Shifts in rainfall patterns and increasing temperatures associated with climate change are likely to cause widespread forest decline in regions where droughts are predicted to increase in duration and severity. One primary cause of productivity loss and plant mortality during drought is hydraulic failure. Drought stress creates trapped gas emboli in the water transport system, which reduces the ability of plants to supply water to leaves for photosynthetic gas exchange and can ultimately result in desiccation and mortality. At present we lack a clear picture of how thresholds to hydraulic failure vary across a broad range of species and environments, despite many individual experiments. Here we draw together published and unpublished data on the vulnerability of the transport system to drought-induced embolism for a large number of woody species, with a view to examining the likely consequences of climate change for forest biomes. We show that 70% of 226 forest species from 81 sites worldwide operate with narrow hydraulic safety margins against injurious levels of drought stress and therefore potentially face long-term reductions in productivity and survival if temperature and aridity increase as predicted for many regions across the globe. Safety margins are largely independent of mean annual precipitation, showing that there is global convergence in the vulnerability of forests to drought, with all forest biomes equally vulnerable to hydraulic failure regardless of their current rainfall environment. These findings provide insight into why drought-induced forest decline is occurring not only in arid regions but also in wet forests not normally considered at drought risk

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 (C leaf ) were monitored. Stomatal responses to C leaf 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 (r 2 = 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 (K leaf ) and a highly C leaf -dependent phase in plants stressed to .50% loss of K leaf . Maximum recoverable water stress (C min ) corresponded to a 95% loss of K leaf . Thus, we conclude that xylem hydraulics represents a direct limit to the drought tolerance of these conifer species.Photosynthesis occurs in an aqueous environment and until evolution comes across a solid-state means of fixing atmospheric CO 2 , terrestrial plant species, even those in humid tropical rainforests (Engelbrecht et al., 2007) will be exposed to potentially lethal desiccation. The reason for this is that in most environments competition between plants forces them to engage in a dangerous balancing act between trading water for carbon at the leaf while minimizing costs associated with replacing this transpired water with water pulled from the soil. The job of seeking and transporting water falls upon the roots and vascular system, and reduced investment in these systems comes at a cost in terms of the safety and efficiency of water carriage. These conflicting demands mold the form and function of vascular plants and have yielded a diverse spectrum of vascular anatomies, each tuned to a specific flow capacity and drought tolerance.Desiccation tolerance is at the center of the vascular cost/benefit equation. The reason for this is that a more desiccation-tolerant vascular system (one that resists embolism better during soil drying) is distinctly more costly to build than a sensitive system (Hacke et al., 2001a), yet the repercussions of vascular failure are likely to be fatal. This trade-off, as with many other systems in biology, leads to functional diversity and hence there is a great range in the ability of...

In this review, we discuss the evolution of xylem structure in the context of our current understanding of the biophysics of water transport in plants. Water transport in land plants occurs while water is under negative pressure and is thus in a metastable state. Vessels filled with metastable water are prone to dysfunction by cavitation whenever gas-filled voids appear in the vessel lumen. Cavitated vessels fill with air and are incapable of water transport until air bubbles dissolve. We know much more about how cavitations occur and the conditions under which air bubbles (embolisms) dissolve. This gives us an improved understanding of the relations hip between xylem structure and function.

Stomata play a significant role in the Earth's water and carbon cycles, by regulating gaseous exchanges between the plant and the atmosphere. Under drought conditions, stomatal control of transpiration has long been thought to be closely coordinated with the decrease in hydraulic capacity (hydraulic failure due to xylem embolism). We tested this hypothesis by coupling a meta-analysis of functional traits related to the stomatal response to drought and embolism resistance with simulations from a soil-plant hydraulic model. We report here a previously unreported phenomenon: the existence of an absolute limit by which stomata closure must occur to avoid rapid death in drought conditions. The water potential causing stomatal closure and the xylem pressure at the onset of embolism formation were equal for only a small number of species, and the difference between these two traits (i.e. safety margins) increased continuously with increasing embolism resistance. Our findings demonstrate the need to revise current views about the functional coordination between stomata and hydraulic traits and provide a mechanistic framework for modeling plant mortality under drought conditions.

SummaryThe evolution of lignified xylem allowed for the efficient transport of water under tension, but also exposed the vascular network to the risk of gas emboli and the spread of gas between xylem conduits, thus impeding sap transport to the leaves. A well-known hypothesis proposes that the safety of xylem (its ability to resist embolism formation and spread) should trade off against xylem efficiency (its capacity to transport water).We tested this safety-efficiency hypothesis in branch xylem across 335 angiosperm and 89 gymnosperm species. Safety was considered at three levels: the xylem water potentials where 12%, 50% and 88% of maximal conductivity are lost.Although correlations between safety and efficiency were weak (r 2 < 0.086), no species had high efficiency and high safety, supporting the idea for a safety-efficiency tradeoff. However, many species had low efficiency and low safety. Species with low efficiency and low safety were weakly associated (r 2 < 0.02 in most cases) with higher wood density, lower leaf-to sapwood-area and shorter stature. There appears to be no persuasive explanation for the considerable number of species with both low efficiency and low safety. These species represent a real challenge for understanding the evolution of xylem.

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.

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.

Hydraulic failure is one of the main causes of tree mortality in conditions of severe drought. Resistance to cavitation is known to be strongly related to drought tolerance and species survival in conifers, but the threshold of water-stress-induced embolism leading to catastrophic xylem dysfunction in angiosperms has been little studied. We investigated the link between drought tolerance, survival and xylem cavitation resistance in five angiosperm tree species known to have contrasting desiccation resistance thresholds. We exposed seedlings in a greenhouse to severe drought to generate extreme water stress. We monitored leaf water potential, total plant water loss rate, leaf transpiration, stomatal conductance and CO2 assimilation rate during drought exposure and after rewatering (recovery phase). The time required for the recovery of 50% of the maximum value of a given ecophysiological variable after rewatering was used to determine the critical water potential corresponding to the threshold beyond which the plant failed to recover. We also investigated the relationship between this potential and stem xylem cavitation resistance, as assessed from vulnerability curves. This minimum recoverable water potential was consistent between ecophysiological variables and varied considerably between species, from -3.4 to -6.0 MPa. This minimum recoverable water potential was strongly correlated with P50 and P88, the pressures inducing 50 and 88% losses of stem hydraulic conductance, respectively. Moreover, the embolism threshold leading to irreversible drought damage was found to be close to 88%, rather than the 50% previously reported for conifers. Hydraulic failure leading to irreversible drought-induced global dysfunction in angiosperm tree species occurred at a very high level of xylem embolism, possibly reflecting the physiological characteristics of their stem water-transport system.