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.

(R.S., M. Piques, M.S., Y.G.)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.

SummaryThe 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.

Contents Summary349I.Leaf growth: volume, structures, water and carbon349II.Coupling water and carbon limitations through the Lockhart model?350III.ABA signalling pathway as a hub to coordinate water and carbon relations353IV.Leaf venation: just a two‐way pipe network?354V.Leaf ontogeny orchestrates the actors involved in the control of leaf growth355VI.The growing leaf in a changing world360VII.Conclusion361Acknowledgements362References362 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 CO2, low light, high temperature and drought.

Leaf expansion is the central process by which plants colonize space, allowing energy capture and carbon acquisition. Water and carbon emerge as main limiting factors of leaf expansion, but the literature remains controversial about their respective contributions. Here, we tested the hypothesis that the importance of hydraulics and metabolics is organized according to both dark/light fluctuations and leaf ontogeny. For this purpose, we established the developmental pattern of individual leaf expansion during days and nights in the model plant Arabidopsis (Arabidopsis thaliana). Under control conditions, decreases in leaf expansion were observed at night immediately after emergence, when starch reserves were lowest. These nocturnal decreases were strongly exaggerated in a set of starch mutants, consistent with an early carbon limitation. However, low-light treatment of wild-type plants had no influence on these early decreases, implying that expansion can be uncoupled from changes in carbon availability. From 4 d after leaf emergence onward, decreases of leaf expansion were observed in the daytime. Using mutants impaired in stomatal control of transpiration as well as plants grown under soil water deficit or high air humidity, we gathered evidence that these diurnal decreases were the signature of a hydraulic limitation that gradually set up as the leaf developed. Changes in leaf turgor were consistent with this pattern. It is concluded that during the course of leaf ontogeny, the predominant control of leaf expansion switches from metabolics to hydraulics. We suggest that the leaf is better armed to buffer variations in the former than in the latter.

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 CO 2 that feeds daytime photosynthesis. Here, we considered the reduction in transpiration rate at night (E n ) as a possible strategy to limit water use without altering growth. For this purpose, we carried out a genetic analysis for E n 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 E n 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 E n . Interestingly, four of them colocalized with QTLs for TE. Moreover, genotypes with favorable alleles on these common QTLs exhibited reduced E n 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.night transpiration | transpiration efficiency | growth | stomata | QTL

High temperature (HT) is a major limiting factor for plant productivity. Because some responses to HT, notably hyponasty, resemble those encountered in low light (LL), we hypothesized that plant responses to HT are under the control of carbon balance. We analysed the interactive effects of HT and irradiance level on hyponasty and a set of traits related to plant growth in natural accessions of Arabidopsis thaliana and mutants affected in heat dissipation through transpiration (NCED6-OE, ost2) and starch metabolism (pgm). HT induced hyponasty, reduced plant growth and modified leaf structure. LL worsened the effects of HT, while increasing light restored trait values close to levels observed at control temperature. Leaf temperature per se did not play a major role in the observed responses. By contrast, a major role of carbon balance was supported by hyponastic growth of pgm, as well as morphological, physiological (photosynthesis, sugar and starch contents) and transcriptional data. Carbon balance could be a common sensor of HT and LL, leading to responses specific of the shade avoidance syndrome. Hyponasty and associated changes in plant traits could be key traits conditioning plant performance under competition for light, particularly in warm environments.

Plant water loss and CO2 uptake are controlled by valve-like structures on the leaf surface known as stomata. Stomatal aperture is regulated by hormonal and environmental signals. We show here that stomatal sensitivity to the drought hormone abscisic acid (ABA) is acquired during leaf development by exposure to an increasingly dryer atmosphere in the rosette plant Arabidopsis. Young leaves, which develop in the center of the rosette, do not close in response to ABA. As the leaves increase in size, they are naturally exposed to increasingly dry air as a consequence of the spatial arrangement of the leaves, and this triggers the acquisition of ABA sensitivity. Interestingly, stomatal ABA sensitivity in young leaves is rapidly restored upon water stress. These findings shed new light on how plant architecture and stomatal physiology have coevolved to optimize carbon gain against water loss in stressing environments.