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

Abstract

SummaryIn 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 ψ.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.

Explaining plant trait variation in response to soil water availability using an optimal height-growth model

“…Maximum sapwood-specific conductivity, K s,max : k l,max increases with K s,max which increases the rate of water transport. However, sapwood with a higher K s,max is also assumed to be less resistant to embolism, consistent with the hypothesis of a hydraulic safety-efficiency trade-off (Liu et al 2019(Liu et al , 2021Franklin et al 2023):…”

“…Another important consideration is that while most analyses of the hydraulic safetyefficiency trade-off, including this analysis, focus on xylem efficiency at the sapwood-level, recent evidence suggests that the trade-off is mediated instead at the individual conduit level (Franklin et al . 2023).…”

“…However, sapwood with a higher K s,max is also assumed to be less resistant to embolism, consistent with the hypothesis of a hydraulic safety-efficiency trade-off (Liu et al . 2019, 2021; Franklin et al . 2023): where P 50 is the xylem pressure at which 50% of conductivity is lost, B hv 1 is the P 50 at the global average of K s,max ( K s,max ,0 ; Table 2) and B hv 2 is the steepness of the relationship between K s,max and P 50 on a log-log scale.…”

“…Another important consideration is that while most analyses of the hydraulic safetyefficiency trade-off, including this analysis, focus on xylem efficiency at the sapwood-level, recent evidence suggests that the trade-off is mediated instead at the individual conduit level (Franklin et al 2023). The implication of this is that the safety-efficiency trade-off may be weaker at the sapwood-level because maximum sapwood-specific conductivity is determined by both the conductivity of an individual conduit (K c ) and the number of conduits, which can vary independently (i.e.…”

Gold perfusion experiments support the multi‐layered, mesoporous nature of intervessel pit membranes in angiosperm xylem

“…2) appears to reflect the nonlinear relationship between embolism resistance and pit membrane thickness (Kaack et al ., 2021). A similar, convex relationship may also suggest that the hydraulic safety and efficiency trade‐off is nonlinear (Gleason et al ., 2016; Franklin et al ., 2023; Pereira et al ., 2023).…”