic plasticity toward water regime: response of leaf growth and underlying candidate genes in Populus

Phenotypic plasticity is considered as an important mechanism for plants to cope with environmental challenges. Leaf growth is one of the first macroscopic processes to be impacted by modification of soil water availability. In this study, we intended to analyze and compare plasticity at different scales. We examined the differential effect of water regime (optimal, moderate water deprivation and recovery) on growth and on the expression of candidate genes in leaves of different growth stages. Candidates were selected to assess components of growth response: abscisic acid signaling, water transport, cell wall modification and stomatal development signaling network. At the tree scale, the four studied poplar hybrids responded similarly to water regime. Meanwhile, leaf growth response was under genotype × environment interaction. Patterns of candidate gene expression enriched our knowledge about their functionality in poplars. For most candidates, transcript levels were strongly structured according to leaf growth performance while response to water regime was clearly dependent on genotype. The use of an index of plasticity revealed that the magnitude of the response was higher for gene expression than for macroscopic traits. In addition, the ranking of poplar genotypes for macroscopic traits well paralleled the one for gene expression.

Nitrogen supply controls vegetative growth, biomass and nitrogen allocation for grapevine (cv. Shiraz) grown in pots

Maintaining grapevine productivity with limited inputs is crucial in Mediterranean areas. Apart from water, nitrogen (N) is also an important limiting factor in grape growing. The effects of N deficiency on grapevine growth were investigated in this study. Two-year-old Vitis vinifera L.cv. Shiraz plants grafted on 110 R were grown in pots placed outside and exposed to various N supplies (0, 0.6, 1.2, 2.4 and 12g plant-1) under well-watered conditions. At veraison, plants were harvested and organs separately dried, weighed and analysed for N. During plant growth, the length of the primary and secondary axes and the number of leaves on them were recorded. The N content of leaves was also analysed at three phenological stages (flowering, bunch closure and veraison). All growth processes were inhibited by N deficiency in an intensity-dependent manner. Quantitative relationships with N supply were established. Vegetative growth responded negatively to N stress when comparing control N supply with no N supply: primary axis elongation (-61%), leaf emergence on the primary axis (-47%), leaf emergence on the secondary axis (-94%) and lamina area expansion (-45%). Significant differences on the plant N status were observed from flowering onwards which might be useful for managing fertilisation.

Abscisic acid down-regulates hydraulic conductance of grapevine leaves in isohydric genotypes only

Abscisic acid reduces the water transport capacity of grapevine leaves, most notably in isohydric genotypes. Plants evolved different strategies to cope with water stress. While isohydric species maintain their midday leaf water potential (ΨM) under soil water deficit by closing their stomata, anisohydric species maintain higher stomatal aperture and exhibit substantial reductions in ΨM. It was hypothesized that isohydry is related to a locally higher sensitivity of stomata to the drought-hormone abscisic acid (ABA). Interestingly, recent lines of evidence in Arabidopsis (Arabidopsis thaliana) suggested that stomatal responsiveness is also controlled by an ABA action on leaf water supply upstream from stomata. Here, we tested the possibility in grapevine (Vitis vinifera) that different genotypes ranging from near isohydric to more anisohydric may have different sensitivities in these ABA responses. Measurements on whole plants in drought conditions were combined with assays on detached leaves fed with ABA. Two different methods consistently showed that leaf hydraulic conductance (Kleaf) was down-regulated by exogenous ABA, with strong variations depending on the genotype. Importantly, variation between isohydry and anisohydry correlated with Kleaf sensitivity to ABA, with Kleaf in the most anisohydric genotypes being unresponsive to the hormone. We propose that the observed response of Kleaf to ABA may be part of the overall ABA regulation of leaf water status.

A Stochastic Growth Model of Grapevine with Full Interaction Between Environment, Trophic Competition and Plant Development

Grapevine development is mainly determined by environmental factors whose effects are modulated by its complex topological structure. The trophic relationships between all the organs of the different axes appear to be the main underlying process which drive axis organogenesis in fluctuating environment. A new modelling approach is proposed based on GreenLab formalism in which axis organogenesis is controlled by stochastic processes according to trophic competition between the different axes. In this model, a water budget was also implemented to account for the effects of water depletion. The model was validated at organ and axis scales on a large range of environmental conditions in terms of photosynthetic active radiation, temperature and soil water supply. The efficiency of the model to simulate plant development at a detailed scale proved its ability to further analyse of the retroactions between plant development and the different environmental variables in order to improve crop management.