Abstract
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.
Highlights
Leaf expansion is the central process by which plants colonize space, allowing energy capture and carbon acquisition
We aimed to discover the relative contributions of water and carbon to the control of growth with respect to leaf ontogeny in the model plant Arabidopsis (Arabidopsis thaliana)
We focused on a developmental window encompassing the first half of leaf expansion after emergence, a period during which relative and absolute leaf expansion are successively maximum (Supplemental Fig. S1) and strongly contribute to final leaf area
Summary
Leaf expansion is the central process by which plants colonize space, allowing energy capture and carbon acquisition. 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. It is one of the first plant functions affected by environmental stresses such as water deficit (Hsiao, 1973), making it a key target for identifying tolerant genotypes and species (Tardieu and Tuberosa, 2010) To this aim, understanding the processes dominating the control of leaf expansion is a crucial step. Among the multiplicity of factors involved in leaf expansion, two major limitations emerge: a biophysical control mainly linked to water fluxes to growing cells, and a metabolic control linked to the supply of carbohydrates (Dale, 1988; Walter et al, 2009). This turnover of starch reserves is thought to be a major integrator in the regulation of growth (Sulpice et al, 2009)
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