Megan K. Bartlett

The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta‐analysis

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.

Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe

Significance Predicting the impacts of climate extremes on plant communities is a central challenge in ecology. Physiological traits may improve prediction of drought impacts on forests globally. We perform a meta-analysis across 33 studies that span all forested biomes and find that, among the examined traits, hydraulic traits explain cross-species patterns in mortality from drought. Gymnosperm and angiosperm mortality was associated with different hydraulic traits, giving insight into the relative weights of different traits and mechanisms in mortality prediction. Our results provide a foundation for more mechanistic predictions of drought-induced tree mortality across Earth’s diverse forests. 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.

The correlations and sequence of plant stomatal, hydraulic, and wilting responses to drought

Significance Many plant species face increasing drought under climate change, making plant drought tolerance integral to predicting species and ecosystem responses. Many physiology traits interact to determine overall drought tolerance, but trait relationships have not been assessed for general patterns across global plant diversity. We analyzed stomatal, hydraulic, and mesophyll drought tolerance traits for 310 species from ecosystems worldwide. We evaluated the sequence of drought responses for plants under increasing water stress, and showed that coselection with environmental water stress drives most trait correlations across species, with functional coordination additionally important for some relationships. These results provide insight into how variation in multiple traits should be represented within plants and across species in models of plant responses to drought. 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.

Outside-xylem vulnerability, not xylem embolism, controls leaf hydraulic decline during dehydration

Changes in leaf outside-xylem properties drive leaf and whole-plant hydraulic decline with dehydration, protecting plants from catastrophic embolism in xylem conduits. Leaf hydraulic supply is crucial to maintaining open stomata for CO2 capture and plant growth. During drought-induced dehydration, the leaf hydraulic conductance (Kleaf) declines, which contributes to stomatal closure and, eventually, to leaf death. Previous studies have tended to attribute the decline of Kleaf 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 Kleaf 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 Kleaf 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.

Stronger seasonal adjustment in leaf turgor loss point in lianas than trees in an Amazonian forest

Pan-tropically, liana density increases with decreasing rainfall and increasing seasonality. This pattern has led to the hypothesis that lianas display a growth advantage over trees under dry conditions. However, the physiological mechanisms underpinning this hypothesis remain elusive. A key trait influencing leaf and plant drought tolerance is the leaf water potential at turgor loss point (πtlp). πtlp adjusts under drier conditions and this contributes to improved leaf drought tolerance. For co-occurring Amazonian tree (n = 247) and liana (n = 57) individuals measured during the dry and the wet seasons, lianas showed a stronger osmotic adjustment than trees. Liana leaves were less drought-tolerant than trees in the wet season, but reached similar drought tolerances during the dry season. Stronger osmotic adjustment in lianas would contribute to turgor maintenance, a critical prerequisite for carbon uptake and growth, and to the success of lianas relative to trees in growth under drier conditions.

The causes of leaf hydraulic vulnerability and its influence on gas exchange in Arabidopsis thaliana

Declines in leaf outside-xylem hydraulic conductance prior to turgor loss point contribute strongly to stomatal closure, and improve performance, survival and efficient water use during drought. The influence of the dynamics of leaf hydraulic conductance (Kleaf) diurnally and during dehydration on stomatal conductance and photosynthesis remains unclear. Using the model species Arabidopsis (Arabidopsis thaliana ecotype Columbia-0), we applied a multitiered approach including physiological measurements, high-resolution x-ray microcomputed tomography, and modeling at a range of scales to characterize (1) Kleaf decline during dehydration; (2) its basis in the hydraulic conductances of leaf xylem and outside-xylem pathways (Kox); (3) the dependence of its dynamics on irradiance; (4) its impact on diurnal patterns of stomatal conductance and photosynthetic rate; and (5) its influence on gas exchange and survival under simulated drought regimes. Arabidopsis leaves showed strong vulnerability to dehydration diurnally in both gas exchange and hydraulic conductance, despite lack of xylem embolism or conduit collapse above the turgor loss point, indicating a pronounced sensitivity of Kox to dehydration. Kleaf increased under higher irradiance in well-hydrated leaves across the full range of water potential, but no shift in Kleaf vulnerability was observed. Modeling indicated that responses to dehydration and irradiance are likely attributable to changes in membrane permeability and that a dynamic Kox would contribute strongly to stomatal closure, improving performance, survival, and efficient water use during drought. These findings for Columbia-0 provide a baseline for assessing variation across genotypes in hydraulic traits and their influence on gas exchange during dehydration.

Dry‐season decline in tree sapflux is correlated with leaf turgor loss point in a tropical rainforest

1. Water availability is a key determinant of forest ecosystem function and tree species distributions. While droughts are increasing in frequency in many ecosystems, including in the tropics, plant responses to water supply vary with species and drought intensity and are therefore difficult to model. Based on physiological first principles, we hypothesized that trees with a lower turgor loss point (pi(tlp)), that is, a more negative leaf water potential at wilting, would maintain water transport for longer into a dry season. 2. We measured sapflux density of 22 mature trees of 10 species during a dry season in an Amazonian rainforest, quantified sapflux decline as soil water content decreased and tested its relationship to tree pi(tlp), size and leaf predawn and midday water potentials measured after the onset of the dry season. 3. The measured trees varied strongly in the response of water use to the seasonal drought, with sapflux at the end of the dry season ranging from 37 to 117% (on average 83 +/- 5 %) of that at the beginning of the dry season. The decline of water transport as soil dried was correlated with tree pi(tlp) (Spearmans rho >= 0.63), but not with tree size or predawn and midday water potentials. Thus, trees with more drought-tolerant leaves better maintained water transport during the seasonal drought. 4. Our study provides an explicit correlation between a trait, measurable at the leaf level, and whole-plant performance under drying conditions. Physiological traits such as pi(tlp) can be used to assess and model higher scale processes in response to drying conditions.

Tree carbon allocation explains forest drought-kill and recovery patterns

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 CO2 fertilisation facilitates more rapid xylem regrowth.