Hydraulic Leaf Research Articles

Leaf hydraulics I: Scaling transport properties from single cells to tissues

In leaf tissues, water may move through the symplast or apoplast as a liquid, or through the airspace as vapor, but the dominant path remains in dispute. This is due, in part, to a lack of models that describe these three pathways in terms of experimental variables. We show that, in plant water relations theory, the use of a hydraulic capacity in a manner analogous to a thermal capacity, though it ignores mechanical interactions between cells, is consistent with a special case of the more general continuum mechanical theory of linear poroelasticity. The resulting heat equation form affords a great deal of analytical simplicity at a minimal cost: we estimate an expected error of less than 12%, compared to the full set of equations governing linear poroelastic behavior. We next consider the case for local equilibrium between protoplasts, their cell walls, and adjacent air spaces during isothermal hydration transients to determine how accurately simple volume averaging of material properties (a ‘composite’ model) describes the hydraulic properties of leaf tissue. Based on typical hydraulic parameters for individual cells, we find that a composite description for tissues composed of thin walled cells with air spaces of similar size to the cells, as in photosynthetic tissues, is a reasonable preliminary assumption. We also expect isothermal transport in such cells to be dominated by the aquaporin-mediated cell-to-cell path. In the non-isothermal case, information on the magnitude of the thermal gradients is required to assess the dominant phase of water transport, liquid or vapor.

Leaf hydraulics II: Vascularized tissues

Current models of leaf hydration employ an Ohm's law analogy of the leaf as an ideal capacitor, neglecting the resistance to flow between cells, or treat the leaf as a plane sheet with a source of water at fixed potential filling the mid-plane, neglecting the discrete placement of veins as well as their resistance. We develop a model of leaf hydration that considers the average conductance of the vascular network to a representative areole (region bounded by the vascular network), and represent the volume of tissue within the areole as a poroelastic composite of cells and air spaces. Solutions to the 3D flow problem are found by numerical simulation, and these results are then compared to 1D models with exact solutions for a range of leaf geometries, based on a survey of temperate woody plants. We then show that the hydration times given by these solutions are well approximated by a sum of the ideal capacitor and plane sheet times, representing the time for transport through the vasculature and tissue respectively. We then develop scaling factors relating this approximate solution to the 3D model, and examine the dependence of these scaling factors on leaf geometry. Finally, we apply a similar strategy to reduce the dimensions of the steady state problem, in the context of peristomatal transpiration, and consider the relation of transpirational gradients to equilibrium leaf water potential measurements.

Hydraulic engineering of the angiosperm leaf: do the Baileyan trends in perforation plate evolution account for the origin of high vein density?

Hydraulic engineering of the angiosperm leaf: do the Baileyan trends in perforation plate evolution account for the origin of high vein density?

Regulation of Arabidopsis Leaf Hydraulics Involves Light-Dependent Phosphorylation of Aquaporins in Veins

The water status of plant leaves depends on the efficiency of the water supply, from the vasculature to inner tissues. This process is under hormonal and environmental regulation and involves aquaporin water channels. In Arabidopsis thaliana, the rosette hydraulic conductivity (Kros) is higher in darkness than it is during the day. Knockout plants showed that three plasma membrane intrinsic proteins (PIPs) sharing expression in veins (PIP1;2, PIP2;1, and PIP2;6) contribute to rosette water transport, and PIP2;1 can fully account for Kros responsiveness to darkness. Directed expression of PIP2;1 in veins of a pip2;1 mutant was sufficient to restore Kros. In addition, a positive correlation, in both wild-type and PIP2;1-overexpressing plants, was found between Kros and the osmotic water permeability of protoplasts from the veins but not from the mesophyll. Thus, living cells in veins form a major hydraulic resistance in leaves. Quantitative proteomic analyses showed that light-dependent regulation of Kros is linked to diphosphorylation of PIP2;1 at Ser-280 and Ser-283. Expression in pip2;1 of phosphomimetic and phosphorylation-deficient forms of PIP2;1 demonstrated that phosphorylation at these two sites is necessary for Kros enhancement under darkness. These findings establish how regulation of a single aquaporin isoform in leaf veins critically determines leaf hydraulics.

Regulation of leaf hydraulics: from molecular to whole plant levels.

The water status of plant leaves is dependent on both stomatal regulation and water supply from the vasculature to inner tissues. The present review addresses the multiple physiological and mechanistic facets of the latter process. Inner leaf tissues contribute to at least a third of the whole resistance to water flow within the plant. Physiological studies indicated that leaf hydraulic conductance (Kleaf) is highly dependent on the anatomy, development and age of the leaf and can vary rapidly in response to physiological or environmental factors such as leaf hydration, light, temperature, or nutrient supply. Differences in venation pattern provide a basis for variations in Kleaf during development and between species. On a short time (hour) scale, the hydraulic resistance of the vessels can be influenced by transpiration-induced cavitations, wall collapses, and changes in xylem sap composition. The extravascular compartment includes all living tissues (xylem parenchyma, bundle sheath, and mesophyll) that transport water from xylem vessels to substomatal chambers. Pharmacological inhibition and reverse genetics studies have shown that this compartment involves water channel proteins called aquaporins (AQPs) that facilitate water transport across cell membranes. In many plant species, AQPs are present in all leaf tissues with a preferential expression in the vascular bundles. The various mechanisms that allow adjustment of Kleaf to specific environmental conditions include transcriptional regulation of AQPs and changes in their abundance, trafficking, and intrinsic activity. Finally, the hydraulics of inner leaf tissues can have a strong impact on the dynamic responses of leaf water potential and stomata, and as a consequence on plant carbon economy and leaf expansion growth. The manipulation of these functions could help optimize the entire plant performance and its adaptation to extreme conditions over short and long time scales.

Habitat specialization and the role of trait lability in structuring diverse willow (genusSalix) communities

The co‐occurrence of closely related species is challenging to explain because biotic filters are expected to limit the ecological similarity of species within communities. To investigate the mechanisms important in facilitating species' co‐occurrence in diverse willow and poplar communities, we examined functional diversity and community phylogenetic structure along a hydrologic gradient. We focused on traits related to drought tolerance, leaf hydraulics, and recruitment, and examined species' phylogenetic relatedness and trait lability using a molecular phylogeny. Within habitats, species exhibited phenotypic clustering, and across the landscape, species distributions were correlated with their functional traits in a manner consistent with environmental filtering. With increasing water availability, communities changed from being phylogenetically even to being phylogenetically clustered. We suggest that this shift results from environmental filtering acting on conserved traits in wet habitats and labile traits in dry habitats. Taken together, these results suggest that environmental filtering is important to community assembly along the entire hydrologic gradient within this system. Although many of the traits important to habitat specialization in upland habitats are phylogenetically labile, species' habitat affinity is phylogenetically conserved overall, indicating that niche conservatism can occur as an emergent property despite trait lability. This study demonstrates the complementary nature of trait and community phylogenetic analyses and how these methods can be used to better understand the processes involved in community assembly along environmental gradients.

Alternative methods for scaling leaf hydraulic conductance offer new insights into the structure-function relationships of sun and shade leaves.

Hydraulic conductance (Kleaf) and morpho-anatomical parameters were measured in sun and shade Quercus ilex L. (holm oak) leaves. Sun leaves had lower surface area (Aleaf) and volume (Vleaf) and higher specific mass (leaf mass per area, LMA) than shade leaves. Transpiration rate and Kleaf scaled by Aleaf (Kleaf_area) were 2-fold higher in sun than in shade leaves. Kleaf_area was not correlated with vein density or stomatal density, which were found to be similar in the two leaf types. Values of Kleaf scaled by Vleaf or leaf dry weight (Kleaf_dw) were only 40% higher in sun than in shade leaves, suggesting that structural changes of Holm oak leaves acclimating to different light intensities enhance water transport to the unit evaporating leaf surface area, while maintaining more constant hydraulic supply to mesophyll cells and carbon costs of the water transport system. Sun leaves had higher Kleaf_dw and LMA than shade ones, indicating that high LMA resulted from resource allocation involved in both water transport and structural rigidity. Future studies of the intra- and inter-specific variability of mass-based hydraulic efficiency might provide important insights into leaf hydraulics and carbon economy. Kleaf_dw might prove to be an important driver of plant acclimation and adaptation to the environment.

Contrasting drought survival strategies of sympatric willows (genus: Salix): consequences for coexistence and habitat specialization

Many willow species (genus: Salix) co-occur within habitats (α-diversity) and across the landscape (β-diversity) throughout North America. This high diversity is challenging to explain because closely related species often share similar functional traits and thus experience heightened competition and shared pest and pathogen susceptibility. To investigate whether traits related to drought survival are important in maintaining diversity, we conducted an experimental dry-down on six willow species in a greenhouse. We compared species' growth rates, stem and leaf hydraulics, leaf function and dieback and examined potential associations between their drought responses and habitat affinities. Habitat affinities were characterized based on species occurrence in randomly established field plots in central Minnesota. Overall, species that occur in drier, more seasonally variable habitats tended to have higher water-use efficiency, and faster growth rates than species from wetter habitats. However, the greatest difference in drought survival strategies was found between two species with similar habitat affinities. We conclude that differences in willow species could be important in both driving habitat differentiation and permitting temporal differentiation in resource utilization within habitats. Therefore, species' water-use strategies could be important in maintaining both α- and β-diversity across the landscape.

Decoding Leaf Hydraulics with a Spatially Explicit Model: Principles of Venation Architecture and Implications for Its Evolution

Leaf venation architecture is tremendously diverse across plant species. Understanding the hydraulic functions of given venation traits can clarify the organization of the vascular system and its adaptation to environment. Using a spatially explicit model (the program K_leaf), we subjected realistic simulated leaves to modifications and calculated the impacts on xylem and leaf hydraulic conductance (K(x) and K(leaf), respectively), important traits in determining photosynthesis and growth. We tested the sensitivity of leaves to altered vein order conductivities (1) in the absence or (2) presence of hierarchical vein architecture, (3) to major vein tapering, and (4) to modification of vein densities (length/leaf area). The K(x) and K(leaf) increased with individual vein order conductivities and densities; for hierarchical venation systems, the greatest impact was from increases in vein conductivity for lower vein orders and increases in density for higher vein orders. Individual vein order conductivities were colimiting of K(x) and K(leaf), as were their densities, but the effects of vein conductivities and densities were orthogonal. Both vein hierarchy and vein tapering increased K(x) relative to xylem construction cost. These results highlight the important consequences of venation traits for the economics, ecology, and evolution of plant transport capacity.

Leafminers help us understanding leaf hydraulic design

Leaf hydraulics of Aesculus hippocastanum L. were measured over the growing season and during extensive leaf mining by the larvae of an invasive moth (Cameraria ohridella Deschka et Dimic) that specifically destroy the palisade tissue. Leaves showed seasonal changes in hydraulic resistance (R(lamina)) which were related to ontogeny. After leaf expansion was complete, the hydraulic resistance of leaves and the partitioning of resistances between vascular and extra-vascular compartments remained unchanged despite extensive disruption of the palisade by leafminers (up to 50%). This finding suggests that water flow from the petiole to the evaporation sites might not directly involve the palisade cells. The analysis of the temperature dependence of R(lamina) in terms of Q(10) revealed that at least one transmembrane step was involved in water transport outside the leaf vasculature. Anatomical analysis suggested that this symplastic step may be located at the bundle sheath where the apoplast is interrupted by hydrophobic thickening of cell walls. Our findings offer some support to the view of a compartmentalization of leaves into well-organized water pools so that the transpiration stream would involve veins, bundle sheath and spongy parenchyma, while the palisade tissue would be largely by-passed with the possible advantage of protecting cells from short-term fluctuations in water status.

Leaf hydraulics and drought stress: response, recovery and survivorship in four woody temperate plant species

Efficient conduction of water inside leaves is essential for leaf function, yet the hydraulic-mediated impact of drought on gas exchange remains poorly understood. Here we examine the decline and subsequent recovery of leaf water potential (Psi(leaf)), leaf hydraulic conductance (K(leaf)), and midday transpiration (E) in four temperate woody species exposed to controlled drought conditions ranging from mild to lethal. During drought the vulnerability of K(leaf) to declining Psi(leaf) varied greatly among the species sampled. Following drought, plants were rewatered and the rate of E and K(leaf) recovery was found to be strongly dependent on the severity of the drought imposed. Gas exchange recovery was strongly correlated with the relatively slow recovery of K(leaf) for three of the four species, indicating conformity to a hydraulic-stomatal limitation model of plant recovery. However, there was also a shift in the sensitivity of stomata to Psi(leaf) suggesting that the plant hormone abscisic acid may be involved in limiting the rate of stomatal reopening. The level of drought tolerance varied among the four species and was correlated with leaf hydraulic vulnerability. These results suggest that species-specific variation in hydraulic properties plays a fundamental role in steering the dynamic response of plants during recovery.

Mechanical properties and impedance model for the branching network of the sapping system in the leaf of Hydrangea Macrophylla

An electrical analogue model has been developed based on main leaf hydraulics characteristics and intrinsic geometry. The simulations show good qualitative agreements with specialized literature reports. The constant-phase behavior and the variation with ambient temperature of the frequency response of the leaf impedance are assessed by means of simulation studies.

Independence of stem and leaf hydraulic traits in six Euphorbiaceae tree species with contrasting leaf phenology.

Hydraulic traits and hydraulic-related structural properties were examined in three deciduous (Hevea brasiliensis, Macaranga denticulate, and Bischofia javanica) and three evergreen (Drypetes indica, Aleurites moluccana, and Codiaeum variegatum) Euphorbiaceae tree species from a seasonally tropical forest in south-western China. Xylem water potential at 50% loss of stem hydraulic conductivity (P50stem) was more negative in the evergreen tree, but leaf water potential at 50% loss of leaf hydraulic conductivity (P50leaf) did not function as P50stem did. Furthermore, P50stem was more negative than P50leaf in the evergreen tree; contrarily, this pattern was not observed in the deciduous tree. Leaf hydraulic conductivity overlapped considerably, but stem hydraulic conductivity diverged between the evergreen and deciduous tree. Correspondingly, structural properties of leaves overlapped substantially; however, structural properties of stem diverged markedly. Consequently, leaf and stem hydraulic traits were closely correlated with leaf and stem structural properties, respectively. Additionally, stem hydraulic efficiency was significantly correlated with stem hydraulic resistance to embolism; nevertheless, such a hydraulic pattern was not found in leaf hydraulics. Thus, these results suggest: (1) that the evergreen and deciduous tree mainly diverge in stem hydraulics, but not in leaf hydraulics, (2) that regardless of leaf or stem, their hydraulic traits result primarily from structural properties, and not from leaf phenology, (3) that leaves are more vulnerable to drought-induced embolism than stem in the evergreen tree, but not always in the deciduous tree and (4) that there exists a trade-off between hydraulic efficiency and safety for stem hydraulics, but not for leaf hydraulics.

Leaf hydraulic conductance, measured in situ, declines and recovers daily: leaf hydraulics, water potential and stomatal conductance in four temperate and three tropical tree species

Adequate leaf hydraulic conductance (Kleaf) is critical for preventing transpiration-induced desiccation and subsequent stomatal closure that would restrict carbon gain. A few studies have reported midday depression of Kleaf (or petiole conductivity) and its subsequent recovery in situ, but the extent to which this phenomenon is universal is not known. The objectives of this study were to measure Kleaf, using a rehydration kinetics method, (1) in the laboratory (under controlled conditions) across a range of water potentials to construct vulnerability curves (VC) and (2) over the course of the day in the field along with leaf water potential and stomatal conductance (gs). Two broadleaf (one evergreen, Arbutus menziesii Pursh., and one deciduous, Quercus garryana Dougl.) and two coniferous species (Pinus ponderosa Dougl. and Pseudotsuga menziesii [Mirbel]) were chosen as representative of different plant types. In addition, Kleaf in the laboratory and leaf water potential in the field were measured for three tropical evergreen species (Protium panamense (Rose), Tachigalia versicolor Standley and L.O. Williams and Vochysia ferruginea Mart) to predict their daily changes in field Kleaf in situ. It was hypothesized that in the field, leaves would close their stomata at water potential thresholds at which Kleaf begins to decline sharply in laboratory-generated VC, thus preventing substantial losses of Kleaf. The temperate species showed a 15-66% decline in Kleaf by midday, before stomatal closure. Although there were substantial midday declines in Kleaf, recovery was nearly complete by late afternoon. Stomatal conductance began to decrease in Pseudotsuga, Pinus and Quercus once Kleaf began to decline; however, there was no detectable reduction in gs in Arbutus. Predicted Kleaf in the tropical species, based on laboratory-generated VC, decreased by 74% of maximum Kleaf in Tachigalia, but only 22-32% in Vochysia and Protium. The results presented here, from the previous work of the authors and from other published studies, were consistent with two different strategies regarding daily maintenance of Kleaf: (1) substantial loss and subsequent recovery or (2) a more conservative strategy of loss avoidance.

Genetic analysis of leaf hydraulics in sunflower (Helianthus annuus L.) under drought stress

Improvement in leaf hydraulics is directly related to the improvement of plant tolerance to drought stress. Therefore, a field and pot experiment was carried out to determine the type of genetic variability and selection of parental types on the basis of combining ability for leaf hydraulics. Genotypes showed similar performance in both experiments; higher values were shown by drought tolerant genotypes in all traits except for osmotic potential, which drought tolerant genotypes maintained lower. Osmotic adjustment in pot experiment showed the highest magnitude of additive type of genetic variability. Female showed a higher and significant contribution of general combining ability effects as compared to male; it suggests that within genotypes female rather than male mostly contribute for additive genes. AMES-10103 showed the highest general combining ability effects for traits such as turgor pressure and osmotic adjustment.

The hydraulic conductance of Fraxinus ornus leaves is constrained by soil water availability and coordinated with gas exchange rates

Leaf hydraulic conductance (Kleaf) is known to be an important determinant of plant gas exchange and photosynthesis. Little is known about the long-term impact of different environmental factors on the hydraulic construction of leaves and its eventual consequences on leaf gas exchange. In this study, we investigate the impact of soil water availability on Kleaf of Fraxinus ornus L. as well as the influence of Kleaf on gas exchange rates and plant water status. With this aim, Kleaf, leaf conductance to water vapour (gL), leaf water potential (Psileaf) and leaf mass per area (LMA) were measured in F. ornus trees, growing in 21 different sites with contrasting water availability. Plants growing in arid sites had lower Kleaf, gL and Psileaf than those growing in sites with higher water availability. On the contrary, LMA was similar in the two groups. The Kleaf values recorded in sites with two different levels of soil water availability were constantly different from each other regardless of the amount of precipitation recorded over 20 days before measurements. Moreover, Kleaf was correlated with gL values. Our data suggest that down-regulation of Kleaf is a component of adaptation of plants to drought-prone habitats. Low Kleaf implies reduced gas exchange which may, in turn, influence the climatic conditions on a local/regional scale. It is concluded that leaf hydraulics and its changes in response to resource availability should receive greater attention in studies aimed at modelling biosphere-atmosphere interactions.

The Fossil Record of Plant Physiology and Development—What Leaves Can Tell Us

Plants provide unmatched opportunities to evaluate long debated evolutionary patterns in terms of the detailed biology of the fossil organisms. Leaves serve here as an example of how those advantages can be exploited. Over the history of vascular plants, three important transitions in leaf evolution—the origin of laminate leaves, the progressive loss of seed plant morphological diversity, and the evolution of more angiosperm-like leaves—also represent major shifts in leaf development and physiology. These transitions often occurred in parallel in different lineages, such as the evolution of marginal growth in each of at least four independent origins of laminate leaves during the Devonian and Carboniferous. Each also entailed dramatic reorganizations of leaf hydraulics. For example, the length of the finest distributary vein order varies from up to tens of centimeters down to hundreds of microns in successive groups of dominant seed plants. Angiosperms impose an additional trend upon these patterns with the evolution of their uniquely high vein densities. Vein density strongly influences and can provide a proxy for other physiological characteristics, such as assimilation and transpiration rates. The large increase in transpiration capacity accompanying the evolution of angiosperm leaf traits may even play an important role in feeding precipitation and thereby altering local climate.

Stem and leaf hydraulics of congeneric tree species from adjacent tropical savanna and forest ecosystems

Leaf and stem functional traits related to plant water relations were studied for six congeneric species pairs, each composed of one tree species typical of savanna habitats and another typical of adjacent forest habitats, to determine whether there were intrinsic differences in plant hydraulics between these two functional types. Only individuals growing in savanna habitats were studied. Most stem traits, including wood density, the xylem water potential at 50% loss of hydraulic conductivity, sapwood area specific conductivity, and leaf area specific conductivity did not differ significantly between savanna and forest species. However, maximum leaf hydraulic conductance (K (leaf)) and leaf capacitance tended to be higher in savanna species. Predawn leaf water potential and leaf mass per area were also higher in savanna species in all congeneric pairs. Hydraulic vulnerability curves of stems and leaves indicated that leaves were more vulnerable to drought-induced cavitation than terminal branches regardless of genus. The midday K (leaf) values estimated from leaf vulnerability curves were very low implying that daily embolism repair may occur in leaves. An electric circuit analog model predicted that, compared to forest species, savanna species took longer for their leaf water potentials to drop from predawn values to values corresponding to 50% loss of K (leaf) or to the turgor loss points, suggesting that savanna species were more buffered from changes in leaf water potential. The results of this study suggest that the relative success of savanna over forest species in savanna is related in part to their ability to cope with drought, which is determined more by leaf than by stem hydraulic traits. Variation among genera accounted for a large proportion of the total variance in most traits, which indicates that, despite different selective pressures in savanna and forest habitats, phylogeny has a stronger effect than habitat in determining most hydraulic traits.

Impairment of leaf hydraulics in young plants of Citrus aurantium (sour orange) infected by Phoma tracheiphila.

Phoma trachephila (Petri) Kantschaveli et Gikachvili causes dieback of several Citrus species. The impact of this fungus on leaf hydraulics was studied in Citrus aurantium L. (sour orange) with the aim of identifying the primary mechanism of damage to leaves. Leaves inoculated with a conidial suspension were measured for conductance to water vapor (gL) and specific hydraulic conductance (Kleaf) every 3 days after inoculation. The earliest symptom of infection consisted of vein chlorosis. Functional vein density (FVD) was monitored and microscopic observations were made of major vein conduits. Impairment of vein hydraulics started 25 days after inoculation with a losses of Kleaf of 40% and gL of ~60%. Most minor veins within chlorotic areas were no longer functioning and some conduits of the major veins showed digested interconduit pits leading to vein cavitation. The close Kleaf-FVD relationship revealed that vein impairment caused drop of Kleaf and, consequently, of gL at chlorotic areas. Leaf infection was focused to veins that were first forced to embolise and then invaded by fungal hyphae. The vein embolism due to the Phoma amplifies the native dominant hydraulic resistance of leaf veins, and leads ultimately to early shedding of infected leaves.

How do leaf hydraulics limit stomatal conductance at high water vapour pressure deficits?

A reduction in leaf stomatal conductance (g) with increasing leaf-to-air difference in water vapour pressure (D) is nearly ubiquitous. Ecological comparisons of sensitivity have led to the hypothesis that the reduction in g with increasing D serves to maintain leaf water potentials above those that would cause loss of hydraulic conductance. A reduction in leaf water potential is commonly hypothesized to cause stomatal closure at high D. The importance of these particular hydraulic factors was tested by exposing Abutilon theophrasti, Glycine max, Gossypium hirsutum and Xanthium strumarium to D high enough to reduce g and then decreasing ambient carbon dioxide concentration ([CO2]), and observing the resulting changes in g, transpiration rate and leaf water potential, and their reversibility. Reducing the [CO2] at high D increased g and transpiration rate and lowered leaf water potential. The abnormally high transpiration rates did not result in reductions in hydraulic conductance. Results indicate that low water potential effects on g at high D could be overcome by low [CO2], and that even lower leaf water potentials did not cause a reduction in hydraulic conductance in these well-watered plants. Reduced g at high D in these species resulted primarily from increased stomatal sensitivity to [CO2] at high D, and this increased sensitivity may mediate stomatal responses to leaf hydraulics at high D.