4.1 Higher vulnerability of roots compared to branches
We observed a notable increase in xylem resistance to cavitation
(P 50), but a decline in hydraulic efficiency
(K S) from roots to branches. Roots were more
vulnerable to cavitation than branches for a given xylem diameter, and
roots had 62% higher (less negative) P 50 value
than branches (Figure 1). These results implied that roots with lower
hydraulic safety, might be more susceptible to drought stress than
branches along plant water transport pathway from soil to the atmosphere
(Jackson et al ., 2000). However,
roots with higher hydraulic
efficiency than branches ensuring the water supply of the whole plant
and prevent water deficit caused by high transpiration
(Rodriguez-Dominguez & Brodribb, 2020). This difference in xylem
cavitation vulnerability between branches and roots is matched by
variability in wood anatomical characteristics, in that we found a lower
vessel wall reinforcement
(t 2/b 2) and a wider
hydraulically weighted mean diameter (D h) in root
xylem compared to branch xylem (Figure 1), and these anatomical traits
showed significant correlations with P 50 both in
roots and branches (Figure 2). Not only to ensure anchorage, woody
species commonly require roots to absorb and transport water with
mineral nutrients, wider conduits are therefore needed to improve
efficiency of transportation in roots. However, branches have to resist
stronger mechanical stress induced by gravity, wind, and ice loading
etc., thus they need a relatively more robust woody structure than roots
(MacFarlane & Kane, 2017). It has been shown at the cellular level,
branches tended to have thicker cell walls and conduits with highert 2/b 2 than roots,
which are often associated with lower conducting efficiency but greater
resistance to cavitation (Hacke & Jansen, 2009; Schulte et al .,
2015).
4.2 Relationships between xylem hydraulic and anatomical traits
Our results suggest a generally positive relationship betweenD h and P 50 (Barottoet al ., 2018; Jacobsen et al ., 2019). However, cavitation
formation may not be directly related to conduit size, but pit
properties (Lemaire et al ., 2021; Levionnois et al .,
2021). 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 (Mrad et al ., 2018). Moreover, thicker cell walls may
also influence pit morphology, including the pit membrane, thereby
increasing xylem cavitation resistance (Li et al ., 2016).
Obviously, the pit membrane area is at least partly affected by conduit
dimensions (Hacke et al ., 2017), suggesting that root xylem with
larger conduits and thinner cell walls than those of branches, may be
more vulnerable to drought-induced collapsing stress or cavitation.
The vulnerability segmentation between branches and roots may be an
adaptive strategy for woody plants to cope with drought stress.
Localized failure in relatively cheap and replaceable units (e.g., roots
and leaves) would avoid disruption of major arteries of axial transport
(Klepsch et al ., 2018; Aritsara et al ., 2022). In this
study, we found a positive correlation between P 50
root - branch and P 50 branch (Figure 3a), but no
correlation was found between P 50 root - branchand P 50 root (Figure 3b). These results implied
that the degree of vulnerability segmentation between roots and branches
is likely to be dominantly affected by the changes in cavitation
vulnerability of branches. By contrast, roots generally maintain a
relatively lower vulnerability to cavitation (Figure 3b). This may due
to the fact that coarse roots (root diameter > 5 mm) are
not easily exposed to very negative water potential. During drought
exposure, cortical lacunae formation caused the outside xylem hydraulic
conductivity within the cortical cells declined earlier before
cavitation formed in coarse roots (Cuneo et al ., 2021).
Cavitation formation in fine roots (root diameter < 2 mm)
would interrupt the soil-root-connectivity during drought, thereby
restricting hydraulic failure to replaceable units. (Carminati &
Javaux, 2020; Aritsara et
al ., 2022). Moreover, coarse roots may also act as hydraulic fuses like
fine roots, which form a multi-stage circuit breaker with fine roots
together to protect the hydraulic safety of the organs with high carbon
investment (e.g., main root and trunk) against potentially extreme
drought. We found woody species with branches that are more resistant to
cavitation also have a greater degree of vulnerability segmentation
(Figure 3a). However, this may be at the cost of partial loss of xylem
hydraulic conductivity. We also found that K S in
both roots and branches were markedly lower in woody species with
greater degree of vulnerable segmentation (Figure 3c, 3d), highlighting
a trade-off between hydraulic safety (capacity to resist cavitation) and
efficiency (capacity to transport water) in the xylem of branches and
roots (Gleason et al ., 2016).