The Causes of Leaf Hydraulic Vulnerability and Its Influence on Gas Exchange in Arabidopsis thaliana1[OPEN]

Declines in leaf outside-xylem hydraulic conductance prior to turgor loss point contribute strongly to stomatal closure, and improve performance, survival and efficient water use during drought. The influence of the dynamics of leaf hydraulic conductance ( K leaf ) diurnally and during dehydration on stomatal conductance and photosynthesis remains unclear. Using the model species Arabidopsis ( Arabidopsis thaliana ecotype Columbia-0), we applied a multitiered approach including physiological measurements, high-resolution x-ray microcomputed tomography, and modeling at a range of scales to characterize (1) K leaf decline during dehydration; (2) its basis in the hydraulic conductances of leaf xylem and outside-xylem pathways ( K ox ); (3) the dependence of its dynamics on irradiance; (4) its impact on diurnal patterns of stomatal conductance and photosynthetic rate; and (5) its influence on gas exchange and survival under simulated drought regimes. Arabidopsis leaves showed strong vulnerability to dehydration diurnally in both gas exchange and hydraulic conductance, despite lack of xylem embolism or conduit collapse above the turgor loss point, indicating a pronounced sensitivity of K ox to dehydration. K leaf increased under higher irradiance in well-hydrated leaves across the full range of water potential, but no shift in K leaf vulnerability was observed. Modeling indicated that responses to dehydration and irradiance are likely attributable to changes in membrane permeability and that a dynamic K ox would contribute strongly to stomatal closure, improving performance, survival, and efficient water use during drought. These findings for Columbia-0 provide a baseline for assessing variation across genotypes in hydraulic traits and their influence on gas exchange during dehydration.