Abstract
Plants are constantly facing rapid changes in evaporative demand and soil water content, which affect their water status and growth. In apparent contradiction to a hydraulic hypothesis, leaf elongation rate (LER) declined in the morning and recovered upon soil rehydration considerably quicker than transpiration rate and leaf water potential (typical half-times of 30 min versus 1-2 h). The morning decline of LER began at very low light and transpiration and closely followed the stomatal opening of leaves receiving direct light, which represent a small fraction of leaf area. A simulation model in maize (Zea mays) suggests that these findings are still compatible with a hydraulic hypothesis. The small water flux linked to stomatal aperture would be sufficient to decrease water potentials of the xylem and growing tissues, thereby causing a rapid decline of simulated LER, while the simulated water potential of mature tissues declines more slowly due to a high hydraulic capacitance. The model also captured growth patterns in the evening or upon soil rehydration. Changes in plant hydraulic conductance partly counteracted those of transpiration. Root hydraulic conductivity increased continuously in the morning, consistent with the transcript abundance of Zea maize Plasma Membrane Intrinsic Protein aquaporins. Transgenic lines underproducing abscisic acid, with lower hydraulic conductivity and higher stomatal conductance, had a LER declining more rapidly than wild-type plants. Whole-genome transcriptome and phosphoproteome analyses suggested that the hydraulic processes proposed here might be associated with other rapidly occurring mechanisms. Overall, the mechanisms and model presented here may be an essential component of drought tolerance in naturally fluctuating evaporative demand and soil moisture.
Highlights
Plants are constantly facing rapid changes in evaporative demand and soil water content, which affect their water status and growth
A total of 1,877 daily time courses of leaf elongation rate (LER) originating from 23 experiments (Supplemental Table S1) were classified into a limited number of patterns in each experiment, according to the evaporative demand and water availability measured on the considered day
The decrease in LER at the transition between day and night was much more rapid than that of transpiration rate, with mean half-times of 0.8 6 0.3 and 2.3 6 0.5 h, respectively, in the mornings of 14 experiments (Supplemental Table S1; Supplemental Fig. S3). It occurred at a time when transpiration rate was still almost negligible (5 6 3 g m22 h21) due to low values of photosynthetic photon flux density (PPFD) and vapor pressure deficit (VPD; 10 6 3 mmol m22 s21 and 0.75 6 0.2 kPa, respectively, over the whole data set)
Summary
Plants are constantly facing rapid changes in evaporative demand and soil water content, which affect their water status and growth. Water movements in the plant are constantly facing boundary conditions that change from low to high offer and demand, leading to rapid oscillations of leaf water status and growth (Hsiao et al, 1970; Ben Haj Salah and Tardieu, 1997; Walter et al, 2009). These rapid changes are artificially avoided in most in-depth analyses. The progress of phenotyping allows one to obtain a large number of time courses of LER, transpiration, and environmental conditions with a time step of minutes (Sadok et al, 2007), thereby making possible the use of this method
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