The Causes of Leaf Hydraulic Vulnerability and Its Influence on Gas Exchange in Arabidopsis thaliana

Abstract

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.

How do stomata respond to water status?

“…K decline due to xylem cavitation does not typically begin until stomata are already mostly closed (Bartlett et al ., ; Martin‐StPaul et al ., ). Hydraulic conductance outside the leaf xylem ( K ox ) apparently declines with dehydration before turgor loss, if measured by the evaporative flux method (Hernandez‐Santana et al ., ; Scoffoni et al ., , ), although leaf hydraulic conductance ( K leaf ) measured by rehydration kinetics methods generally does not show such an effect (Brodribb et al ., , ; Skelton et al ., ). The mechanism of putative K ox decline with dehydration is unknown, and may involve effects of ABA on aquaporin function (Shatil‐Cohen et al ., ; Pantin et al ., 2013a).…”

“…A thorough quantitative understanding of hydroactive feedback is not possible until these factors are characterized in detail. The importance of leaf and plant anatomy in stomatal function also has been highlighted by the discovery of fundamental differences in stomatal function between major taxonomic groups as a result of differences in stomatal anatomy (Franks & Farquhar, 2007;Brodribb & McAdam, 2011), and by growing awareness of the impact of leaf hydraulics and capacitance on stomata (Buckley et al, 2011;Deans et al, 2017;Scoffoni et al, 2018). These insights need to be further developed and extended across diverse taxa.…”

Linking water relations and hydraulics with photosynthesis

“…The response of K leaf to declining Ψ leaf was thought to be only due to xylem cavitation events affecting K x (Brodribb and Holbrook, ). However, in recent years, leaf shrinkage and changes in membrane permeability with dehydration have been related to K ox reduction, which nowadays is suspected to be the main driver of K leaf decline under water stress (Trifilo et al ., ; Scoffoni et al ., , ). The coordination between K leaf and g s has been widely studied in order to establish if hydraulic decline triggers stomatal closure or stomata close in order to prevent further potentially damaging cavitation events (Brodribb and Holbrook, ; Theroux‐Rancourt et al ., ; Flexas et al ., ), i.e.…”

Neither xylem collapse, cavitation, or changing leaf conductance drive stomatal closure in wheat

“…Contribution of leaf hydraulic conductance decline to stomatal conductance decline (F, in %) in wheat. The calculation of the F index was based on the equation from Scoffoni et al ().…”

“…Xylem vulnerability to cavitation has been widely studied and provides a predictive indication of plant tolerance and mortality during drought (Anderegg et al, 2015). However, some studies report declines in K leaf at water potentials insufficient to cause cavitation but before or concomitant with stomatal closure (Brodribb & Holbrook, 2006;Holloway-Phillips & Brodribb, 2011;Scoffoni et al, 2018; Torres-Ruiz, Diaz-Espejo, Perez-Martin, & Hernandez-Santana, 2015;Wang, Du, Huang, Peng, & Xiong, 2018). One possible explanation for this behaviour is xylem wall implosion (i.e., xylem collapse) under negative pressure (Cochard, Froux, Mayr, & Coutand, 2004).…”