John S. Sperry

Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought?

Severe droughts have been associated with regional-scale forest mortality worldwide. Climate change is expected to exacerbate regional mortality events; however, prediction remains difficult because the physiological mechanisms underlying drought survival and mortality are poorly understood. We developed a hydraulically based theory considering carbon balance and insect resistance that allowed development and examination of hypotheses regarding survival and mortality. Multiple mechanisms may cause mortality during drought. A common mechanism for plants with isohydric regulation of water status results from avoidance of drought-induced hydraulic failure via stomatal closure, resulting in carbon starvation and a cascade of downstream effects such as reduced resistance to biotic agents. Mortality by hydraulic failure per se may occur for isohydric seedlings or trees near their maximum height. Although anisohydric plants are relatively drought-tolerant, they are predisposed to hydraulic failure because they operate with narrower hydraulic safety margins during drought. Elevated temperatures should exacerbate carbon starvation and hydraulic failure. Biotic agents may amplify and be amplified by drought-induced plant stress. Wet multidecadal climate oscillations may increase plant susceptibility to drought-induced mortality by stimulating shifts in hydraulic architecture, effectively predisposing plants to water stress. Climate warming and increased frequency of extreme events will probably cause increased regional mortality episodes. Isohydric and anisohydric water potential regulation may partition species between survival and mortality, and, as such, incorporating this hydraulic framework may be effective for modeling plant survival and mortality under future climate conditions.

Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure

Wood density (Dt), an excellent predictor of mechanical properties, is typically viewed in relation to support against gravity, wind, snow, and other environmental forces. In contrast, we show the surprising extent to which variation in Dt and wood structure is linked to support against implosion by negative pressure in the xylem pipeline. The more drought-tolerant the plant, the more negative the xylem pressure can become without cavitation, and the greater the internal load on the xylem conduit walls. Accordingly, Dt was correlated with cavitation resistance. This trend was consistent with the maintenance of a safety factor from implosion by negative pressure: conduit wall span (b) and thickness (t) scaled so that (t/b)2 was proportional to cavitation resistance as required to avoid wall collapse. Unexpectedly, trends in Dt may be as much or more related to support of the xylem pipeline as to support of the plant.

Global convergence in the vulnerability of forests to drought.

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 (<1 megapascal) 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.

Functional and ecological xylem anatomy

Abstract Cohesion-tension transport of water is an energetically efficient way to carry large amounts of water from the roots up to the leaves. However, the cohesion-tension mechanism places the xylem water under negative hydrostatic pressure ( P x ), rendering it susceptible to cavitation. There are conflicts among the structural requirements for minimizing cavitation on the one hand vs maximizing efficiency of transport and construction on the other. Cavitation by freeze-thaw events is triggered by in situ air bubble formation and is much more likely to occur as conduit diameter increases, creating a direct conflict between conducting efficiency and sensitivity to freezing induced xylem failure. Temperate ring-porous trees and vines with wide diameter conduits tend to have a shorter growing season than conifers and diffuse-porous trees with narrow conduits. Cavitation by water stress occurs by air seeding at interconduit pit membranes. Pit membrane structure is at least partially uncoupled from conduit size, leading to a much less pronounced trade-off between conducting efficiency and cavitation by drought than by freezing. Although wider conduits are generally more susceptible to drought-induced cavitation within an organ, across organs or species this trend is very weak. Different trade-offs become apparent at the level of the pit membranes that interconnect neighbouring conduits. Increasing porosity of pit membranes should enhance conductance but also make conduits more susceptible to air seeding. Increasing the size or number of pit membranes would also enhance conductance, but may weaken the strength of the conduit wall against implosion. The need to avoid conduit collapse under negative pressure creates a significant trade-off between cavitation resistance and xylem construction cost, as revealed by relationships between conduit wall strength, wood density and cavitation pressure. Trade-offs involving cavitation resistance may explain the correlations between wood anatomy, cavitation resistance, and the physiological range of negative pressure experienced by species in their native habitats.

Xylem Embolism in Ring‐Porous, Diffuse‐Porous, and Coniferous Trees of Northern Utah and Interior Alaska

Xylem embolism was measured in nine tree species for one or more years. Species were ring-porous (Quercus sp.), diffuse-porous (Alnus, Betula, Populus spp.) or coniferous (Picea, Larix, Abies spp.). Intraspecific (Populus tremuloides) and intrageneric (Betula, Alnus) comparisons were made between sites in northern Utah and interior Alaska. Most embolism, >90% in some dicot species, occurred in winter. Within sites, dicot trees embolized more than conifers. Between sites, Alaskan dicot trees embolized less than their Utah counterparts. Differences were explained by vulnerability to embolism caused by freeze-thaw cycles. Most conifers were entirely resistant, whereas dicot trees were vulner- able. Less embolism in Alaskan dicot trees was associated with fewer freeze-thaw events in Alaska vs. Utah. Vulnerability was positively correlated with conduit volume and hy- draulic conductance per unit xylem area (ks). Tracheids were superior to vessels in avoiding freeze-thaw-induced embolism, and had lower k,. At the other extreme, ring-porous xylem had the highest k, but lost > 90% of hydraulic conductance after a single freeze-thaw event. Vulnerability to water-stress-induced cavitation was not correlated with conduit volume or k,. Dicot species either reversed winter embolism by refilling vessels with positive root pressures during spring (Betula, Alnus spp.), or tolerated it and relied on new xylem pro- duction to restore hydraulic conductance (Quercus sp.). Conifers reversed embolism by refilling tracheids in the absence of positive pressure. Populus species behaved inconsis- tently, showing some reversal one year but none the next. Even without embolism reversal, Populus species had hydraulic conductances per unit leaf area equal to other diffuse-porous species.

Hydraulic constraints on plant gas exchange

Stomatal conductance (gs) and transpiration (E) are often positively correlated with the hydraulic conductance of the soil‐leaf continuum (ks‐l). Interaction between gs and ks‐l helps regulate water potential (9) of leaves. When soil and plant 9 decreases during water stress, ks‐l decreases. A well-documented cause of the decrease in ks‐l is xylem cavitation. The interaction between k and 9 in xylem creates physical limits on the range of 9 and E over which gas exchange can occur. Differences in drought tolerance between species correlate with hydraulic limits. Safety margins from complete hydraulic failure are often small enough to require stomatal regulation of 9 and E. While stomatal regulation avoids complete hydraulic failure, controlled decreases in plant k can be substantial during drought. Decreasing plant k amplifies the effect of water stress on the leaves and effectively increases the sensitivity of the stomatal response to drought. Increased stomatal sensitivity may promote drought survival.

Root water uptake and transport: using physiological processes in global predictions

Plant water loss, regulated by stomata and driven by atmospheric demand, cannot exceed the maximum steady-state supply through roots. Just as an electric circuit breaks when carrying excess current, the soil-plant continuum breaks if forced to transport water beyond its capacity. Exciting new molecular, biophysical and ecological research suggests that roots are the weakest link along this hydraulic flow path. We attempt here to predict rooting depth and water uptake using the hydraulic properties of plants and the soil, and also to suggest how new physiological tools might contribute to larger-scale studies of hydraulic lift, the water balance and biosphere-atmosphere interactions.

The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off

Forest ecosystems store approximately 45% of the carbon found in terrestrial ecosystems, but they are sensitive to climate-induced dieback. Forest die-off constitutes a large uncertainty in projections of climate impacts on terrestrial ecosystems, climate–ecosystem interactions, and carbon-cycle feedbacks. Current understanding of the physiological mechanisms mediating climate-induced forest mortality limits the ability to model or project these threshold events. We report here a direct and in situ study of the mechanisms underlying recent widespread and climate-induced trembling aspen (Populus tremuloides) forest mortality in western North America. We find substantial evidence of hydraulic failure of roots and branches linked to landscape patterns of canopy and root mortality in this species. On the contrary, we find no evidence that drought stress led to depletion of carbohydrate reserves. Our results illuminate proximate mechanisms underpinning recent aspen forest mortality and provide guidance for understanding and projecting forest die-offs under climate change.

Influence of leaf water status on stomatal response to humidity, hydraulic conductance, and soil drought in Betula occidentalis

Whole-canopy measurements of water flux were used to calculate stomatal conductance (gs) and transpiration (E) for seedlings of western water birch (Betula occidentalis Hook.) under various soil-plant hydraulic conductances (k), evaporative driving forces (ΔN; difference in leaf-to-air molar fraction of water vapor), and soil water potentials (Ψs). As expected, gs dropped in response to decreased k or ΨS, or increased ΔN(> 0.025). Field data showed a decrease in mid-day gs with decreasing k from soil-to-petiole, with sapling and adult plants having lower values of both parameters than juveniles. Stomatal closure prevented E and Ψ from inducing xylem cavitation except during extreme soil drought when cavitation occurred in the main stem and probably roots as well. Although all decreases in gs were associated with approximately constant bulk leaf water potential (ψl), this does not logically exclude a feedback response between ΨL and gs. To test the influence of leaf versus root water status on gs, we manipulated water status of the leaf independently of the root by using a pressure chamber enclosing the seedling root system; pressurizing the chamber alters cell turgor and volume only in the shoot cells outside the chamber. Stomatal closure in response to increased ΔN, decreased k, and decreased ΨS was fully or partially reversed within 5 min of pressurizing the soil. Bulk ΨL remained constant before and after soil pressurizing because of the increase in E associated with stomatal opening. When ΔN was low (i.e., < 0.025), pressurizing the soil either had no effect on gs, or caused it to decline; and bulk ΨL increased. Increased Ψl may have caused stomatal closure via increased backpressure on the stomatal apparatus from elevated epidermal turgor. The stomatal response to soil pressurizing indicated a central role of leaf cells in sensing water stress caused by high ΔN, low k, and low ΨS. Invoking a prominent role for feedforward signalling in short-term stomatal control may be premature.

Size and function in conifer tracheids and angiosperm vessels

The wide size range of conifer tracheids and angiosperm vessels has important consequences for function. In both conduit types, bigger is better for conducting efficiency. The gain in efficiency with size is maximized by the control of conduit shape, which balances end-wall and lumen resistances. Although vessels are an order of magnitude longer than tracheids of the same diameter, they are not necessarily more efficient because they lack the low end-wall resistance of tracheids with torus-margo pits. Instead, vessels gain conducting efficiency over tracheids by achieving wider maximum diameters. End-walls contributed 56-64% to total xylem resistance in both conduit types, indicating that length limits conducting efficiency. Tracheid dimensions may be more limited by unicellularity and the need to supply strength to homoxylous wood than by the need to protect against cavitation. In contrast, the greater size of the multicellular vessel is facilitated by fibers that strengthen heteroxylous wood. Vessel dimensions may be most limited by the need to restrict intervessel pitting and cavitation by air-seeding. Stressful habitats that promote narrow vessels should favor coexistence of conifers and angiosperms. The evolution of vessels in angiosperm wood may have required early angiosperms to survive a phase of mechanic and hydraulic instability.