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