Leaves as bottlenecks: The contribution of tree leaves to hydraulic resistance within the soil-plant-atmosphere continuum.

Within vascular plants, the partitioning of hydraulic resistance along the soil-to-leaf continuum affects transpiration and its response to environmental conditions. In trees, the fractional contribution of leaf hydraulic resistance (Rleaf ) to total soil-to-leaf hydraulic resistance (Rtotal ), or fRleaf (=Rleaf /Rtotal ), is thought to be large, but this has not been tested comprehensively. We compiled a multibiome data set of fRleaf using new and previously published measurements of pressure differences within trees in situ. Across 80 samples, fRleaf averaged 0.51 (95% confidence interval [CI] = 0.46-0.57) and it declined with tree height. We also used the allometric relationship between field-based measurements of soil-to-leaf hydraulic conductance and laboratory-based measurements of leaf hydraulic conductance to compute the average fRleaf for 19 tree samples, which was 0.40 (95% CI = 0.29-0.56). The in situ technique produces a more accurate descriptor of fRleaf because it accounts for dynamic leaf hydraulic conductance. Both approaches demonstrate the outsized role of leaves in controlling tree hydrodynamics. A larger fRleaf may help stems from loss of hydraulic conductance. Thus, the decline in fRleaf with tree height would contribute to greater drought vulnerability in taller trees and potentially to their observed disproportionate drought mortality.

Mechanisms of xylem hydraulic recovery after drought in Eucalyptus saligna.

The mechanisms by which woody plants recover xylem hydraulic capacity after drought stress are not well understood, particularly with regard to the role of embolism refilling. We evaluated the recovery of xylem hydraulic capacity in young Eucalyptus saligna plants exposed to cycles of drought stress and rewatering. Plants were exposed to moderate and severe drought stress treatments, with recovery monitored at time intervals from 24 h to 6 months after rewatering. The percentage loss of xylem vessels due to embolism (PLV) was quantified at each time point using microcomputed tomography with stem water potential (Ψx ) and canopy transpiration (Ec ) measured before scans. Plants exposed to severe drought stress suffered high levels of embolism (47.38% ± 10.97% PLV) and almost complete canopy loss. No evidence of embolism refilling was observed at 24 h, 1 week, or 3 weeks after rewatering despite rapid recovery in Ψx . Recovery of hydraulic capacity was achieved over a 6-month period by growth of new xylem tissue, with canopy leaf area and Ec recovering over the same period. These findings indicate that E. saligna recovers slowly from severe drought stress, with potential for embolism to persist in the xylem for many months after rainfall events.

Differences in biochemical, gas exchange and hydraulic response to water stress in desiccation tolerant and sensitive fronds of the fern Anemia caffrorum.

Desiccation tolerant plants can survive extreme water loss in their vegetative tissues. The fern Anemia caffrorum produces desiccation tolerant (DT) fronds in the dry season and desiccation sensitive (DS) fronds in the wet season, providing a unique opportunity to explore the physiological mechanisms associated with desiccation tolerance. Anemia caffrorum plants with either DT or DS fronds were acclimated in growth chambers. Photosynthesis, frond structure and anatomy, water relations and minimum conductance to water vapour were measured under well-watered conditions. Photosynthesis, hydraulics, frond pigments, antioxidants and abscisic acid contents were monitored under water deficit. A comparison between DT and DS fronds under well-watered conditions showed that the former presented higher leaf mass per area, minimum conductance, tissue elasticity and lower CO2 assimilation. Water deficit resulted in a similar induction of abscisic acid in both frond types, but DT fronds maintained higher stomatal conductance and upregulated more prominently lipophilic antioxidants. The seasonal alternation in production of DT and DS fronds in A. caffrorum represents a mechanism by which carbon gain can be maximized during the rainy season, and a greater investment in protective mechanisms occurs during the hot dry season, enabling the exploitation of episodic water availability.

Beyond leaf habit: generalities in plant function across 97 tropical dry forest tree species.

Leaf habit has been hypothesized to define a linkage between the slow-fast plant economic spectrum and the drought resistance-avoidance trade-off in tropical forests ('slow-safe vs fast-risky'). However, variation in hydraulic traits as a function of leaf habit has rarely been explored for a large number of species. We sampled leaf and branch functional traits of 97 tropical dry forest tree species from four sites to investigate whether patterns of trait variation varied consistently in relation to leaf habit along the 'slow-safe vs fast-risky' trade-off. Leaf habit explained from 0% to 43.69% of individual trait variation. We found that evergreen and semi-deciduous species differed in their location along the multivariate trait ordination when compared to deciduous species. While deciduous species showed consistent trait values, evergreen species trait values varied as a function of the site. Last, trait values varied in relation to the proportion of deciduous species in the plant community. We found that leaf habit describes the strategies that define drought avoidance and plant economics in tropical trees. However, leaf habit alone does not explain patterns of trait variation, which suggests quantifying site-specific or species-specific uncertainty in trait variation as the way forward.

Cell wall thickness and composition are involved in photosynthetic limitation.

The key role of cell walls in setting mesophyll conductance to CO2 (gm) and, consequently, photosynthesis is reviewed. First, the theoretical properties of cell walls that can affect gm are presented. Then, we focus on cell wall thickness (Tcw) reviewing empirical evidence showing that Tcw varies strongly among species and phylogenetic groups in a way that correlates with gm and photosynthesis; that is, the thicker the mesophyll cell walls, the lower the gm and photosynthesis. Potential interplays of gm, Tcw, dehydration tolerance, and hydraulic properties of leaves are also discussed. Dynamic variations of Tcw in response to the environment and their implications in the regulation of photosynthesis are discussed, and recent evidence suggesting an influence of cell wall composition on gm is presented. We then propose a hypothetical mechanism for the influence of cell walls on photosynthesis, combining the effects of thickness and composition, particularly pectins. Finally, we discuss the prospects for using biotechnology for enhancing photosynthesis by altering cell wall-related genes.

Stability of tropical forest tree carbon-water relations in a rainfall exclusion treatment through shifts in effective water uptake depth.

Increasing severity and frequency of drought is predicted for large portions of the terrestrial biosphere, with major impacts already documented in wet tropical forests. Using a 4-year rainfall exclusion experiment in the Daintree Rainforest in northeast Australia, we examined canopy tree responses to reduced precipitation and soil water availability by quantifying seasonal changes in plant hydraulic and carbon traits for 11 tree species between control and drought treatments. Even with reduced soil volumetric water content in the upper 1 m of soil in the drought treatment, we found no significant difference between treatments for predawn and midday leaf water potential, photosynthesis, stomatal conductance, foliar stable carbon isotope composition, leaf mass per area, turgor loss point, xylem vessel anatomy, or leaf and stem nonstructural carbohydrates. While empirical measurements of aboveground traits revealed homeostatic maintenance of plant water status and traits in response to reduced soil moisture, modeled belowground dynamics revealed that trees in the drought treatment shifted the depth from which water was acquired to deeper soil layers. These findings reveal that belowground acclimation of tree water uptake depth may buffer tropical rainforests from more severe droughts that may arise in future with climate change.

Visual and hydraulic techniques produce similar estimates of cavitation resistance in woody species.

Hydraulic failure of the plant vascular system is a principal cause of forest die-off under drought. Accurate quantification of this process is essential to our understanding of the physiological mechanisms underpinning plant mortality. Imaging techniques increasingly are applied to estimate xylem cavitation resistance. These techniques allow for in situ measurement of embolism formation in real time, although the benefits and trade-offs associated with different techniques have not been evaluated in detail. Here we compare two imaging methods, microcomputed tomography (microCT) and optical vulnerability (OV), to standard hydraulic methods for measurement of cavitation resistance in seven woody species representing a diversity of major phylogenetic and xylem anatomical groups. Across the seven species, there was strong agreement between cavitation resistance values (P50 ) estimated from visualization techniques (microCT and OV) and between visual techniques and hydraulic techniques. The results indicate that visual techniques provide accurate estimates of cavitation resistance and the degree to which xylem hydraulic function is impacted by embolism. Results are discussed in the context of trade-offs associated with each technique and possible causes of discrepancy between estimates of cavitation resistance provided by visual and hydraulic techniques.

Independent genetic control of drought resistance, recovery, and growth of Eucalyptus globulus seedlings.

Drought is a major stress impacting forest ecosystems worldwide. We utilized quantitative trait loci (QTL) analysis to study the genetic basis of variation in (a) drought resistance and recovery and (b) candidate traits that may be associated with this variation in the forest tree Eucalyptus globulus. QTL analysis was performed using a large outcrossed F2 mapping population from which 300 trees were phenotyped based on the mean performance of their open-pollinated F3 progeny. Progenies were grown in a glasshouse in a randomized complete block design. A subset of seedlings was subjected to a drought treatment after which they were rewatered and scored for damage and growth postdrought. Nondroughted seedlings were assessed for growth traits as well as lignotuber size and resprouting following severe damage to the main stem. QTL were detected for most traits. Importantly, independent QTL were detected for (a) drought damage and plant size, (b) drought damage and growth recovery, and (c) lignotuber size and resprouting capacity. Such independence argues that trade-offs are unlikely to be a major limitation to the response to selection and at the early life history stage studied; there are opportunities to improve resilience to drought without adverse effects on productivity.

Guard cells in fern stomata are connected by plasmodesmata, but control cytosolic Ca2+ levels autonomously.

Recent studies have revealed that some responses of fern stomata to environmental signals differ from those of their relatives in seed plants. However, it is unknown whether the biophysical properties of guard cells differ fundamentally between species of both clades. Intracellular micro-electrodes and the fluorescent Ca2+ reporter FURA2 were used to study voltage-dependent cation channels and Ca2+ signals in guard cells of the ferns Polypodium vulgare and Asplenium scolopendrium. Voltage clamp experiments with fern guard cells revealed similar properties of voltage-dependent K+ channels as found in seed plants. However, fluorescent dyes moved within the fern stomata, from one guard cell to the other, which does not occur in most seed plants. Despite the presence of plasmodesmata, which interconnect fern guard cells, Ca2+ signals could be elicited in each of the cells individually. Based on the common properties of voltage-dependent channels in ferns and seed plants, it is likely that these key transport proteins are conserved in vascular plants. However, the symplastic connections between fern guard cells in mature stomata indicate that the biophysical mechanisms that control stomatal movements differ between ferns and seed plants.

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.

Residual transpiration as a component of salinity stress tolerance mechanism: a case study for barley.

BACKGROUND: While most water loss from leaf surfaces occurs via stomata, part of this loss also occurs through the leaf cuticle, even when the stomata are fully closed. This component, termed residual transpiration, dominates during the night and also becomes critical under stress conditions such as drought or salinity. Reducing residual transpiration might therefore be a potentially useful mechanism for improving plant performance when water availability is reduced (e.g. under saline or drought stress conditions). One way of reducing residual transpiration may be via increased accumulation of waxes on the surface of leaf. Residual transpiration and wax constituents may vary with leaf age and position as well as between genotypes. This study used barley genotypes contrasting in salinity stress tolerance to evaluate the contribution of residual transpiration to the overall salt tolerance, and also investigated what role cuticular waxes play in this process. Leaves of three different positions (old, intermediate and young) were used. RESULTS: Our results show that residual transpiration was higher in old leaves than the young flag leaves, correlated negatively with the osmolality, and was positively associated with the osmotic and leaf water potentials. Salt tolerant varieties transpired more water than the sensitive variety under normal growth conditions. Cuticular waxes on barley leaves were dominated by primary alcohols (84.7-86.9%) and also included aldehydes (8.90-10.1%), n-alkanes (1.31-1.77%), benzoate esters (0.44-0.52%), phytol related compounds (0.22-0.53%), fatty acid methyl esters (0.14-0.33%), ß-diketones (0.07-0.23%) and alkylresorcinols (1.65-3.58%). A significant negative correlation was found between residual transpiration and total wax content, and residual transpiration correlated significantly with the amount of primary alcohols. CONCLUSIONS: Both leaf osmolality and the amount of total cuticular wax are involved in controlling cuticular water loss from barley leaves under well irrigated conditions. A significant and negative relationship between the amount of primary alcohols and a residual transpiration implies that some cuticular wax constituents act as a water barrier on plant leaf surface and thus contribute to salinity stress tolerance. It is suggested that residual transpiration could be a fundamental mechanism by which plants optimize water use efficiency under stress conditions.

Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world's woody plant species.

The 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.

Stomatal dynamics are limited by leaf hydraulics in ferns and conifers: results from simultaneous measurements of liquid and vapour fluxes in leaves.

Stomatal responsiveness to vapour pressure deficit (VPD) results in continuous regulation of daytime gas-exchange directly influencing leaf water status and carbon gain. Current models can reasonably predict steady-state stomatal conductance (gs ) to changes in VPD but the gs dynamics between steady-states are poorly known. Here, we used a diverse sample of conifers and ferns to show that leaf hydraulic architecture, in particular leaf capacitance, has a major role in determining the gs response time to perturbations in VPD. By using simultaneous measurements of liquid and vapour fluxes into and out of leaves, the in situ fluctuations in leaf water balance were calculated and appeared to be closely tracked by changes in gs thus supporting a passive model of stomatal control. Indeed, good agreement was found between observed and predicted gs when using a hydropassive model based on hydraulic traits. We contend that a simple passive hydraulic control of stomata in response to changes in leaf water status provides for efficient stomatal responses to VPD in ferns and conifers, leading to closure rates as fast or faster than those seen in most angiosperms.

Unified changes in cell size permit coordinated leaf evolution.

The processes by which the functions of interdependent tissues are coordinated as lineages diversify are poorly understood. Here, we examine evolutionary coordination of vascular, epidermal and cortical leaf tissues in the anatomically, ecologically and morphologically diverse woody plant family Proteaceae. We found that, across the phylogenetic range of Proteaceae, the sizes of guard, epidermal, palisade and xylem cells were positively correlated with each other but negatively associated with vein and stomatal densities. The link between venation and stomata resulted in a highly efficient match between potential maximum water loss (determined by stomatal conductance) and the leaf vascular system's capacity to replace that water. This important linkage is likely to be driven by stomatal size, because spatial limits in the packing of stomata onto the leaf surface apparently constrain the maximum size and density of stomata. We conclude that unified evolutionary changes in cell sizes of independent tissues, possibly mediated by changes in genome size, provide a means of substantially modifying leaf function while maintaining important functional links between leaf tissues. Our data also imply the presence of alternative evolutionary strategies involving cellular miniaturization during radiation into closed forest, and cell size increase in open habitats.

Replicated Evolution in Plants.

Similar traits and functions commonly evolve in nature. Here, we explore patterns of replicated evolution across the plant kingdom and discuss the processes responsible for such patterns. We begin this review by defining replicated evolution and the theoretical, genetic, and ecological concepts that help explain it. We then focus our attention on empirical cases of replicated evolution at the phenotypic and genotypic levels. We find that replication at the ecotype level is common, but evidence for repeated ecological speciation is surprisingly sparse. On the other hand, the replicated evolution of ecological strategies and physiological mechanisms across similar biomes appears to be pervasive. We conclude by highlighting where future efforts can help us bridge the understanding of replicated evolution across different levels of biological organization. Earth's landscape is diverse but also repeats itself. Organisms seem to have followed suit.

The maximum height of grasses is determined by roots.

Grasses such as bamboos can produce upright stems more than 30 m tall, yet the processes that constrain plant height in this important group have never been investigated. Air embolisms form commonly in the water transport system of grasses and we hypothesised that root pressure-dependent refilling these embolisms should limit the maximum height of grass species to the magnitude of their root pressure. Confirming this hypothesis, we show that in 59 species of bamboo grown in two common gardens, the maximum heights of culms of 67 clones are closely predicted by the maximum measured root pressure overnight. Furthermore, we demonstrate that water transport in these bamboo species is dependent on root pressure to repair hydraulic dysfunction sustained during normal diurnal gas exchange. Our results established the critical importance of root pressure in the tallest grass species and provide a new basis for understanding the limits for plant growth.

Stem hydraulic traits and leaf water-stress tolerance are co-ordinated with the leaf phenology of angiosperm trees in an Asian tropical dry karst forest.

BACKGROUND AND AIMS: The co-occurring of evergreen and deciduous angiosperm trees in Asian tropical dry forests on karst substrates suggests the existence of different water-use strategies among species. In this study it is hypothesized that the co-occurring evergreen and deciduous trees differ in stem hydraulic traits and leaf water relationships, and there will be correlated evolution in drought tolerance between leaves and stems. METHODS: A comparison was made of stem hydraulic conductivity, vulnerability curves, wood anatomy, leaf life span, leaf pressure-volume characteristics and photosynthetic capacity of six evergreen and six deciduous tree species co-occurring in a tropical dry karst forest in south-west China. The correlated evolution of leaf and stem traits was examined using both traditional and phylogenetic independent contrasts correlations. KEY RESULTS: It was found that the deciduous trees had higher stem hydraulic efficiency, greater hydraulically weighted vessel diameter (D(h)) and higher mass-based photosynthetic rate (A(m)); while the evergreen species had greater xylem-cavitation resistance, lower leaf turgor-loss point water potential (π(0)) and higher bulk modulus of elasticity. There were evolutionary correlations between leaf life span and stem hydraulic efficiency, A(m), and dry season π(0). Xylem-cavitation resistance was evolutionarily correlated with stem hydraulic efficiency, D(h), as well as dry season π(0). Both wood density and leaf density were closely correlated with leaf water-stress tolerance and A(m). CONCLUSIONS: The results reveal the clear distinctions in stem hydraulic traits and leaf water-stress tolerance between the co-occurring evergreen and deciduous angiosperm trees in an Asian dry karst forest. A novel pattern was demonstrated linking leaf longevity with stem hydraulic efficiency and leaf water-stress tolerance. The results show the correlated evolution in drought tolerance between stems and leaves.

Leaf hydraulic vulnerability influences species' bioclimatic limits in a diverse group of woody angiosperms.

The ability of plants to maintain water flow through leaves under water stress-induced tension (assessed as the leaf hydraulic vulnerability; P50(leaf)) is intimately linked with survival. We examined the significance of P50(leaf) as an adaptive trait in influencing the dry-end distributional limits of cool temperate woody angiosperm species. We also examined differences in within-site variability in P50(leaf) between two high-rainfall montane rainforest sites in Tasmania and Peru, respectively. A significant relationship between P50(leaf) and the 5th percentile of mean annual rainfall across each species distribution was found in Tasmania, suggesting that P50(leaf) influences species climatic limits. Furthermore, a strong correlation between P50(leaf) and the minimum rainfall availability was found using five phylogenetically independent species pairs in wet and dry evergreen tree species, suggesting that rainfall is an important selective agent in the evolution of leaf hydraulic vulnerability. Greater within-site variability in P50(leaf) was found among dominant montane rainforest species in Tasmania than in Peru and this result is discussed within the context of differences in spatial and temporal environmental heterogeneity and parochial historical ecology.