Evolutionary relationships between drought-related traits and climate shape large hydraulic safety margins in western North American oaks - INRAE - Institut national de recherche pour l’agriculture, l’alimentation et l’environnement Access content directly
Journal Articles Proceedings of the National Academy of Sciences of the United States of America Year : 2021

Evolutionary relationships between drought-related traits and climate shape large hydraulic safety margins in western North American oaks

Abstract

Significance A fundamental association between sustained water transport and downstream tissue survival should select for xylem that avoids embolism in long-lived woody plants. Previous studies suggest that long-vessel species, such as oaks and vines, are more susceptible to drought-induced loss of function than other species. We show that western North American oaks—even those occurring in wet temperate forest—possess xylem capable of tolerating substantial water stress. Evolutionary relationships between drought tolerance traits combined with plant–climate interactions yield positive hydraulic safety margins in oaks from diverse habitats, demonstrating that these key species are not yet on the verge of hydraulically mediated loss of function. Quantifying physical tolerance limits to desiccation is imperative for predicting ecological consequences of future droughts. Quantitative knowledge of xylem physical tolerance limits to dehydration is essential to understanding plant drought tolerance but is lacking in many long-vessel angiosperms. We examine the hypothesis that a fundamental association between sustained xylem water transport and downstream tissue function should select for xylem that avoids embolism in long-vessel trees by quantifying xylem capacity to withstand air entry of western North American oaks (Quercus spp.). Optical visualization showed that 50% of embolism occurs at water potentials below −2.7 MPa in all 19 species, and −6.6 MPa in the most resistant species. By mapping the evolution of xylem vulnerability to embolism onto a fossil-dated phylogeny of the western North American oaks, we found large differences between clades (sections) while closely related species within each clade vary little in their capacity to withstand air entry. Phylogenetic conservatism in xylem physical tolerance, together with a significant correlation between species distributions along rainfall gradients and their dehydration tolerance, suggests that closely related species occupy similar climatic niches and that species' geographic ranges may have shifted along aridity gradients in accordance with their physical tolerance. Such trends, coupled with evolutionary associations between capacity to withstand xylem embolism and other hydraulic-related traits, yield wide margins of safety against embolism in oaks from diverse habitats. Evolved responses of the vascular system to aridity support the embolism avoidance hypothesis and reveal the importance of quantifying plant capacity to withstand xylem embolism for understanding function and biogeography of some of the Northern Hemisphere’s most ecologically and economically important plants.
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hal-03610298 , version 1 (16-03-2022)

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Robert Skelton, Leander Anderegg, Jessica Diaz, Matthew Kling, Prahlad Papper, et al.. Evolutionary relationships between drought-related traits and climate shape large hydraulic safety margins in western North American oaks. Proceedings of the National Academy of Sciences of the United States of America, 2021, 118 (10), ⟨10.1073/pnas.2008987118⟩. ⟨hal-03610298⟩
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