Optimal balancing of xylem efficiency and safety explains plant vulnerability to drought

Franklin, O. ORCID: https://orcid.org/0000-0002-0376-4140, Fransson, P., Hofhansl, F. ORCID: https://orcid.org/0000-0003-0073-0946, & Joshi, J. (2022). Optimal balancing of xylem efficiency and safety explains plant vulnerability to drought. bioRxiv (preprint) 10.1101/2022.05.16.491812.

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Abstract

In vast areas of the world, the growth of forests and vegetation is water-limited and plant survival depends on the ability to avoid catastrophic hydraulic failure. Therefore, it is remarkable that plants take high hydraulic risks by operating at water potentials (ψ) that induce partial failure of the water conduits (xylem). Here we present an eco-evolutionary optimality principle for xylem conduit design that explains this phenomenon. Based on the hypothesis that conductive efficiency and safety are optimally co-adapted to the environment, we derive a simple relationship between the intrinsic tolerance to negative water potential (ψ50) and the environmentally dependent minimum xylem, ψmin. This relationship is constrained by a physiological tradeoff between xylem conductivity and safety, which is relatively strong at the level of individual conduits although it may be weak at the whole sapwood level. The model explains observed variation in ψ50 both across a large number of species, and along the xylem path in two species. The larger hydraulic safety margin in gymnosperms compared to angiosperms is explained as an adaptation to the gymnosperms' lower capacity to recover from conductivity loss. The constant xylem safety factor provides a powerful principle for simplifying and improving plant and vegetation models.

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