Increasing drought is one of the most critical challenges facing species and ecosystems worldwide, and improved theory and practices are needed for quantification of species tolerances. Leaf water potential at turgor loss, or wilting (π(tlp) ), is classically recognised as a major physiological determinant of plant water stress response. However, the cellular basis of π(tlp) and its importance for predicting ecological drought tolerance have been controversial. A meta-analysis of 317 species from 72 studies showed that π(tlp) was strongly correlated with water availability within and across biomes, indicating power for anticipating drought responses. We derived new equations giving both π(tlp) and relative water content at turgor loss point (RWC(tlp) ) as explicit functions of osmotic potential at full turgor (π(o) ) and bulk modulus of elasticity (ε). Sensitivity analyses and meta-analyses showed that π(o) is the major driver of π(tlp) . In contrast, ε plays no direct role in driving drought tolerance within or across species, but sclerophylly and elastic adjustments act to maintain RWC(tlp,) preventing cell dehydration, and additionally protect against nutrient, mechanical and herbivory stresses independent of drought tolerance. These findings clarify biogeographic trends and the underlying basis of drought tolerance parameters with applications in comparative assessments of species and ecosystems worldwide.
Drought-induced tree mortality has been observed globally and is expected to increase under climate change scenarios, with large potential consequences for the terrestrial carbon sink. Predicting mortality across species is crucial for assessing the effects of climate extremes on forest community biodiversity, composition, and carbon sequestration. However, the physiological traits associated with elevated risk of mortality in diverse ecosystems remain unknown, although these traits could greatly improve understanding and prediction of tree mortality in forests. We performed a meta-analysis on species' mortality rates across 475 species from 33 studies around the globe to assess which traits determine a species' mortality risk. We found that species-specific mortality anomalies from community mortality rate in a given drought were associated with plant hydraulic traits. Across all species, mortality was best predicted by a low hydraulic safety margin-the difference between typical minimum xylem water potential and that causing xylem dysfunction-and xylem vulnerability to embolism. Angiosperms and gymnosperms experienced roughly equal mortality risks. Our results provide broad support for the hypothesis that hydraulic traits capture key mechanisms determining tree death and highlight that physiological traits can improve vegetation model prediction of tree mortality during climate extremes.meta-analysis | climate change | carbon cycle | climate extremes | biodiversity F orests assimilate and sequester ∼2.4 Pg carbon per year (1), equivalent to 25% of anthropogenic emissions, and provide manifold goods and services to society (2). Climate extremes, such as severe drought, could trigger abrupt and irreversible changes in Earth's forests (3, 4), which would have profound implications for their biodiversity, ecosystem services, and carbon storage (5). Episodes of widespread tree mortality in response to drought and/or heat stress have been observed across the globe in the past few decades (4). In addition, drought severity and frequency are projected to increase with temperature-driven rises in evaporative demand (6). There is fundamental concern that increased climate-induced mortality of trees (7) could offset carbon sinks currently yielded in old growth and regrowth forests alike (8).Predicting plant demographic rates, such as mortality, using physiological traits is a central aim of ecology with critical importance for modeling climate change impacts and the carbon cycle (9). Drought-induced tree mortality has been particularly challenging to model and predict because of uncertainty in traits and mechanisms underlying the physiology of tree death (10, 11). Despite this uncertainty (12, 13), the failure of the plant vascular hydraulic transport system is considered to be a central pathway to mortality (7,(14)(15)(16)(17). This failure happens through embolism of a tree's water transport elements by air bubbles during high xylem tensions induced by low soil moisture and/or high atmospheric evaporative demand during...
Climate change is expected to exacerbate drought for many plants, making drought tolerance a key driver of species and ecosystem responses. Plant drought tolerance is determined by multiple traits, but the relationships among traits, either within individual plants or across species, have not been evaluated for general patterns across plant diversity. We synthesized the published data for stomatal closure, wilting, declines in hydraulic conductivity in the leaves, stems, and roots, and plant mortality for 262 woody angiosperm and 48 gymnosperm species. We evaluated the correlations among the drought tolerance traits across species, and the general sequence of water potential thresholds for these traits within individual plants. The trait correlations across species provide a framework for predicting plant responses to a wide range of water stress from one or two sampled traits, increasing the ability to rapidly characterize drought tolerance across diverse species. Analyzing these correlations also identified correlations among the leaf and stem hydraulic traits and the wilting point, or turgor loss point, beyond those expected from shared ancestry or independent associations with water stress alone. Further, on average, the angiosperm species generally exhibited a sequence of drought tolerance traits that is expected to limit severe tissue damage during drought, such as wilting and substantial stem embolism. This synthesis of the relationships among the drought tolerance traits provides crucial, empirically supported insight into representing variation in multiple traits in models of plant and ecosystem responses to drought. drought tolerance | stem hydraulics | leaf hydraulics | stomatal closure | turgor loss point P lants worldwide are expected to face more frequent and severe droughts under climate change (1). Characterizing drought tolerance for diverse species is key to improved predictions of ecosystem responses to global change (2), and ecological and phylogenetic patterns have been established across many species for individual drought tolerance traits (3-7). However, plant drought tolerance is determined by multiple traits. The relationships among traits within plants and across species have not been evaluated for general patterns across global plant diversity. We synthesized the published data to elucidate global patterns in the relationships among stomatal, hydraulic, and leaf mesophyll drought tolerance traits. We evaluated the roles of functional coordination, covariance with water stress, and shared ancestry in driving trait correlations across species. Additionally, we focused on clarifying relationships among drought tolerance traits within plants of given species, i.e., determining the sequence of their water potential thresholds.Classical drought tolerance traits quantify the water potentials that induce declines in key physiological processes, such as stomatal conductance, hydraulic conductivity, and cell turgor pressure. Previous studies have shown that these water potential thresholds are i...
Summary1. Across plant species, drought tolerance and distributions with respect to water availability are strongly correlated with two physiological traits, the leaf water potential at wilting, that is, turgor loss point (p tlp ), and the cell solute potential at full hydration, that is, osmotic potential (p o ). We present methods to determine these parameters 30 times more rapidly than the standard pressurevolume (p-v) curve approach, making feasible community-scale studies of plant drought tolerance. 2. We optimized existing methods for measurements of p o using vapour-pressure osmometry of freeze-thawed leaf discs from 30 species growing in two precipitation regimes, and developed the first regression relationships to accurately estimate pressure-volume curve values of both p o and p tlp from osmometer values . 3. The p o determined with the osmometer (p osm ) was an excellent predictor of the p o determined from the p-v curve (p pv, r 2 = 0AE80). Although the correlation of p osm and p pv enabled prediction, the relationship departed from the 1 : 1 line. The discrepancy between the methods could be quantitatively accounted for by known sources of error in osmometer measurements, that is, dilution by the apoplastic water, and solute dissolution from destroyed cell walls. An even stronger prediction of p pv could be made using p osm, leaf density (q), and their interaction (r 2 = 0AE85, all P < 2 · 10 )10). 4. The p osm could also be used to predict p tlp (r 2 = 0AE86). Indeed, p osm was a better predictor of p tlp than leaf mass per unit area (LMA; r 2 = 0AE54), leaf thickness (T; r 2 = 0AE12), q (r 2 = 0AE63), and leaf dry matter content (LDMC; r 2 = 0AE60), which have been previously proposed as drought tolerance indicators. Models combining p osm with LMA, T, q, or LDMC or other p-v curve parameters (i.e. elasticity and apoplastic fraction) did not significantly improve prediction of p tlp . 5. This osmometer method enables accurate measurements of drought tolerance traits across a wide range of leaf types and for plants with diverse habitat preferences, with a fraction of effort of previous methods. We expect it to have wide application for predicting species responses to climate variability and for assessing ecological and evolutionary variation in drought tolerance in natural populations and agricultural cultivars.
Leaf hydraulic supply is crucial to maintaining open stomata for CO 2 capture and plant growth. During drought-induced dehydration, the leaf hydraulic conductance (K leaf ) declines, which contributes to stomatal closure and, eventually, to leaf death. Previous studies have tended to attribute the decline of K leaf to embolism in the leaf vein xylem. We visualized at high resolution and quantified experimentally the hydraulic vulnerability of xylem and outside-xylem pathways and modeled their respective influences on plant water transport. Evidence from all approaches indicated that the decline of K leaf during dehydration arose first and foremost due to the vulnerability of outside-xylem tissues. In vivo x-ray microcomputed tomography of dehydrating leaves of four diverse angiosperm species showed that, at the turgor loss point, only small fractions of leaf vein xylem conduits were embolized, and substantial xylem embolism arose only under severe dehydration. Experiments on an expanded set of eight angiosperm species showed that outside-xylem hydraulic vulnerability explained 75% to 100% of K leaf decline across the range of dehydration from mild water stress to beyond turgor loss point. Spatially explicit modeling of leaf water transport pointed to a role for reduced membrane conductivity consistent with published data for cells and tissues. Plant-scale modeling suggested that outside-xylem hydraulic vulnerability can protect the xylem from tensions that would induce embolism and disruption of water transport under mild to moderate soil and atmospheric droughts. These findings pinpoint outside-xylem tissues as a central locus for the control of leaf and plant water transport during progressive drought.
The mechanisms governing tree drought mortality and recovery remain a subject of inquiry and active debate given their role in the terrestrial carbon cycle and their concomitant impact on climate change. Counter-intuitively, many trees do not die during the drought itself. Indeed, observations globally have documented that trees often grow for several years after drought before mortality. A combination of meta-analysis and tree physiological models demonstrate that optimal carbon allocation after drought explains observed patterns of delayed tree mortality and provides a predictive recovery framework. Specifically, post-drought, trees attempt to repair water transport tissue and achieve positive carbon balance through regrowing drought-damaged xylem. Furthermore, the number of years of xylem regrowth required to recover function increases with tree size, explaining why drought mortality increases with size. These results indicate that tree resilience to drought-kill may increase in the future, provided that CO fertilisation facilitates more rapid xylem regrowth.
Many species face increasing drought under climate change. Plasticity has been predicted to strongly influence species' drought responses, but broad patterns in plasticity have not been examined for key drought tolerance traits, including turgor loss or 'wilting' point (πtlp ). As soil dries, plants shift πtlp by accumulating solutes (i.e. 'osmotic adjustment'). We conducted the first global analysis of plasticity in Δπtlp and related traits for 283 wild and crop species in ecosystems worldwide. Δπtlp was widely prevalent but moderate (-0.44 MPa), accounting for 16% of post-drought πtlp. Thus, pre-drought πtlp was a considerably stronger predictor of post-drought πtlp across species of wild plants. For cultivars of certain crops Δπtlp accounted for major differences in post-drought πtlp. Climate was correlated with pre- and post-drought πtlp, but not Δπtlp. Thus, despite the wide prevalence of plasticity, πtlp measured in one season can reliably characterise most species' constitutive drought tolerances and distributions relative to water supply.
1.Amazonian droughts are predicted to become increasingly frequent and intense, and the vulnerability of Amazonian trees has become increasingly documented. However, little is known about the physiological mechanisms and the diversity of drought tolerance of tropical trees due to the lack of quantitative measurements. 2.Leaf water potential at wilting or turgor loss point (π tlp ) is a determinant of the tolerance of leaves to drought stress, and contributes to plant-level physiological drought tolerance. Recently, it has been demonstrated that leaf osmotic water potential at full hydration (π 0 ) is tightly correlated with π tlp . Estimating π tlp from osmometer measurements of π 0 is much faster than the standard pressure-volume curve approach of π tlp determination. We used this technique to estimate π tlp for 165 trees of 71 species, at three sites within forests in French Guiana. Our dataset represents a significant increase in available data for this trait for tropical tree species. 3.Tropical trees showed a wider range of drought tolerance than previously found in the literature, π tlp ranging from -1.4 to -3.2 MPa. This range likely corresponds in part to adaptation and acclimation to occasionally extreme droughts during the dry season. 4.Leaf-level drought tolerance varied across species, in agreement with the available published observations of species variation in drought-induced mortality. On average, species with a more negative π tlp (i.e., with greater leaf-level drought tolerance) occurred less frequently across the region than drought-sensitive species. Accepted ArticleThis article is protected by copyright. All rights reserved. 5.Across individuals, π tlp correlated positively but weakly with leaf toughness (R 2 =0.22, P=0.04) and leaf thickness (R 2 =0.03, P=0.03). No correlation was detected with other functional traits (leaf mass per area, leaf area, nitrogen or carbon concentrations, carbon isotope ratio, sapwood density or bark thickness).6. The variability in π tlp among species indicates a potential for highly diverse species responses to drought within given forest communities. Given the weak correlations between π tlp and traditionally measured plant functional traits, vegetation models seeking to predict forest response to drought should integrate improved quantification of comparative drought tolerance among tree species.
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