Combined high leaf hydraulic safety and efficiency provides drought tolerance in Caragana species adapted to low mean annual precipitation

Abstract

Clarifying the coordination of leaf hydraulic traits with gas exchange across closely-related species adapted to varying rainfall can provide insights into plant habitat distribution and drought adaptation. The leaf hydraulic conductance (K leaf), stomatal conductance (g s), net assimilation (A), vein embolism and abscisic acid (ABA) concentration during dehydration were quantified, as well as pressure-volume curve traits and vein anatomy in 10 Caragana species adapted to a range of mean annual precipitation (MAP) conditions and growing in a common garden. We found a positive correlation between Ψ leaf at 50% loss of K leaf (K leaf P 50) and maximum K leaf (K leaf-max) across species. Species from low-MAP environments exhibited more negative K leaf P 50 and turgor loss point, and higher K leaf-max and leaf-specific capacity at full turgor, along with higher vein density and midrib xylem per leaf area, and a higher ratio of K leaf-max : maximum g s. Tighter stomatal control mediated by higher ABA accumulation during dehydration in these species resulted in an increase in hydraulic safety and intrinsic water use efficiency (WUE i) during drought. Our results suggest that high hydraulic safety and efficiency combined with greater stomatal sensitivity triggered by ABA production and leading to greater WUE i provides drought tolerance in Caragana species adapted to low-MAP environments.

Leaf hydraulic safety margin and safety–efficiency trade-off across angiosperm woody species

“…Interestingly, our result also showed that arid species had higher K leaf at a given P50 leaf than humid species. This result partially supported a recent study about interspecific variations in leaf hydraulic traits of 10 Caragana species from a range of rainfall environments, which indicates that high K leaf plays a role for species adapted to low rainfall habitats because high leaf hydraulic efficiency may match the requirement of high transpiration caused by high vapour pressure deficit and protect leaves from overheating during drought conditions [41]. Therefore, shifts of the hydraulic safety-efficiency trade-off across different water environments may provide a way to elucidate plants' hydraulic adaptation to drought.…”

Ethylene, not ABA, is closely linked to the recovery of gas exchange after drought in four Caragana species

“…Here, our results showed that 71 and 80% loss of leaf hydraulic conductance (PLC) occurred at −3.2 MPa in two isohydric species and 40% and 44% PLC at −3.2 MPa and 88% and 82% PLC at −6.0 MPa in the two anisohydric species, respectively, suggesting that leaf xylem conduit embolism occurred during dehydration in all species. Indeed, the results from the optical method also showed that discrete embolisms propagate in the midrib at ψ leaf reaching approximately −4.0 MPa in six Caragana species, including two C. intermedia and C. microphylla studied here (Yao et al, 2020). Therefore, we proposed that hydraulic impairment may be a potential candidate for explaining the slow recovery of g s after the release of drought (Creek et al, 2018; Skelton et al, 2017).…”

“…K leaf P 50 is considered to be important in influencing species distribution in environments across water availability gradients at local and global scales (Blackman, Brodribb, & Jordan, 2012; Blackman et al, 2014; Nardini & Luglio, 2014; Yao et al, 2020). Our findings in this study revealed that two Caragana species with anisohydric traits have a stronger ability to resist hydraulic loss (more negative K leaf P 50 ) than two Caragana species with isohydric traits.…”

“…When plants experience soil drought, stomatal closure is a plant's first response to limit transpiration (Bartlett, Klein, Jansen, Choat, & Sack, 2017; Dayer, José, Dai, Régis, & Gambetta, 2020; Trueba et al, 2019) to maintain relatively high leaf water potentials (Scoffoni & Sack, 2017) and thus to avoid hydraulic failure of their hydraulic transportation system (Brodribb & McAdam, 2013; Brodribb, McAdam, Jordan, & Martins, 2014; Kumagai & Porporato, 2012; Nolan et al, 2017; Trueba et al, 2019; Yao et al, 2020). Across species, this regulation of water status by stomata has been characterized as a continuum of behaviours from isohydric to anisohydric (Brodribb & McAdam, 2013; Brodribb et al, 2014; Fu & Meinzer, 2018; X. Li et al, 2019; Meinzer et al, 2016; Nolan et al, 2017), which, in turn, are closely driven by abscisic acid (ABA) dynamics (Brodribb & McAdam, 2013, Brodribb et al, 2014;Nolan et al, 2017).…”

Evolution of stomatal closure to optimize water‐use efficiency in response to dehydration in ferns and seed plants

“…Plants invest high amounts of energy to build a safe and effective water transport system (mainly comprised of the vascular bundles) (Brodribb et al, 2017;Waseem et al, 2021). Furthermore, plants have evolved a fully functional signalling network for the optimal adjustment of stomatal aperture, aiming to regulate water-use efficiency (WUE) (Xiao et al, 2018), such that it may be maximal under a wide range of environmental conditions (Cowan & Farquhar, 1977;Brodribb et al, 2009;McAdam & Brodribb, 2012;Yao et al, 2021b).…”