This study combines existing hydraulic principles with recently developed methods for probing leaf hydraulic function to determine whether xylem physiology can explain the dynamic response of gas ...exchange both during drought and in the recovery phase after rewatering. Four conifer species from wet and dry forests were exposed to a range of water stresses by withholding water and then rewatering to observe the recovery process. During both phases midday transpiration and leaf water potential (Ψleaf) were monitored. Stomatal responses to Ψleaf were established for each species and these relationships used to evaluate whether the recovery of gas exchange after drought was limited by postembolism hydraulic repair in leaves. Furthermore, the timing of gas-exchange recovery was used to determine the maximum survivable water stress for each species and this index compared with data for both leaf and stem vulnerability to water-stress-induced dysfunction measured for each species. Recovery of gas exchange after water stress took between 1 and >100 d and during this period all species showed strong 1:1 conformity to a combined hydraulic-stomatal limitation model (r² = 0.70 across all plants). Gas-exchange recovery time showed two distinct phases, a rapid overnight recovery in plants stressed to <50% loss of leaf hydraulic conductance (Kleaf) and a highly Ψleaf-dependent phase in plants stressed to >50% loss of Kleaf. Maximum recoverable water stress (Ψmin) corresponded to a 95% loss of Kleaf. Thus, we conclude that xylem hydraulics represents a direct limit to the drought tolerance of these conifer species.
Adapting agriculture to climate change is driving the need for the selection and breeding of drought-tolerant crops. The aim of this study was to identify key drought tolerance traits and determine ...the sequence of their water potential thresholds across three grapevine cultivars with contrasting water use behaviors, Grenache, Syrah, and Semillon. We quantified differences in water use between cultivars and combined this with the determination of other leaf-level traits (e.g. leaf turgor loss point, π TLP), leaf vulnerability to embolism (P50), and the hydraulic safety margin (HSM P50). Semillon exhibited the highest maximum transpiration (Emax), and lowest sensitivity of canopy stomatal conductance (Gc) to vapor pressure deficit (VPD), followed by Syrah and Grenache. Increasing Emax was correlated with more negative water potential at which stomata close (Pgs90), π TLP, and P50, suggesting that increasing water use is associated with hydraulic traits allowing gas exchange under more negative water potentials. Nevertheless, all the cultivars closed their stomata prior to leaf embolism formation. Modeling simulations demonstrated that despite a narrower HSM, Grenache takes longer to reach thresholds of hydraulic failure due to its conservative water use. This study demonstrates that the relationships between leaf hydraulic traits are complex and interactive, stressing the importance of integrating multiple traits in characterizing drought tolerance.
Stomata play a key role in plant adaptation to changing environmental conditions as they control both water losses and CO₂ uptake. Particularly, in the context of global change, simulations of the ...consequences of drought on crop plants are needed to design more efficient and water-saving cropping systems. However, most of the models of stomatal conductance (gs) developed at the leaf level link gs to environmental factors or net photosynthesis (Anet), but do not include satisfactorily the effects of drought, impairing our capacity to simulate plant functioning in conditions of limited water supply. The objective of this review was to draw an up-to-date picture of the gs models, from the empirical to the process-based ones, along with their mechanistic or deterministic bases. It focuses on models capable to account for multiple environmental influences with emphasis on drought conditions. We examine how models that have been proposed for well-watered conditions can be combined with those specifically designed to deal with drought conditions. Ideas for future improvements of gs models are discussed: the issue of co-regulation of gs and Anet; the roles of CO₂, absissic acid and H₂O₂; and finally, how to better address the new challenges arising from the issue of global change.
Resistance to cavitation is a major determinant of plant survival under severe drought and can be used to quantify species adaptive potential. Interspecific variation in this key trait is well ...defined in woody species, but intraspecific variation (level and structure) resulting from standing genetic variation and phenotypic plasticity has never been determined.
Combining for the first time in situ characterization of natural populations and two reciprocal common gardens in dry and wet sites, we estimated variance components (phenotypic, genetic, environmental, and genetic 9 environmental) of cavitation resistance based on 513 genotypes of a Mediterranean pine, Pinus pinaster.
Despite the selected populations being climatically contrasted, phenotypic plasticity in resistance to cavitation remained low and was essentially attributed to family level. Between-population variation in cavitation resistance for both phenotypic and genetic variation was limited.
These results strongly suggest that cavitation resistance is buffered against genetic and to a lesser extent environmental variation (canalization) in maritime pine. Consequently, in a drier world, the increasing drought tolerance of Pinus species might be severely constrained by the low level of cavitation resistance variation, resulting in a large-scale loss of productivity.
Key message
Xylem vulnerability to drought-induced embolism did not differ between stems and petioles of four woody species (
Betula pendula
,
Liriodendron tulipifera
,
Populus tremula
and
Olea ...europaea
). Our results, together with data compiled from published literature, indicate that hydraulic segmentation during drought stress is not consistently driven by difference in vulnerability to embolism between stem and terminal organs.
Context
Hydraulic failure and disconnection of distal organs during protracted drought stress is thought to protect large branches or trunks by reducing water loss and restricting the spread of embolism. Hydraulic segmentation and preferential sacrifice of distal organs such as leaves can be driven by two mechanisms: more negative water potentials at the terminal section of the hydraulic pathway and/or by higher vulnerability to xylem embolism of distal organs. Although vulnerability segmentation has been reported in the literature, the generality of this phenomenon is unclear, in part due to the methodological limitations related to direct measurement of xylem vulnerability to embolism in intact plants.
Aims
The objective of this study was to evaluate vulnerability segmentation between petioles and stems using non-invasive micro computed tomography (microCT).
Methods
Vulnerability to embolism was measured in leaf petioles and subtending stems of four woody species (
Betula pendula
R.,
Liriodendron tulipifera
L.,
Populus tremula
L. and
Olea europaea
L.) with contrasting drought tolerances. In addition, previously published vulnerability data for petioles and stems were compiled from the literature to investigate the commonality of hydraulic segmentation across a wide range of woody species, with the vulnerability curve methodology distinguished.
Results
Using non-invasive imaging on intact plants, we found no evidence of hydraulic segmentation between petioles and stems of four angiosperm tree species, regardless of mechanism. Moreover, the literature dataset indicated that little or no difference in vulnerability to embolism is present between petioles and stems when vulnerability curves were constructed using methods specifically measuring the dynamics of xylem tissue during dehydration (e.g. optical visualization, MicroCT).
Conclusion
Our results suggest that vulnerability segmentation between stems and distal organs (petioles and leaves) is limited when only xylem tissue is considered. Large differences in vulnerability between stems and leaves are likely to be driven by extra-xylary components, rather than xylem embolism.
Hanging by a thread? Forests and drought Brodribb, Timothy J; Powers, Jennifer; Cochard, Hervé ...
Science (American Association for the Advancement of Science),
04/2020, Letnik:
368, Številka:
6488
Journal Article
Recenzirano
Trees are the living foundations on which most terrestrial biodiversity is built. Central to the success of trees are their woody bodies, which connect their elevated photosynthetic canopies with the ...essential belowground activities of water and nutrient acquisition. The slow construction of these carbon-dense, woody skeletons leads to a slow generation time, leaving trees and forests highly susceptible to rapid changes in climate. Other long-lived, sessile organisms such as corals appear to be poorly equipped to survive rapid changes, which raises questions about the vulnerability of contemporary forests to future climate change. The emerging view that, similar to corals, tree species have rather inflexible damage thresholds, particularly in terms of water stress, is especially concerning. This Review examines recent progress in our understanding of how the future looks for forests growing in a hotter and drier atmosphere.
Ecosystems worldwide are facing increasingly severe and prolonged droughts during which hydraulic failure from drought-induced embolism can lead to organ or whole plant death. Understanding the ...determinants of xylem failure across species is especially critical in leaves, the engines of plant growth.
If the vulnerability segmentation hypothesis holds within leaves, higher order veins that are most terminal in the plant hydraulic system should be more susceptible to embolism to protect the rest of the water transport system. Increased vulnerability in the higher order veins would also be consistent with these experiencing the greatest tensions in the plant xylem network.
To test this hypothesis, we combined X-ray micro-computed tomography imaging, hydraulic experiments, cross-sectional anatomy and 3D physiological modelling to investigate how embolisms spread throughout petioles and vein orders during leaf dehydration in relation to conduit dimensions.
Decline of leaf xylem hydraulic conductance (K
x) during dehydration was driven by embolism initiating in petioles and midribs across all species, and K
x vulnerability was strongly correlated with petiole and midrib conduit dimensions. Our simulations showed no significant impact of conduit collapse on K
x decline. We found xylem conduit dimensions play a major role in determining the susceptibility of the leaf water transport system during strong leaf dehydration.
Plants can be highly segmented organisms with an independently redundant design of organs. In the context of plant hydraulics, leaves may be less embolism resistant than stems, allowing hydraulic ...failure to be restricted to distal organs that can be readily replaced.
We quantified drought‐induced embolism in needles and stems of Pinus pinaster using high‐resolution computed tomography (HRCT). HRCT observations of needles were compared with the rehydration kinetics method to estimate the contribution of extra‐xylary pathways to declining hydraulic conductance.
High‐resolution computed tomography images indicated that the pressure inducing 50% of embolized tracheids was similar between needle and stem xylem (P50 needle xylem = −3.62 MPa, P50 stem xylem = −3.88 MPa). Tracheids in both organs showed no difference in torus overlap of bordered pits. However, estimations of the pressure inducing 50% loss of hydraulic conductance at the whole needle level by the rehydration kinetics method were significantly higher (P50 needle = −1.71 MPa) than P50 needle xylem derived from HRCT.
The vulnerability segmentation hypothesis appears to be valid only when considering hydraulic failure at the entire needle level, including extra‐xylary pathways. Our findings suggest that native embolism in needles is limited and highlight the importance of imaging techniques for vulnerability curves.
The main goal of this paper is to test the vulnerability segmentation hypothesis in Pinus pinaster, which suggests that needles are more vulnerable to drought‐induced cavitation than stems. Results based on high resolution X‐ray computed tomography (HRCT) provide unambiguous evidence that xylem tracheids in needles of P. pinaster are not more vulnerable to cavitation than stem xylem. However, comparison of vulnerability curves based on HRCT with the rehydration kinetics method show that the vulnerability segmentation hypothesis is valid when hydraulic conductance is considered at the whole needle level. This paper illustrates the importance of visualizing embolism at the tissue level to interpret vulnerability curves of stems and leaves, and raises questions about earlier reports of daily embolism formation and refilling in gymnosperm xylem.
ABSTRACT
Adequate radial water transport between elastic bark tissue and xylem is crucial in trees, because it smoothens abrupt changes in xylem water potential, greatly reducing the likelihood of ...suffering dangerous levels of embolism. The radial hydraulic conductance involved is generally thought to be constant. Evidence collected about variable root and leaf hydraulic conductance led us to speculate that radial hydraulic conductance in stem/branches might also be variable and possibly modulated by putative aquaporins. We therefore correlated diameter changes in walnut (Juglans regia L.) with changes in water potential, altered by perfusion of twig samples with d‐mannitol solutions having different osmotic potentials. Temperature and cycloheximide (CHX; a protein synthesis inhibitor) treatments were performed. The temperature response and diameter change inhibition found in CHX‐treated twigs underpinned our hypothesis that radial hydraulic conductance is variable and likely mediated by a putative aquaporin abundance and/or activity. Our data demonstrate that radial water transport in stem/branches can take two routes in parallel: an apoplastic and a cell‐to‐cell route. The contribution of either route depends on the hydraulic demand and is closely linked to a boost of putative aquaporins, causing radial conductance to be variable. This variability should be considered when interpreting and modelling diameter changes.
This study shows that the radial hydraulic conductance between the xylem and the bark in tree branches and trunks can change and be controlled by aquaporin abundance and/or activity. The contribution of the protein‐mediated cell‐to‐cell pathway to the overall radial water transport could be greater than generally thought and appears to be activated by environmental stimuli that increase transpiration.
PDF
