Weak tradeoff between xylem hydraulic efficiency and safety: Climatic seasonality matters

Authors: LIU, HUI - Chinese Academy Of Sciences; Gleason, Sean; HE, PENGCHENG - Chinese Academy Of Sciences; YE, QING - Chinese Academy Of Sciences

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/4/2020
Publication Date: 10/15/2020
Citation: Liu, H., Gleason, S.M., He, P., Ye, Q. 2020. Weak tradeoff between xylem hydraulic efficiency and safety: Climatic seasonality matters. New Phytologist. 229(3):1440-1452. https://doi.org/10.1111/nph.16940.
DOI: https://doi.org/10.1111/nph.16940

Interpretive Summary: The capacity of plant tissues to transport water (hereafter "efficiency") and the susceptibility of these tissues to damage (hereafter "safety") are key traits conferring growth in all vascular plant species, especially during drought. However, it is currently unknown what the proximal causes of safety and efficiency are, as well as whether or not these two traits should tradeoff against one another. The degree to which these traits can be modified independently of one another, either via artificial selection or gene editing, depends directly on whether or not a tradeoff between these traits exists. For example, although improvement of safety and efficiency would both be good things for crop plants, is it not well understood if the improvement of one of these traits would necessarily result in poorer performance in the other trait. With aim to understand this we looked at variation in these traits across species spanning a broad range of climate and soils. We hypothesized that if developmental constraints forced a tradeoff between safety and efficiency we should then observe departure from the expected tradeoff when climate conditions favor one trait over the other, i.e., when soil and/or atmospheric conditions allow for the maximization of both traits. Although particular climate conditions were associated with slightly stronger as well as slightly weaker correlation coefficients, we found that natural selection has resulted in nearly independent variation in each of these traits, suggesting that breeding and gene editing efforts should be effective in improving both of these traits simultaneously.

Technical Abstract: A classic theory proposes that plant xylem cannot be both highly efficient and resistant to embolism (safe), and therefore a hydraulic efficiency-safety tradeoff should exist. However, many species exhibit both low hydraulic efficiency and low safety and fall outside of the expected tradeoff space. It remains unclear under what environmental conditions these species are able to maintain competitive fitness. We compiled hydraulic efficiency and safety traits for 682 observations of 499 woody species from 178 sites, and measured the distance each species was positioned away from the proposed tradeoff space, represented by a standardized major axis model. For angiosperms, species from sites with low precipitation (P), high vapour pressure deficit (VPD) and high solar radiation (SR) during the wet season were located close to the tradeoff space, whereas geographic range and niche breadth across global localities were not associated with distance from the tradeoff. For gymnosperms, species with wide geographic ranges, from sites with high VPD, high SR, and low P during the wet season exhibited higher efficiency and safety than species from the opposite environments. Climatic seasonality and geographic range provide the ecological context for the physiologically unexplained tradeoff, which could help predict the distribution of species in the face of climate change.