Abstract
The hydraulic vulnerability segmentation hypothesis proposes that plant branches are more resistant to cavitation than roots, namely, the difference in vulnerability to cavitation between branches and roots is positive (P 50 root - branch > 0). However, it is not clear how this phenomenon can vary along environmental aridity gradients.
We compiled the above hypothesis with 105 woody species from four biomes with increasing aridity, by compiling functional traits related to hydraulic properties and anatomical structures of branches and roots. We investigated the relationships between P 50 root - branch and several environmental factors that are associated with aridity.
We found a positive P 50 root - branch across species, which supported the hydraulic vulnerability segmentation hypothesis, and P 50 root - branch increased significantly with environmental aridity. Branch xylem hydraulic conductivity changed from “more efficient” (e.g., wider conduit, higher hydraulic conductivity) to “safer” (e.g., narrower conduit, more negative P 50) in response to increased aridity, while root xylem hydraulic conductivity remained unchanged across aridity gradients.
Our results demonstrated that hydraulic vulnerability segmentation is more pronounced for species from arid regions. Changes in branch traits may be responsible for hydraulic vulnerability segmentation between branches and roots.
Key-words: cavitation, environment variables, hydraulic conductivity, vulnerability segmentation, xylem anatomy
Introduction
Climate change is currently escalating so rapidly that many woody plants may not be able to adapt the extreme drought caused by the gradual global warming (Brodribb et al ., 2020). A number of previous studies documented an increased risk of forest mortality due to extreme drought events (Klein & Henrik, 2018; Hajek et al ., 2022). Continuous water transport supply from roots to stems and leaves through xylem can be interrupted by cavitation and collapse of conduits during drought (Tyree & Sperry, 1989), which is tightly linked to drought-induced mortality in plants (Choat et al ., 2018). Roots represent the direct interface of a plant to soil water, which is a critical component of plant water transport pathway, and hydraulic failure due to cavitation in the root system may directly lead to plant mortality (Peters et al ., 2020). Branches transport the water absorbed by roots to leaves for continuation of photosynthesis and transpiration. Investigating the coordination and dissonance of plant adaptive traits between aboveground parts (i.e., branches) and underground parts (i.e., roots) is particularly important for better understanding plant survival strategies to climate change (Aleixoet al ., 2019).
The hydraulic vulnerability segmentation hypothesis is a plant adaptive strategy to drought, which suggests that the terminal organs (e.g., leaves and roots) are first to be cavitated, thereby ensuring the hydraulic safety of more expensive organs like trunk and branches (Tyree & Ewers, 1991). Hydraulic vulnerability of xylem can be quantified by xylem pressure inducing 50% loss of hydraulic conductivity (P 50), which reflected plant resistance to drought (Volaire, 2018). Previous studies have examinedP 50 between roots and branches of woody species, and a general finding is that roots are more vulnerable to drought-induced cavitation than branches (i.e.,P 50 root - branch > 0), and extensive cavitation in roots limited water supply in plant hydraulic pathway during drought (Alder et al ., 1996; Johnson et al ., 2018). Investigating the vulnerability segmentation of plants can help to judge whether xylem cavitation is systemic, and whether it would cause a catastrophic and lethal failure of the whole plant water transport system (Schenk et al ., 2008; Wu et al ., 2020). Interestingly, some recent studies employing optical methods found that roots have similar (e.g., Cedrus deodara and Eucalyptus saligna ) (Peters et al ., 2020) or even stronger cavitation resistance than branches (e.g., Olea europaea ) (Rodriguez-Dominguez et al ., 2018). Explanations for these findings include that plant survival during drought would be best served by adaptive xylem integrity where root and branch xylem exhibited similar vulnerabilities, leading to shorter recovery time to roots cavitation and greater investment in new root tissues after being relieved from drought stress (Lamarque et al ., 2018). However, these studies focused on a few species from particular habitats, thus comparisons of hydraulic traits between branches and roots across species covering broad geographical regions are needed, to better understand how resistance to drought is coordinated at the whole plant level.
It has been shown that P 50 varies widely among plant species and is primarily determined by the differences in the xylem structure (Lens et al ., 2022). The more drought-tolerant the plant, the more resistant the xylem to cavitation under negative pressure, and the less likely the xylem conduit walls to implosion under increased negative pressure (Zhao et al ., 2020). Previous studies reported that conduit wall thickness to span ratio (t 2/b 2) is proportional to P 50 as required to avoid wall collapse (Cochard et al ., 2008; Rodriguez-Dominguez et al ., 2018). In addition, the pit area hypothesis (also called ‘rare pit’ hypothesis) proposed that the larger conduits tend to have a greater pitted wall area, which is more vulnerable to cavitation (Hacke et al ., 2017, Mrad et al ., 2018). Therefore, whether roots have anatomical properties that are more vulnerable to cavitation than branches, is the structural basis for exploring the hydraulic vulnerability segmentation between these two organs.
Environmental factors are important driving forces for the variability of plant hydraulic traits. Trueba et al ., (2017) reported that branch P 50 of rainforest species was significantly correlated with elevation and mean annual temperature. In addition, plants from arid regions were found to have narrow vessels or tracheids (Gao et al ., 2021). Meanwhile, vulnerability segmentation between plant organs may shift with environmental factors. For instance, Zhu et al ., (2016) observed that vulnerability segmentation between branches and leaves became less positive and even negative with the increase of environmental aridity. However, it is lack of studies to explore how environmental factors drive the potential vulnerability segmentation between roots and branches, this question deserves a more detailed analysis. Because a better understanding of the linkages between P 50 and environmental factors in different organs could help to synthesize plant adaptive strategies, and more precisely predict their responses to global climate change (Liet al ., 2015).
Here, we compiled a global dataset of 105 woody species (10 species were measured in the present study) from 59 study sites worldwide. We assembled P 50 and K S(specific xylem conductivity per unit of cross-sectional sapwood area) values measured simultaneously in the xylem of branches and roots. In addition, we collected hydraulically weighted mean diameter (D h) andt 2/b 2 values to investigate whether anatomical structures can explain the differences in xylem vulnerability between roots and branches.
We had two hypotheses:
Roots of woody species would have more vulnerable xylem to drought-induced cavitation than branches i.e., the difference in water potential at 50% loss of hydraulic conductance between branches and roots is positive (P 50 root - branch> 0). Hence, roots can sacrifice a small part of the investment to protect plant hydraulic pathway from drought-induced dysfunction in main organs (e.g., main root, trunk and branch).
The degree of vulnerability segmentation between branches and roots decreases with the increasing water availability across different habitats. Plants in arid habitats would have a higher degree of segmentation (P 50 root - branch is more positive) than those in humid areas. Like the segmentation between branches and leaves, plants are likely to adopt a hydraulic strategy by sacrificing terminal roots to prevent branches from hydraulic failure, as drought increases.
Materials and Methods