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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.

Stomata, the microvalves on leaf surfaces, exert major influences across scales, from plant growth and productivity to global carbon and water cycling. Stomatal opening enables leaf photosynthesis, and plant growth and water use, whereas plant survival of drought depends on stomatal closure. Here we report that stomatal function is constrained by a safety-efficiency trade-off, such that species with greater stomatal conductance under high water availability ( g max ) show greater sensitivity to closure during leaf dehydration, i.e., a higher leaf water potential at which stomatal conductance is reduced by 50% (Ψ gs50 ). The g max - Ψ gs50 trade-off and its mechanistic basis is supported by experiments on leaves of California woody species, and in analyses of previous studies of the responses of diverse flowering plant species around the world. Linking the two fundamental key roles of stomata—the enabling of gas exchange, and the first defense against drought—this trade-off constrains the rates of water use and the drought sensitivity of leaves, with potential impacts on ecosystems. Stomata enable gas exchange for photosynthesis but close to promote survival during drought. Here, Henry et al. provide evidence for a safety-efficiency trade-off whereby plants with greater stomatal conductance under well-watered conditions are more sensitive to stomatal closure during dehydration.

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 (pi(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 (pi(o)) is tightly correlated with pi(tlp). Estimating pi(tlp) from osmometer measurements of pi(o) is much faster than the standard pressure-volume curve approach of pi(tlp) determination. We used this technique to estimate pi(tlp) for 165 trees of 71 species, at three sites within forests in French Guiana. Our data set 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, pi(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 pi(tlp) (i.e. with greater leaf-level drought tolerance) occurred less frequently across the region than drought-sensitive species. 5. Across individuals, pi(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 pi(tlp) among species indicates a potential for highly diverse species responses to drought within given forest communities. Given the weak correlations between pi(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.

Maintaining phloem transport under water stress is expected to be crucial to whole-plant drought tolerance, but the traits that benefit phloem function under drought are poorly understood. Nearly half of surveyed angiosperm species, including important crops, use sucrose transporter proteins to actively load sugar into the phloem. Plants can alter transporter abundance in response to stress, providing a potential mechanism for active-loading species to closely regulate phloem loading rates to avoid drought-induced reductions or failures in phloem transport. We developed an integrated xylem-phloem-stomatal model to test this hypothesis by quantifying the joint impacts of transporter kinetics, phloem anatomy, and plant water status on sucrose export to sinks. We parameterized the model with phloem hydraulic resistances and sucrose transporter kinetic parameters compiled from the literature, and simulated loading regulation by allowing loading rates to decline exponentially with phloem pressure to prevent excessive sucrose concentrations from inducing viscosity limitations. In the absence of loading regulation, where loading rates were independent of phloem pressure, most resistance values produced unrealistic phloem pressures owing to viscosity effects, even under well-watered conditions. Conversely, pressure-regulated loading helped to control viscosity buildup and improved export to sinks for both lower and higher resistant phloem pathways, while maintaining realistic phloem pressures. Regulation also allowed for rapid loading and export in wet conditions while maintaining export and viable phloem pressures during drought. Therefore, we expect feedbacks between phloem pressure and loading to be critical to carbon transport in active-loading species, especially under drought, and for transporter kinetics to be strongly coordinated with phloem architecture and plant water status. This work provides an important and underexplored physiological framework to understand the ecophysiology of phloem transport under drought and to enhance the genetic engineering of crop plants.

The application of functional traits to predict and explain plant species’ distributions and vital rates has been a major direction in functional ecology for decades, yet numerous physiological traits have not yet been incorporated into the approach. Using commonly measured traits such as leaf mass per area (LMA) and wood density (WD), and additional traits related to water transport, gas exchange and resource economics, including leaf vein, stomatal and wilting traits, we tested hypotheses for Hawaiian wet montane and lowland dry forests (MWF and LDF, respectively): (1) Forests would differ in a wide range of traits as expected from contrasting adaptation; (2) trait values would be more convergent among dry than wet forest species due to the stronger environmental filtering; (3) traits would be intercorrelated within “modules” supporting given functions; (4) relative growth rate (RGR) and mortality rate (m) would correlate with a number of specific traits; with (5) stronger relationships when stratifying by tree size; and (6) RGR and m can be strongly explained from trait‐based models. The MWF species’ traits were associated with adaptation to high soil moisture and nutrient supply and greater shade tolerance, whereas the LDF species’ traits were associated with drought tolerance. Thus, on average, MWF species achieved higher maximum heights than LDF species and had leaves with larger epidermal cells, higher maximum stomatal conductance and CO2 assimilation rate, lower vein lengths per area, higher saturated water content and greater shrinkage when dry, lower dry matter content, higher phosphorus concentration, lower nitrogen to phosphorus ratio, high chlorophyll to nitrogen ratio, high carbon isotope discrimination, high stomatal conductance to nitrogen ratio, less negative turgor loss point and lower WD. Functional traits were more variable in the MWF than LDF, were correlated within modules, and predicted species’ RGR and m across forests, with stronger relationships when stratifying by tree size. Models based on multiple traits predicted vital rates across forests (R2 = 0.70–0.72; p < 0.01). Our findings are consistent with a powerful role of broad suites of functional traits in contributing to forest species’ distributions, integrated plant design and vital rates. A plain language summary is available for this article. Plain Language Summary

Environmental filtering and dispersal limitation can both maintain diversity in plant communities by aggregating conspecifics, but parsing the contribution of each process has proven difficult empirically. Here, we assess the contribution of filtering and dispersal limitation to the spatial aggregation patterns of 456 tree species in a hyperdiverse Amazonian forest and find distinct functional trait correlates of interspecific variation in these processes. Spatial point process model analysis revealed that both mechanisms are important drivers of intraspecific aggregation for the majority of species. Leaf drought tolerance was correlated with species topographic distributions in this aseasonal rainforest, showing that future increases in drought severity could significantly impact community structure. In addition, seed mass was associated with the spatial scale and density of dispersal-related aggregation. Taken together, these results suggest environmental filtering and dispersal limitation act in concert to influence the spatial and functional structure of diverse forest communities.

Premise of the Study Studies across diverse species have established theory for the contribution of leaf traits to plant drought tolerance. For example, species in more arid climates tend to have smaller leaves of higher vein density, higher leaf mass per area, and more negative osmotic potential at turgor loss point (πTLP). However, few studies have tested these associations for species within a given lineage that have diversified across an aridity gradient. Methods We analyzed the anatomy and physiology of 10 Ceanothus (Rhamnaceae) species grown in a common garden for variation between and within “wet” and “dry” subgenera (Ceanothus and Cerastes, respectively) and analyzed a database for 35 species for leaf size and leaf mass per area (LMA). We used a phylogenetic generalized least squares approach to test hypothesized relationships among traits, and of traits with climatic aridity in the native range. We also tested for allometric relationships among anatomical traits. Key Results Leaf form, anatomy, and drought tolerance varied strongly among species within and between subgenera. Cerastes species had specialized anatomy including hypodermis and encrypted stomata that may confer superior water storage and retention. The osmotic potentials at turgor loss point (πTLP) and full turgor (πo) showed evolutionary correlations with the aridity index (AI) and precipitation of the 10 species’ native distributions, and LMA with potential evapotranspiration for the 35 species in the larger database. We found an allometric correlation between upper and lower epidermal cell wall thicknesses, but other anatomical traits diversified independently. Conclusions Leaf traits and drought tolerance evolved within and across lineages of Ceanothus consistently with climatic distributions. The πTLP has signal to indicate the evolution of drought tolerance within small clades.

Climate change is impacting the wine industry by accelerating ripening processes due to warming temperatures, especially in areas of significant grape production like California. Increasing temperatures accelerate the rate of sugar accumulation (measured in ⁰Brix) in grapes, however this presents a problem to wine makers as flavor profiles may need more time to develop properly. To alleviate the mismatch between sugar accumulation and flavor compounds, growers may sync vine cultivars with climates that are most amenable to their distinct growing conditions. However, the traits which control such cultivar specific climate adaptation, especially for ⁰Brix accumulation rate, are poorly understood. Recent studies have shown that higher rates of fruit development and sugar accumulation are predicted by larger phloem areas in different organs of the plant. Here we test this phloem area hypothesis using a common garden experiment in the Central Valley of Northern California using 18 cultivars of the common grapevine ( ) and assess the grape berry sugar accumulation rates as a function of phloem area in leaf and grape organs. We find that phloem area in the leaf petiole organ as well as the berry pedicel is a significant predictor of ⁰Brix accumulation rate across 13 cultivars and that grapes from warm climates overall have larger phloem areas than those from hot climates. In contrast, other physiological traits such as photosynthetic assimilation and leaf water potential did not predict berry accumulation rates. As hot climate cultivars have lower phloem areas which would slow down brix accumulation, growers may have inadvertently been selecting this trait to align flavor development with sugar accumulation across the common cultivars tested. This work highlights a new trait that can be easily phenotyped (i.e., petiole phloem area) and be used for growers to match cultivar more accurately with the temperature specific climate conditions of a growing region to obtain satisfactory sugar accumulation and flavor profiles.

Key messageLeaf density links the resistance to mechanical and hydraulic stress in Mediterranean shrubs as it is associated with the water potential at turgor loss and the moduli of elasticity and strength.Understanding the patterns of hydraulic and mechanical trait variation in vascular plants is critical to predicting species’ stress tolerance. Although previous work has shown that hydraulic and mechanical traits are decoupled in stems, there is little information available for leaves, which are organs more diversified in structure, function, and possibly drought tolerance strategies across habitats. We tested for coordination between leaf hydraulic traits related to drought tolerance and the mechanical resistance of leaves, for 17 shrub species from the arid and semiarid vegetation of the California Floristic Province. Bayesian and phylogenetic correlations showed that across species, hydraulic and mechanical traits both had strong associations with the water potential at turgor loss, and with leaf tissue density. However, leaf maximum hydraulic conductance and the water potential at 50% and 80% loss of hydraulic conductance were statistically independent of two key mechanical traits, the leaf modulus of elasticity and leaf structural strength. Our results suggest that leaf biomechanical traits, which reflect construction costs and contribute to leaf longevity, are decoupled from hydraulic capacity and safety. The independence of hydraulic and mechanical protection in leaves enables a wide range of trait combinations in leaves, which would increase their adaptive potential across ecosystems.

Leaf hydraulic supply is crucial to maintaining open stomata for CO₂ 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.