Plant resistance to drought depends on timely stomatal closure

Abstract

Stomata play a significant role in the Earth's water and carbon cycles, by regulating gaseous exchanges between the plant and the atmosphere. Under drought conditions, stomatal control of transpiration has long been thought to be closely coordinated with the decrease in hydraulic capacity (hydraulic failure due to xylem embolism). We tested this hypothesis by coupling a meta-analysis of functional traits related to the stomatal response to drought and embolism resistance with simulations from a soil-plant hydraulic model. We report here a previously unreported phenomenon: the existence of an absolute limit by which stomata closure must occur to avoid rapid death in drought conditions. The water potential causing stomatal closure and the xylem pressure at the onset of embolism formation were equal for only a small number of species, and the difference between these two traits (i.e. safety margins) increased continuously with increasing embolism resistance. Our findings demonstrate the need to revise current views about the functional coordination between stomata and hydraulic traits and provide a mechanistic framework for modeling plant mortality under drought conditions.

Over‐accumulation of abscisic acid in transgenic tomato plants increases the risk of hydraulic failure

“…Daily simulated patterns of stomatal conductance ( g s ) and loss of hydraulic conductivity (PLC) during the progression of a simulated soil drought (SurEau model; Martin‐StPaul et al, ). (a) Declining g s and increasing PLC modelled for both wild type control (medium dashed and solid red line, respectively) and 9‐ cis ‐epoxycarotenoid dioxygenase overexpressing transformant (sp12; medium dashed and solid green line, respectively).…”

“…A simplified discrete‐time soil–plant hydraulic model (SurEau; Martin‐StPaul, Delzon, & Cochard, ) was used to (a) simulate for each line the temporal decline in g s and the increasing loss of hydraulic conductivity during the progression of a simulated soil drought and (b) to estimate the sensitivity of the loss of hydraulic conductivity dynamics to a change in either g s or Ψ 50 . For this latter objective, simulations were performed by modelling the PLC dynamics of the wild type line using the g s or Ψ 50 values of the sp12 line.…”

Forests, atmospheric water and an uncertain future: the new biology of the global water cycle

“…The control of these pores determines the exchange of gases, including water vapour and carbon dioxide, between the plants' intercellular space and the external atmosphere. The behaviour of stomatal pores is assumed to optimize carbon gain (growth), depending on environmental conditions including access to water and the risks that arise from drought, but our understanding of these relationships remains a "work in progress" (Klein 2014;Martin-StPaul et al 2017;Matthews et al 2017;Meinzer et al 2017). Furthermore, trees capture nutrients by drawing in soil water, thus increased transpiration rates can be a response to low nutrient environments (Matimati et al 2013;Huang et al 2017).…”

Coordination and trade‐offs between leaf and stem hydraulic traits and stomatal regulation along a spectrum of isohydry to anisohydry

“…At the stem level, the degree of iso/anisohydry is associated with the degree of embolism resistance (Fu & Meinzer, ; Martínez‐Vilalta et al, ). At the leaf level, the degree of iso/anisohydry is associated with the turgor loss point (Ψ TLP ; Fu & Meinzer, ; Martin‐StPaul, Delzon, & Cochard, ; Meinzer et al, ), foliar abscisic acid dynamics during dehydration (McAdam & Brodribb, ; Nolan et al, ), the kinetics of light‐induced stomatal opening and activation of photosynthesis (Meinzer et al, ), and the sensitivity of intrinsic water‐use efficiency to environmental change (Yi et al, ). Coordination of stomatal control of plant water potential with stem embolism resistance leads to variation in the difference between stem water potential and the water potential at which 50% of hydraulic conductivity is lost (i.e., the hydraulic safety margin) along a spectrum of iso/anisohydry (Skelton et al, ).…”