Functional coordination between leaf gas exchange and vulnerability to xylem cavitation in temperate forest trees

We examined functional coordination among stem and root vulnerability to xylem cavitation, plant water transport characteristics and leaf traits in 14 co-occurring temperate tree species. Relationships were evaluated using both traditional cross-species correlations and phylogenetically independent contrast (PIC) correlations. For stems, the xylem tension at which 50% of hydraulic conductivity was lost (psi50) was positively associated (P < 0.001) with specific conductivity (K(S)) and with mean hydraulically weighted xylem conduit diameter (D(h-w)), but was only marginally (P = 0.06) associated with leaf specific conductivity (K(L)). The PIC correlation for each of these relationships, however, was not statistically significant. There was also no relationship between root psi50 and root K(S) in either cross-species or PIC analysis. Photosynthetic rate (A) and stomatal conductance (g(s)) were strongly and positively correlated with root psi50 in the cross-species analysis (P < 0.001), a relationship that was robust to phylogenetic correction (P < 0.01). A and g(s) were also positively correlated with stem psi50 in the cross-species analysis (P = 0.02 and 0.10, respectively). However, only A was associated with stem psi50 in the PIC analysis (P = 0.04). Although the relationship between vulnerability to cavitation and xylem conductivity traits within specific organs (i.e. stems and roots) was weak, the strong correlation between g(s) and root psi50 across species suggests that there is a trade-off between vulnerability to cavitation and water transport capacity at the whole-plant level. Our results were therefore consistent with the expectation of coordination between vulnerability to xylem cavitation and the regulation of stomatal conductance, and highlight the potential physiological and evolutionary significance of root hydraulic properties in controlling interspecific variation in leaf function.     

Higher rates of leaf gas exchange are associated with higher leaf hydrodynamic pressure gradients

Steady-state leaf gas-exchange parameters and leaf hydraulic conductance were measured on 10 vascular plant species, grown under high light and well-watered conditions, in order to test for evidence of a departure from hydraulic homeostasis within leaves as hydraulic conductance varied across species. The plants ranged from herbaceous crop plants to mature forest trees. Across species, under standardized environmental conditions (saturating light, well watered), mean steady-state stomatal conductance to water vapour (g(w)) was highly correlated with mean rate of CO2 assimilation (A) and mean leaf hydraulic conductance normalized to leaf area (k(leaf)). The relationship between A and g(w) was well described by a power function, while that between A and k(leaf) was highly linear. Non-linearity in the relationship between g(w) and k(leaf) contributed to an increase in the hydrodynamic (transpiration-induced) water potential drawdown across the leaf (delta psi(leaf)) as k(leaf) increased across species, although across the 10 species the total increase in delta psi(leaf) was slightly more than twofold for an almost 30-fold increase in g(w). Higher rates of leaf gas exchange were therefore associated with higher k(leaf) and higher leaf hydrodynamic pressure gradients. A mechanistic model incorporating the stomatal hydromechanical feedback loop is used to predict the relationship between delta psi(leaf) and k(leaf), and to explore the coordination of stomatal and leaf hydraulic properties in supporting higher rates of leaf gas exchange.     

Hydraulic analysis of water flow through leaves of sugar maple and red oak

Leaves constitute a substantial fraction of the total resistance to water flow through plants. A key question is how hydraulic resistance within the leaf is distributed among petiole, major veins, minor veins, and the pathways downstream of the veins. We partitioned the leaf hydraulic resistance (R(leaf)) for sugar maple (Acer saccharum) and red oak (Quercus rubra) by measuring the resistance to water flow through leaves before and after cutting specific vein orders. Simulations using an electronic circuit analog with resistors arranged in a hierarchical reticulate network justified the partitioning of total R(leaf) into component additive resistances. On average 64% and 74% of the R(leaf) was situated within the leaf xylem for sugar maple and red oak, respectively. Substantial resistance-32% and 49%- was in the minor venation, 18% and 21% in the major venation, and 14% and 4% in the petiole. The large number of parallel paths (i.e. a large transfer surface) for water leaving the minor veins through the bundle sheath and out of the leaf resulted in the pathways outside the venation comprising only 36% and 26% of R(leaf). Changing leaf temperature during measurement of R(leaf) for intact leaves resulted in a temperature response beyond that expected from changes in viscosity. The extra response was not found for leaves with veins cut, indicating that water crosses cell membranes after it leaves the xylem. The large proportion of resistance in the venation can explain why stomata respond to leaf xylem damage and cavitation. The hydraulic importance of the leaf vein system suggests that the diversity of vein system architectures observed in angiosperms may reflect variation in whole-leaf hydraulic capacity.     

The hydraulic conductivity of the xylem in conifer needles (Picea abies and Pinus mugo)

Main resistances of the plant water transport system are situated in leaves. In contrast to angiosperm leaves, knowledge of conifer needle hydraulics and of the partitioning of resistances within needles is poor. A new technique was developed which enabled flow-meter measurements through needles embedded in paraffin and thus quantification of the specific hydraulic conductivity (K(s)) of the needle xylem. In Picea abies, xylem K(s) of needle and axes as well as in needles of different age were compared. In Pinus mugo, resistance partitioning within needles was estimated by measurements of xylem K(s) and leaf conductance (K(leaf), measured via 'rehydration kinetics'). Mean K(s) in P. abies needles was 3.5×10(-4) m(2) s(-1) MPa(-1) with a decrease in older needles, and over all similar to K(s) of corresponding axes xylem. In needles of P. mugo, K(s) was 0.9×10(-4) m(2) s(-1) MPa(-1), and 24% of total needle resistance was situated in the xylem. The results indicate species-specific differences in the hydraulic efficiency of conifer needle xylem. The vascular section of the water transport system is a minor but relevant resistance in needles.     

Sequential leaf senescence and correlatively controlled increases in xylem flow resistance

In bean, Phaseolus vulgaris L. (Contender), the directly measured hydraulic resistance of the xylem pathway between roots and primary leaf pulvinal junctions increased rapidly and progressively from 21 to 28 days after planting. These increases in xylem resistance (+390%) were specifically located in the pulvinal junction of the primary leaf. Moreover, they occurred just prior to the onset of primary leaf yellowing. Developmental increases in xylem hydraulic flow resistance and stomatal resistance, as well as subsequent primary leaf yellowing, were completely prevented by detopping the shoots above the primary leaves at 21 days. Thus, the onset of these senescence-associated symptoms was correlatively controlled. In short-term investigations of the mechanisms involved, flow between petiole and cut tip of excised leaves was rapidly reduced by infiltration of 20 picomoles of soluble dextran into the xylem. Moreover, imbibition of approximately 120 picomoles of dextran by excised leaves increased stomatal resistances. A programmed secretion of hormonal concentrations of similar polysaccharides into specific xylem sections in vivo might provide a mechanism for regulating the partitioning of essential xylem supplies between leaves, thus inducing sequential leaf senescence.     

Coordination and trade‐offs between leaf and stem hydraulic traits and stomatal regulation along a spectrum of isohydry to anisohydry

The degree of plant iso/anisohydry, a widely used framework for classifying species‐specific hydraulic strategies, integrates multiple components of the whole‐plant hydraulic pathway. However, little is known about how it associates with coordination of functional and structural traits within and across different organs. We examined stem and leaf hydraulic capacitance and conductivity/conductance, stem xylem anatomical features, stomatal regulation of daily minimum leaf and stem water potential (Ψ), and the kinetics of stomatal responses to vapour pressure deficit (VPD) in six diverse woody species differing markedly in their degree of iso/anisohydry. At the stem level, more anisohydric species had higher wood density and lower native capacitance and conductivity. Like stems, leaves of more anisohydric species had lower hydraulic conductance; however, unlike stems, their leaves had higher native capacitance at their daily minimum values of leaf Ψ. Moreover, rates of VPD‐induced stomatal closure were related to intrinsic rather than native leaf capacitance and were not associated with species' degree of iso/anisohydry. Our results suggest a trade‐off between hydraulic storage and efficiency in the leaf, but a coordination between hydraulic storage and efficiency in the stem along a spectrum of plant iso/anisohydry.     

Vein recovery from embolism occurs under negative pressure in leaves of sunflower (Helianthus annuus)

Leaf veins undergo cavitation at water potentials (Psi(leaf)) commonly experienced by field-growing plants. Theoretically, embolism reversal should not be possible until xylem pressures rise by several kilopascals of atmospheric pressure, but recent evidence suggests that embolized conduits can be refilled even when surrounded by others at substantial tension (novel refilling). The present study reports 'novel refilling' occurring in leaf veins of sunflower (Helianthus annuus L.) while at Psi(leaf) = -0.33 MPa. Sixty per cent loss of vein hydraulic conductance (K(vein)) was recorded at Psi(leaf) < -0.65 MPa, while stem hydraulic conductance (K(stem)) was unaffected even at Psi(leaf) = -1.1 MPa. Loss of K(vein) was accompanied by stomatal closure. Water-stressed plants (Psi(leaf) = -1.1 MPa) were rehydrated overnight to different target water potentials achieved by using PEG at different concentrations as irrigation medium. K(vein) recovered by 50% at Psi(leaf) = -0.47 MPa and vein refilling was complete at Psi(leaf) = -0.33 MPa, i.e. well below the theoretical limit for conduit refilling (-0.05 MPa as calculated for sunflower minor veins). Mercurials supplied to detached leaves had no effect on the refilling process. Upon rehydration, recovery of K(vein) was not paralleled by recovery of whole-plant hydraulic conductance or leaf conductance to water vapour (g(L)), as a likely consequence of hydraulic failure of other components of the water pathway (root system or extravascular leaf compartments) and/or root-to-leaf chemical signalling. This is the first study providing experimental evidence for 'novel refilling' in a herbaceous dicot and highlighting the importance of this process in the leaf.     

Leaf hydraulic conductivity and photosynthesis are genetically correlated in an annual grass

Comparative studies suggest that a positive correlation between xylem water transport and photosynthesis is adaptive. A requirement for the adaptive evolution of coordination between xylem and photosynthetic functions is the presence of genetic variation and covariation for these traits within populations. Here it was determined whether there was genetic variation and covariation for leaf blade hydraulic conductivity (K(W)), photosynthetic rate (A), stomatal conductance (g(s)), and time to flowering in a population of recombinant inbred lines of Avena barbata, a Mediterranean annual grass. Significant (P < 0.05) broad-sense heritabilities (H(2)) were detected for K(W) (H(2) = 0.33), A (H(2) = 0.23) and flowering time (H(2) = 0.62), but not for g(s). Significant positive genetic covariation between A and K(W) was also observed. There was no other genetic covariation among traits. The first evidence of genetic variation for K(W) within a species was obtained. These results also indicate that there is a genetic basis for the positive association between xylem water transport and photosynthesis. The presence of significant genetic variation and covariation for these traits in natural populations would facilitate correlated evolution between xylem and leaf functions.     

Scaling of xylem vessels and veins within the leaves of oak species

General models of plant vascular architecture, based on scaling of pipe diameters to remove the length dependence of hydraulic resistance within the xylem, have attracted strong interest. However, these models have neglected to consider the leaf, an important hydraulic component; they assume all leaves to have similar hydraulic properties, including similar pipe diameters in the petiole. We examine the scaling of the leaf xylem in 10 temperate oak species, an important hydraulic component. The mean hydraulic diameter of petiole xylem vessels varied by 30% among the 10 oak species. Conduit diameters narrowed from the petiole to the midrib to the secondary veins, consistent with resistance minimization, but the power function scaling exponent differed from that predicted for stems. Leaf size was an organizing trait within and across species. These findings indicate that leaf vasculature needs to be included in whole-plant scaling models, for these to accurately reflect and predict whole-plant transport and its implications for performance and ecology.     

Changes in stomatal conductance along grass blades reflect changes in leaf structure

Identifying the consequences of grass blade morphology (long, narrow leaves) on the heterogeneity of gas exchange is fundamental to an understanding of the physiology of this growth form. We examined acropetal changes in anatomy, hydraulic conductivity and rates of gas exchange in five grass species (including C(3) and C(4) functional types). Both stomatal conductance and photosynthesis increased along all grass blades despite constant light availability. Hydraulic efficiency within the xylem remained constant along the leaf, but structural changes outside the xylem changed in concert with stomatal conductance. Stomatal density and stomatal pore index remained constant along grass blades but interveinal distance decreased acropetally resulting in a decreased path length for water movement from vascular bundle to stomate. The increase in stomatal conductance was correlated with the decreased path length through the leaf mesophyll. A strong correlation between the distance from vascular bundles to stomatal pores and stomatal conductance has been identified across species; our results suggest this relationship also exists within individual leaves.     

Water transport properties of seven woody species from the semi-arid Mu Us Sandy Land,China

Maintenance of water transport is very important for plant growth and survival. We studied seven woody species that inhabit the semi-arid Mu Us Sandy Land, China, to understand their strategies for maintaining hydraulic function. We evaluated water transport properties, including cavitation resistance, hydraulic recovery, and water loss regulation by stomatal control, which are associated with xylem structural and leaf physiological traits. We also discussed the water-use characteristics of these species by comparing them with those of species in other regions. Species with tracheids had higher levels of xylem resistance to cavitation and a smaller midday transpiration rate than the other species studied. Although species with vessels were less resistant to cavitation, some recovered hydraulic conductivity within 12 h of rehydration. Species with xylem tracheids could maintain their hydraulic function through resistance to cavitation and by relaxing xylem tension. Although species with vessels had less resistant xylem, they could maintain hydraulic function through hydraulic recovery even when xylem dysfunction occurred. Additionally, the species studied here were less resistant to cavitation than species in semi-arid environments, and equally or less resistant than species in humid environments. Rather than allow hydraulic dysfunction due to drought-induced dehydration, they may develop water absorption systems to avoid or recover quickly from hydraulic dysfunction. Thus, not only stem cavitation resistance to drought but also stem–root coordination should be considered when selecting plants for the revegetation of arid regions.     

Unraveling the Effects of Plant Hydraulics on Stomatal Closure during Water Stress in Walnut

The objectives of the study were to identify the relevant hydraulic parameters associated with stomatal regulation during water stress and to test the hypothesis of a stomatal control of xylem embolism in walnut (Juglans regia x nigra) trees. The hydraulic characteristics of the sap pathway were experimentally altered with different methods to alter plant transpiration (Eplant) and stomatal conductance (gs). Potted trees were exposed to a soil water depletion to alter soil water potential (Psisoil), soil resistance (Rsoil), and root hydraulic resistances (Rroot). Soil temperature was changed to alter Rroot alone. Embolism was created in the trunk to increase shoot resistance (Rshoot). Stomata closed in response to these stresses with the effect of maintaining the water pressure in the leaf rachis xylem (P(rachis)) above -1.4 MPa and the leaf water potential (Psileaf) above -1.6 MPa. The same dependence of Eplant and gs on P(rachis) or Psileaf was always observed. This suggested that stomata were not responding to changes in Psisoil, Rsoil, Rroot, or Rshoot per se but rather to their impact on P(rachis) and/or Psileaf. Leaf rachis was the most vulnerable organ, with a threshold P(rachis) for embolism induction of -1.4 MPa. The minimum Psileaf values corresponded to leaf turgor loss point. This suggested that stomata are responding to leaf water status as determined by transpiration rate and plant hydraulics and that P(rachis) might be the physiological parameter regulated by stomatal closure during water stress, which would have the effect of preventing extensive developments of cavitation during water stress.     

The distribution of xylem hydraulic resistance in the fruiting truss of tomato

The distribution of hydraulic resistances in xylem throughout the pathway leading to the tomato fruit was investigated. Previous work had indicated that there were large resistances within the supporting sections of this pathway (the peduncle and pedicel), perhaps associated with interruptions in the xylem. These high resistances are believed to impede calcium flux into the fruit and thus impair fruit development. It is shown here that fruit on intact plants do not shrink detectably during drought, even when the drought is sufficient to cause marked shrinkage of leaves and visible wilting of the shoot. In explants, it is possible to induce back‐flow from the fruit into the stem (probably via the xylem) but this flow is small and very slow. These observations support the view that there is a large hydraulic resistance in the pathway between fruit and stem. When pulses of water were made available within explants, by scorching of one leaflet, there was a rapid swelling of leaves and sepals. Such rapid fluxes indicate the presence of strong hydraulic (xylem) connections throughout the pathway between leaf and calyx. This shows that there are no significant hydraulic constrictions in the xylem proximal to the calyx. This finding is contrary to some previous conclusions but it is supported by experiments with dyes which showed continuous, functional xylem throughout the peduncle and pedicel. Calculations show that over 90% of the hydraulic resistance between stem and fruit must reside within the fruit pericarp. Implications for calcium nutrition are discussed.     

Anisohydric but isohydrodynamic: seasonally constant plant water potential gradient explained by a stomatal control mechanism incorporating variable plant hydraulic conductance

Isohydric and anisohydric regulations of plant water status have been observed over several decades of field, glasshouse and laboratory studies, yet the functional significance and mechanism of both remain obscure. We studied the seasonal trends in plant water status and hydraulic properties in a natural stand of Eucalyptus gomphocephala through cycles of varying environmental moisture (rainfall, groundwater depth, evaporative demand) in order to test for isohydry and to provide physiological information for the mechanistic interpretation of seasonal trends in plant water status. Over a 16 month period of monitoring, spanning two summers, midday leaf water potential (psi(leaf)) correlated with predawn psi(leaf), which was correlated with water table depth below ground level, which in turn was correlated with total monthly rainfall. Eucalyptus gomphocephala was therefore not seasonally isohydric. Despite strong stomatal down-regulation of transpiration rate in response to increasing evaporative demand, this was insufficient to prevent midday psi(leaf) from falling to levels below -2 MPa in the driest month, well into the region likely to induce xylem air embolisms, based on xylem vulnerability curves obtained in the study. However, even though midday psi(leaf) varied by over 1.2 MPa across seasons, the hydrodynamic (transpiration-induced) water potential gradient from roots to shoots (delta psi(plant)), measured as the difference between predawn and midday psi(leaf), was relatively constant across seasons, averaging 0.67 MPa. This unusual pattern of hydraulic regulation, referred to here as isohydrodynamic, is explained by a hydromechanical stomatal control model where plant hydraulic conductance is dependent on transpiration rate.     

Correlated evolution of stem and leaf hydraulic traits in Pereskia (Cactaceae)

Recent studies have demonstrated significant correlations between stem and leaf hydraulic properties when comparing across species within ecological communities. This implies that these traits are co-evolving, but there have been few studies addressing plant water relations within an explicitly evolutionary framework. This study tests for correlated evolution among a suite of plant water-use traits and environmental parameters in seven species of Pereskia (Cactaceae), using phylogenetically independent contrasts. There were significant evolutionary correlations between leaf-specific xylem hydraulic conductivity, Huber Value, leaf stomatal pore index, leaf venation density and leaf size, but none of these traits appeared to be correlated with environmental water availability; only two water relations traits - mid-day leaf water potentials and photosynthetic water use efficiency - correlated with estimates of moisture regime. In Pereskia, it appears that many stem and leaf hydraulic properties thought to be critical to whole-plant water use have not evolved in response to habitat shifts in water availability. This may be because of the extremely conservative stomatal behavior and particular rooting strategy demonstrated by all Pereskia species investigated. These results highlight the need for a lineage-based approach to understand the relative roles of functional traits in ecological adaptation.     

Relations between stomatal closure, leaf turgor and xylem vulnerability in eight tropical dry forest trees

This study examined the linkage between xylem vulnerability, stomatal response to leaf water potential (Ψ_L), and loss of leaf turgor in eight species of seasonally dry tropical forest trees. In order to maximize the potential variation in these traits species that exhibit a range of leaf habits and phenologies were selected. It was found that in all species stomatal conductance was responsive to Ψ_L over a narrow range of water potentials, and that Ψ_L inducing 50% stomatal closure was correlated with both the Ψ_L inducing a 20% loss of xylem hydraulic conductivity and leaf water potential at turgor loss in all species. In contrast, there was no correlation between the water potential causing a 50% loss of conductivity in the stem xylem, and the water potential at stomatal closure (Ψ_SC) amongst species. It was concluded that although both leaf and xylem characters are correlated with the response of stomata to Ψ_L, there is considerable flexibility in this linkage. The range of responses is discussed in terms of the differing leaf‐loss strategies exhibited by these species.     

Sensitivity of stem and petiole hydraulic conductance of deciduous trees to xylem sap ion concentration

Hydraulic conductance of stem and petioles increased in response to an increase in xylem sap ion concentration, and decreased in response to a decrease in the ion concentration in six temperate deciduous tree species. The ion sensitivity of hydraulic conductance of stem and petioles was higher than the ion sensitivity of the stem alone. The ion sensitivity was lowest in the earliest developmental stages of the xylem, and had a seasonal maximum in the second half of summer. The ion sensitivity was highest in slow-growing species and lowest in fast-growing species. The ion sensitivity correlated negatively with mean radius of xylem conduits, hydraulic conductance of stem and petioles, hydraulic conductance of leaf laminae, and stomatal conductance, and positively with response of the hydraulic conductance of leaf laminae to HgCl₂, and stomatal response to a decrease in leaf water potential or abscisic acid. It was concluded that the high ion sensitivity of xylem hydraulic conductance is a relevant characteristic of slow growth and a conservative water use strategy.     

Internal coordination between hydraulics and stomatal control in leaves

The stomatal response to changing leaf-atmospheric vapour pressure gradient (D(l)) is a crucial yet enigmatic process that defines the daily course of leaf gas exchange. Changes in the hydration of epidermal cells are thought to drive this response, mediated by the transpiration rate and hydraulic conductance of the leaf. Here, we examine whether species-specific variation in the sensitivity of leaves to perturbation of D(l) is related to the efficiency of water transport in the leaf (leaf hydraulic conductivity, K(leaf)). We found good correlation between maximum liquid (K(leaf)) and gas phase conductances (g(max)) in leaves, but there was no direct correlation between normalized D(l) sensitivity and K(leaf). The impact of K(leaf) on D(l) sensitivity in our diverse sample of eight species was important only after accounting for the strong relationship between K(leaf) and g(max). Thus, the ratio of g(max)/K(leaf) was strongly correlated with stomatal sensitivity to D(l). This ratio is an index of the degree of hydraulic buffering of the stomata against changes in D(l), and species with high g(max) relative to K(leaf) were the most sensitive to D(l) perturbation. Despite the potentially high adaptive significance of this phenomenon, we found no significant phylogenetic or ecological trend in our species.     

Tree hydraulic traits are coordinated and strongly linked to climate‐of‐origin across a rainfall gradient

Plant hydraulic traits capture the impacts of drought stress on plant function, yet vegetation models lack sufficient information regarding trait coordination and variation with climate‐of‐origin across species. Here, we investigated key hydraulic and carbon economy traits of 12 woody species in Australia from a broad climatic gradient, with the aim of identifying the coordination among these traits and the role of climate in shaping cross‐species trait variation. The influence of environmental variation was minimized by a common garden approach, allowing us to factor out the influence of environment on phenotypic variation across species. We found that hydraulic traits (leaf turgor loss point, stomatal sensitivity to drought [P_gs], xylem vulnerability to cavitation [P_x], and branch capacitance [C_branch]) were highly coordinated across species and strongly related to rainfall and aridity in the species native distributional range. In addition, trade‐offs between drought tolerance and plant growth rate were observed across species. Collectively, these results provide critical insight into the coordination among hydraulic traits in modulating drought adaptation and will significantly advance our ability to predict drought vulnerability in these dominant trees species.     

Diversity of hydraulic traits in nine Cordia species growing in tropical forests with contrasting precipitation

Inter- and intraspecific variation in hydraulic traits was investigated in nine Cordia (Boraginaceae) species growing in three tropical rainforests differing in mean annual precipitation (MAP). Interspecific variation was examined for the different Cordia species found at each site, and intraspecific variation was studied in populations of the widespread species Cordia alliodora across the three sites. Strong intra- and interspecific variation were observed in vulnerability to drought-induced embolism. Species growing at drier sites were more resistant to embolism than those growing at moister sites; the same pattern was observed for populations of C. alliodora. By contrast, traits related to hydraulic capacity, including stem xylem vessel diameter, sapwood specific conductivity (K(s)) and leaf specific conductivity (K(L)), varied strongly but independently of MAP. For C. alliodora, xylem anatomy, K(s), K(L) and Huber value varied little across sites, with K(s) and K(L) being consistently high relative to other Cordia species. A constitutively high hydraulic capacity coupled with plastic or genotypic adjustment in vulnerability to embolism and leaf water relations would contribute to the ability of C. alliodora to establish and compete across a wide precipitation gradient.