Lawren Sack 1 and N. Michele Holbrook 2. 1 Department of Botany, University of Hawai i at Mānoa, Honolulu, Hawaii 96822;

Transcription

1 Annu. Rev. Plant Biol : The Annual Review of Plant Biology is online at plant.annualreviews.org doi: / annurev.arplant Copyright c 2006 by Annual Reviews. All rights reserved First published online as a Review in Advance on January 30, /06/ $20.00 Leaf Hydraulics Lawren Sack 1 and N. Michele Holbrook 2 1 Department of Botany, University of Hawai i at Mānoa, Honolulu, Hawaii 96822; LSack@hawaii.edu 2 Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts Key Words aquaporins, cavitation, embolism, stomata, xylem Abstract Leaves are extraordinarily variable in form, longevity, venation architecture, and capacity for photosynthetic gas exchange. Much of this diversity is linked with water transport capacity. The pathways through the constitute a substantial ( 30%) part of the resistance to water flow through plants, and thus influence rates of transpiration and photosynthesis. Leaf hydraulic conductance (K ) varies more than 65-fold across species, reflecting differences in the anatomy of the petiole and the venation architecture, as well as pathways beyond the xylem through living tissues to sites of evaporation. K is highly dynamic over a range of time scales, showing circadian and developmental trajectories, and responds rapidly, often reversibly, to changes in temperature, irradiance, and water supply. This review addresses how structure and physiology influence K, and the mechanisms by which K contributes to dynamic functional responses at the level of both individual leaves and the whole plant. 361

2 Contents Annu. Rev. Plant. Biol : Downloaded from arjournals.annualreviews.org K : hydraulic conductance (units mmol m 2 s 1 MPa 1 ) INTRODUCTION LEAF HYDRAULIC CONDUCTANCE Relation to Whole-Plant Hydraulic Conductance Maximum Leaf Hydraulic Conductance Across Species and Life Forms PATHWAYS OF WATER MOVEMENT IN THE LEAF Water Movement Through Leaf Xylem: Petiole and Venation Water Movement Outside the Xylem: Bundle Sheath and Mesophyll Partitioning the Leaf Hydraulic Resistance COORDINATION OF MAXIMUM LEAF HYDRAULIC CONDUCTANCE WITH LEAF STRUCTURE AND FUNCTION Coordination with Gas Exchange. 367 INTRODUCTION The role of the hydraulic system in constraining plant function has long been recognized (15, 37, 135), but until recently the hydraulic properties of leaves had received little sustained attention. This is somewhat surprising given that the constitutes an important hydraulic bottleneck. Research in previous decades focused on the question of the major pathways for water movement across leaves (14, 38). Current research on hydraulics continues to elucidate these pathways, as well as seeks to understand the influence of the water transport pathways on gas exchange rates, the coordination of hydraulic design with structural diversity, and the dynamics of hydraulic conductance, diurnally, over the lifetime, and in response to multiple environmental factors (Figure 1). Coordination with Leaf Flux-Related Structural Traits. 368 Independence of Maximum K and Traits Related to Leaf Mass Per Area, or to Leaf Drought Tolerance DYNAMICS OF LEAF HYDRAULICS OVER SHORT AND LONG TIME SCALES Responses of Leaf Hydraulic Conductance to Dehydration and Damage Responses of Leaf Hydraulic Conductance to Changes in Temperature and Irradiance Diurnal Rhythms in Leaf Hydraulic Conductance Trajectories of Leaf Hydraulic Conductance During Development and Leaf Aging Plasticity of Leaf Hydraulic Conductance Across Growing Conditions LEAF HYDRAULIC CONDUCTANCE K is a measure of how efficiently water is transported through the, determined as the ratio of water flow rate (F ) through the (through the petiole and veins, and across the living tissues in the to the sites where water evaporates into the airspaces) to the driving force for flow, the water potential difference across the ( ). K is typically normalized by area (i.e., F / is further divided by lamina area; units of mmol water m 2 s 1 MPa 1 ). Hydraulic conductance is the inverse of resistance, R. K is the more commonly used metric. However, because resistances are additive in series, R is used in discussion of the as a component of whole-plant resistance, or when partitioning the resistances within the. 362 Sack Holbrook

3 Why does K have such a strong influence on water movement through the whole plant? The resistance of open stomata to vapor diffusion out of the is typically hundreds of times greater than the hydraulic resistance to bulk flow of the liquid moving through the plant (37). Transpiration rates are thus dictated by this diffusion process, which in turn depends on the stomatal and boundarylayer conductances and the difference in vapor pressure between the intercellular air spaces of the and the atmosphere (Figure 1). However, the maintenance of open stomata depends on having a well-hydrated interior, i.e., a high water potential ( ). From the Ohm s law analogy for the soilplant-atmosphere continuum (52, 135), = soil ρgh E/K plant, 1. where E, soil, ρ, g, h, and K plant represent, respectively, transpiration rate, soil water potential, the density of water, acceleration due to gravity, plant height, and the whole-plant hydraulic conductance. Thus, at a given soil water supply, declines with higher E, with a sensitivity that depends on K plant. For a to sustain at a level high enough to maintain stomata open (i.e., for the to maintain a high E, or a high g s ), K plant must be sufficiently high. Consequently, K plant strongly constrains plant gas exchange. As shown in the following, K is a major determinant of K plant. Relation to Whole-Plant Hydraulic Conductance Leaves contribute a majority of the hydraulic resistance to water flow in shoots, and form a substantial part of the hydraulic resistance in whole plants (80, 132, 146). For 34 species of a range of life forms, the, including petiole, contributed on average 30% of R plant (R plant = 1/K plant ) (99). However, there are cases in which the is reported to contribute up to 80% to 98% of R plant (23, 80). Notably, the contribution of R will vary with time of day; early in the day, when there is net water movement from stem storage (48, Figure 1 Irradiance Water storage VPD E g b g s K K stem K root K soil Ψ Ψ soil Temperature Ψ stem xylem K plant Leaf hydraulic conductance (K ) as a component in a simplified electronic circuit analog of the whole-plant system (modified after 52). K soil, K root, K stem, and K plant represent, respectively, the hydraulic conductance (inverse of resistance) of soil, root, stem, and plant; soil, stem xylem, and represent the water potentials of soil, stem xylem, and ; g s, g b, E, and VPD represent the stomatal and boundary-layer conductances, transpiration rate, and to air vapor pressure difference. This schema is much simplified, as will vary across a crown because of height differences as well as differences in transpiration and hydraulic supply to different leaves (88, 130). Impacts of microclimate on g s and K are shown with red arrows; thus, K, like g s and g b, is represented as a variable conductance; decreases in, an internal variable, drive declines in K via its linkage with increasing xylem tensions. 123), leaves are likely to constitute a higher proportion of resistance than when water is obtained directly from the soil (Figure 1). Additionally, R changes with temperature, water supply, and irradiance, and as leaves age Leaf Hydraulics 363

4 E: transpiration rate (units mmol m 2 s 1 ) Ψ soil : soil water potential (units MPa) Ψ : water potential (units MPa) K plant : whole-plant hydraulic conductance (units mmol m 2 s 1 MPa 1 ) K max : maximum hydraulic conductance (i.e., for hydrated ; units mmol m 2 s 1 MPa 1 ) (see section on Dynamics of Leaf Hydraulics Over Short and Long Time Scales), and can thus increase as a proportion of R plant to become the dominant factor in defining wholeplant water transport capacity. Maximum Leaf Hydraulic Conductance Across Species and Life Forms Measurements of hydraulic conductance for hydrated leaves (K max ), made with several methods (103), indicate a dramatic variability across the 107 species so far examined (Figure 2). K max ranges 65-fold from the lowest value (for the fern Adiantum lunulatum; 0.76 mmol m 2 s 1 MPa 1 ) to the highest (for the tropical tree Macaranga triloba; 49 mmol m 2 s 1 MPa 1 ). K max is highly variable within a life form, varying by tenfold among coexisting tree species (104), and on average tends to be lowest for conifers and pteridophytes, higher for temperate and tropical woody angiosperms, and highest for crop plants (Figure 2). The model species Arabidopsis thaliana and Nicotiana tabacum have moderate Crop herbs Tropical woody angiosperms Temperate woody angiosperms Conifers Pteridophytes All species average Leaf hydraulic conductance (mmol m -2 s -1 MPa -1 ) Figure 2 Leaf hydraulic conductance averaged for contrasting life forms (for hydrated whole leaves, including petiole, and when possible for fully illuminated sun leaves; data pooled across plant age and habitat; pteridophytes, 4 species, 19, 24; conifers, 6 species, 7, 24, 133; temperate woody angiosperms, 38 species; 1, 24, 34, 47, 63, 64, 81, 83, 92, 99, 102, 106, , 146; tropical woody angiosperms, 49 species, 7, 16 20, 24, 41, 104, 118, 131, 133; crop herbs, 7 species, 65, 82, 115, 117, ; all species average for 107 species also includes 2 grass species, 19, 66; and Arabidopsis, 68) Error bars = 1 SE. values of 12 and 26 mmol m 2 s 1 MPa 1, respectively (68, 115). Interspecific variation in K max reflects differences in the anatomy of the petiole and venation, as well as pathways beyond the xylem through living tissues to sites of evaporation. PATHWAYS OF WATER MOVEMENT IN THE LEAF Water Movement Through Leaf Xylem: Petiole and Venation On entering the petiole of a dicotyledonous, the vascular bundles in the traces reorganize, differentially supplying midrib bundles, which branch into the second- and third-order veins (42, 58). Water exits the major veins into the surrounding tissue, or into the minor veins, the tracheid-containing fine veins embedded in the mesophyll (5, 27). In dicotyledons the minor veins account for the preponderance of the total vein length (e.g., 86% 97% in temperate and tropical trees) (91, 100). Thus, the bulk of transpired water will be drawn out of minor veins, resulting in the major and minor veins acting approximately in series (99, 146). Leaf vein systems are enormously variable in many aspects: in vein arrangement and density; and in the number, size, and geometry of the vascular bundles in the veins; and of the xylem conduits within the bundles (97). These structural characteristics play a critical role in how water is distributed across the, and thus an increasing number of studies focus on the relationship of K max to venation architecture. K max correlates with the dimensions of conduits in the midrib (1, 3, 79, 100), and for ten species of tropical trees, correlated strongly with the midrib conductivity calculated from the Poiseuille equation for the xylem conduits (100). This correlation does not imply that the midrib is a substantial constraint on the conductance of the venation, or on K max, but rather implies a scaling of hydraulic resistances throughout the (see below) (100). Higher minor vein density in 364 Sack Holbrook

5 general corresponds to a higher supply capacity (or K max ), not by increasing the conductance through the vein xylem system per se (34), but rather primarily by increasing the surface area for exchange of xylem water with surrounding mesophyll, and reducing the distance through which water travels outside the xylem (97, 100). By contrast, the arrangement and density of major veins is not related to K max (100). However, major vein arrangement plays an essential role in distributing water equitably across the lamina (97, 150), and redundancy of major veins could buffer the impacts of damage and/or cavitation (discussed below). Water Movement Outside the Xylem: Bundle Sheath and Mesophyll Water movement pathways outside the xylem are complex and potentially vary strongly across species that diverge in mesophyll anatomy. Important progress has been made on this critical topic, although a full understanding will likely require new approaches. Once water leaves the xylem, it enters the bundle sheath, made up of parenchymatous cells wrapped around the veins (42). A number of early studies concluded that water exits the xylem through cell walls, moving around the bundle sheath protoplasts, because membranes were thought to be too resistive to occur in the transpirational pathways (e.g., 12, 13). However, the presence of aquaporins and the high surface area for water transport across the membranes of bundle sheath cells means that intercellular water movement is, in fact, plausible (53, 68, 102, 112). Indeed, in some species, water seems constrained to enter bundle sheath cells by suberized perpendicular walls, a barrier analogous to the root Casparian strip (60, 136). Dye experiments suggest movement into the bundle sheath cells; in leaves transpiring a solution of apoplastic dye, crystals form in the minor veins (27). Other evidence comes from the temperature response of measured K (69, 102) and the recently demonstrated role of aquaporins (82, but see 68), both consistent with crossing membranes (see below). The bundle sheath cells may be a control center in water transport, the locus for the striking temperature and light responses of K. What happens to water once it passes out of the xylem into the bundle sheath and beyond? Although this is clearly a question of great importance, current evidence remains indirect. A large portion of the mesophyll volume is airspace, with limited cell-to-cell contact, but spongy mesophyll cells are in contact to a far greater degree than palisade cells, and thus would seem better suited to conduct water (142, 143). The epidermis has substantial cell-to-cell contact, and water could move directly there from the minor veins, in species with bundle sheath extensions tightly packed, chloroplast-free cells that connect the bundle sheath that surrounds the minor veins to the epidermides in many species (70, 145). In those species, the epidermis can remain hydrated despite having little vertical contact with the photosynthetic mesophyll (59, 138). In species lacking bundle sheath extensions, water must move across the mesophyll. Whether water moves principally apoplastically (i.e., in the cell walls), transcellularly (i.e., crossing membranes), or symplastically (i.e., cell-to-cell via plasmodesmata) is not yet known, and probably differs among species and conditions. The first experimental studies on sunflower suggested that apoplastic movement dominates during transpiration, and that water crosses mesophyll membranes only during rehydration or growth (13, 139). However, other experiments showed that movement through symplastic routes was plausible (129, 134); the cell pressure probe has indicated significant symplastic water transport among mesophyll cells in succulent Kalanchoë leaves (77). Finally, there is the question of where in the water evaporates, important because the resistances in the pathways to those sites will determine overall R. Mathematical and physical models predict that evaporation inside the will occur principally Leaf Hydraulics 365

6 near the stomata from surrounding epidermal cells, and/or from the mesophyll directly above the stomata, and/or from the guard cells themselves (71, 134). However, such models do not account for the fact that in at least several species, the cuticle extends into the substomatal cavity, potentially reducing evaporation (90 and references therein). An alternative scenario is that most water evaporates deep within the mesophyll, close to the veins (13, 14). Circumstantial support for this idea comes from the fact that the measurement of resistance to helium diffusion across an amphistomatous equaled about twice that of water vapor out of the which travels half the distance (43), suggesting that water begins its diffusion deep within the (14). A third scenario is that water evaporates relatively evenly throughout the mesophyll (87). This scenario predicts a vapor diffusion pathway similar to that of CO 2 assimilated during photosynthesis (though opposite in direction). Indeed, the computation of intercellular CO 2 concentration using typical photosynthesis systems relies on this assumption (44), as does the use of the pressure bomb to estimate the driving force for transpiration (103, 146). Where water principally evaporates within the is not clear; the data from modeling, dye studies, biophysics, and gas exchange measurements do not provide a coherent story. A definitive answer is likely to require new approaches, such as the use of in vivo imaging to track changes in cell dimensions within transpiring leaves (e.g., 111). A complete understanding of water flow pathways will illuminate several important aspects of function, including the enrichment of oxygen isotopes (6), and the response of stomata to water status. Guard cells can respond within seconds (93, 95, 98, 114); their movement depends on cell water potential and turgor pressure, which in turn depends on where precisely the bulk of water evaporates in the, and on the hydraulic conductances from the veins to epidermis and guard cells (e.g., 26, 45). Quantifying these parameters should help explain the onset of patchy behavior of stomata at small scales (76). Partitioning the Leaf Hydraulic Resistance How is K determined from these complex pathways of water movement? This question is especially important because the way in which the hydraulic resistance ( = 1/K ) is partitioned between the xylem and across the extraxylem pathways will strongly influence the responsiveness of R to changing conditions. If the resistance of the xylem (R xylem ) is a major component of R, then the enormous variation in venation architecture across species could reflect strong differences in R. That would be very unlikely, however, if R xylem were negligible relative to the extraxylem resistance (R outside xylem ); in that case, even large relative differences in R xylem among species would have little impact on overall R. Additionally, the larger R xylem is, relative to R outside xylem, the greater the effect on R of changes in R xylem due to environment (e.g., drought-induced cavitation; see 72). Thus, substantial discussion surrounds the issue of where the major resistances to water flow occur within leaves (e.g., 34, 47, 82, 102, 104). Some of this controversy resulted from methodological differences, including the failure to take into account the effect of irradiance on R (see below) and the use of treatments to determine R xylem that opened up pathways for water to move out of low-order veins, bypassing conduit endings and higher-order veins that contain higher resistance; using those methods resulted in estimates of R xylem as 27% of R, averaged for the ten species tested (12, 34, 109, 125, , 146). Recent studies conducted under high irradiance, in which only minor veins were severed, found R xylem to be 59% of R, averaged for 14 species (47, 82, 102, 104). The current consensus is that the hydraulic resistance of the s xylem is about the same order as in the extraxylem pathways (47, 79, 366 Sack Holbrook

7 82, 102, 104; but see 34), and that species vary in their partitioning. Indeed, among tropical trees, the % of R in the xylem differed significantly between species (ranging from 26% to 89%); species that establish in high-light environments had 70% of R in the xylem on average, whereas those from low irradiance had 52% (104). Despite this variation, across the range of species values, R xylem, R outside xylem and R were linearly correlated across species (104). The implications of this finding are that differences in venation architecture reflect strong differences in R, and also that R will be sensitive to changes in the conductance of both the xylem and extraxylem pathways. Indeed, the ratio of R xylem to R outside xylem is dynamic. For example, R xylem will increase if vein xylem embolizes during drought, whereas R outside xylem changes according to an endogenous circadian rhythm, and also increases under low irradiance (82, 101, 131); both resistances increase at lower temperatures, with R outside xylem increasing more strongly (69, 102; see below). Because vein systems consist of water movement through a well-defined arrangement of fixed tubes, they should be amenable to quantitative methods used in the study of biological (and other) networks (e.g., 8, 34, 66, 102, 140, 147). In the most anatomically explicit model to date, R xylem is estimated for dicotyledonous leaves by assuming Poiseuille flow through a network parameterized with measured venation densities and conduit numbers and dimensions (34). However, contrary to empirical data, which showed that R xylem constitutes on average over 50% of R (see above), the model suggested from the xylem conduit measurements that R xylem was only 2% of R. Thus, anatomical features not included in the model, for example, the resistance to water movement between xylem conduits, must play an important role (34, 121). Next generation studies will improve our ability to scale up from anatomical measurements to accurate prediction of venation network R xylem. COORDINATION OF MAXIMUM LEAF HYDRAULIC CONDUCTANCE WITH LEAF STRUCTURE AND FUNCTION The coordination of hydraulics with structure and gas exchange is likely to have played a critical role in the early evolution of the laminate. Lower CO 2 levels and cooler temperatures during the Devonian would have allowed large leaves to avoid overheating, but the higher stomatal densities, which evolved to maintain CO 2 assimilation, would have led to more rapid transpiration (89) and thus required concomitant increases in hydraulic capacity (9 11). The coordination among hydraulic supply and demand and form remains a key design element among modern plants. Coordination with Gas Exchange Recent work demonstrates correlations across species between liquid phase (hydraulic) conductances of stems, shoots, or whole plants and vapor phase (stomatal) conductance (g s ) and maximum rates of gas exchange (e.g., 3, 54, 57, 73, 74, 80, 110). Consistent with this matching of hydraulic supply and demand is the strong coordination across species between K max and stomatal pore area per area, maximum g s, and photosynthetic capacity (3, 19, 24, 99, 104). What is the basis for the interspecific coordination of hydraulic properties and gas exchange? The coordination of K plant (and K ) and maximum g s and E would arise from convergence among species in, soil, boundary-layer conductance and to-air vapor pressure difference (see Equation 1 and Figure 1) (104). Given that hydraulic conductances scale through the plant (99), species would converge also in the water potential of the stem xylem proximal to the ( stem xylem ), the water potential drop across the ( = stem xylem ), and that across the whole plant ( plant = soil ; 74). The linkage indicates a standardization of water relations among plants of g s : stomatal conductance to water vapor (units mmol m 2 s 1 ) Leaf Hydraulics 367

8 a given life form and vegetation type during peak transpiration, when soil is moist. There is evidence of strong convergence in water relations parameters, stem xylem,, and soil during peak transpiration for plants of a given system in moist soil during the growing season (23, 24, 55, 80, 123). The typically modest range in these parameters (typically ± <0.5 MPa) occurs despite variation within a vegetation type in plant size and age, rooting depth and vulnerability to cavitation, as well as divergence among species in the season during which they manifest peak activity, which would further destabilize the coordination (104). The convergence in is Table 1 Leaf structural and functional traits, sorted by putative association with maximum water flux per area (and K ), mass per area, or drought tolerance a across species Maximum flux-related traits Leaf hydraulic conductance Stomatal pore area Stomatal conductance Net maximum photosynthesis per area Leaf midrib xylem conduit diameters Mesophyll area/ area Thickness of and palisade mesophyll Leaf chlorophyll concentration per area Leaf nitrogen concentration per area Leaf shape (margin dissection) Leaf water storage capacitance per area Leaf mass per area-related traits Leaf density Leaf thickness Leaf lifespan Leaf chlorophyll concentration per mass (negatively related) Leaf nitrogen concentration per mass (negatively related) Leaf water content per mass (negatively related) Leaf drought tolerance traits Cuticular conductance (negatively related) Modulus of elasticity (variably related) Leaf density (variably related) Leaf water storage capacitance per area Osmotic potentials at full and at zero turgor Resistance to xylem cavitation a Associations are positive except when noted. analogous to the range of household appliances in a given country being designed to run at a given voltage from lamps to ovens with the current through the appliance dependent on the electric conductance, or resistance. The finding of narrowly constrained water relations in a given vegetation type provides a potentially powerful basis for a general relationship between K and maximum rates of gas exchange. In addition, increased understanding of how the coordination of K max and gas exchange shifts across life forms and habitats will allow prediction of performance differences for plants adapted to different zones around the world. One study so far has demonstrated that the coordination between hydraulics and gas exchange varies among vegetation types: Tropical rainforest trees as a group have higher potential gas exchange relative to K than temperate deciduous trees, consistent with their adaptation to higher and soil, and/or lower VPD during peak activity (104). Coordination with Leaf Flux-Related Structural Traits Leaves vary tremendously in area, thickness, shape, nutrient concentrations, and capacity for gas exchange. The intercorrelation of many traits places some bound on this diversity, for instance among those related to carbon economy, including mass per area (LMA; dry mass/area), lifespan (e.g., 96, 141), and nitrogen concentration per mass and net maximum photosynthetic rate per mass (A mass ; 141), and provides a framework for understanding the integrated function of clusters of traits. Similarly, coordination among traits related to water flux through leaves exists for plants of a particular life form and habitat (99) (Table 1). In addition to their higher total maximum stomatal pore area and gas exchange per area (see above; 3, 19, 99), leaves with high K max tend to have wider xylem conduits in the midrib and higher venation densities (3, 102). K max correlated 368 Sack Holbrook

9 with palisade thickness, and palisade/spongy mesophyll ratio for tropical rainforest tree species (100), and with total thickness and water storage capacitance per area for temperate woody species (99). These correlations arose due to structural coordination the sharing of an anatomical or developmental basis and/or due to functional coordination the coselection of characters for benefit in a particular environment (99, 116). Independence of Maximum K and Traits Related to Leaf Mass Per Area, or to Leaf Drought Tolerance Certain traits show a disproportionate number of linkages with other traits (86). LMA is one such hub trait (Table 1). However, K max, a hub trait in its own right (being linked with many water-flux traits), is unrelated to LMA (Table 1) (20, 78, 99, 104, 133). Because this complex of water flux related traits is coordinated with net maximum photosynthesis per area, which is equal to LMA in its driving differences in A mass across species globally (data in 141), and because A mass generally scales up to whole-plant relative growth rate, water flux related traits including K are a potentially fundamental determinant of species performance differences. However, K max is apparently independent of a partially interrelated complex of traits associated with drought tolerance, i.e., the ability to maintain positive turgor and gas exchange at low (Table 1). These traits are evidently coselected by desiccating conditions (85, 107), and include low osmotic potentials at full and at zero turgor, and low cuticular conductance (99, 100). DYNAMICS OF LEAF HYDRAULICS OVER SHORT AND LONG TIME SCALES K is highly dynamic, varying over a wide range of time scales, from minutes to months, and according to microclimate and growing conditions. The dynamics of K are typically closely correlated with those of gas exchange (Equation 1 and Figure 1) (32, 35, 36, 69, 72). As K declines (e.g., owing to dehydration), will similarly decline, and stomata will close as, or before, becomes damaging, leading to reduction of g s and E (32, 108). In droughted plants such a mechanism operates in tandem with chemical signals from the roots to close the stomata (36, 39). Associated declines in intercellular CO 2 concentration (c i ) drive a reduction in photosynthetic rate (46, 69). Declines in can also directly reduce photosynthetic rate metabolically (40). Why is K dynamic, given that its decline drives such loss of function? K reduction during water stress would protect the xylem by driving stomatal closure, thus alleviating the tensions in the transpiration stream. Also, membrane channels important in maintaining a high K require metabolic energy for expression and potentially for activation. Responses of Leaf Hydraulic Conductance to Dehydration and Damage The hydraulic conductance of the petiole (K petiole ) and of the whole declines during drought, correlating in vivo with declines in gas exchange (Figure 3a) (17 19, 25, 30, 32, 33, 49, 50, 62, 63, 81, 83, 105, 108, 109, 117, 124, 125, 149). An important factor contributing to the decline of K at low is xylem cavitation (55, 83, 149). Petioles with lower conductance take up dye into fewer vessels (25, 149), and dehydrated leaves take up dye into fewer minor veins in the network (83, 105, 124, 125). The xylem can become increasingly vulnerable with increasing drying iterations i.e., cavitation fatigue, as shown in petioles of Aesculus hippocastanum (50). However, cavitation is not the only potential source of K decline during dehydration. Dehydrating conifer leaves decline in K owing to collapse of xylem conduits, which precedes cavitation (21, 33). The potential collapse of xylem conduits in dicotyledonous LMA: mass per area ( dry mass/area; units gm 2 ) Leaf Hydraulics 369

10 a Ψ = -1 MPa Ψ = -2 MPa Ψ = -3 MPa Leaf dehydration b c Leaf measured under low vs. high irradiance Older vs. younger Annu. Rev. Plant. Biol : Downloaded from arjournals.annualreviews.org d e 0% 20% 40% 60% 80% 100% Mean reduction of hydraulic conductance in given conditions Shade vs. sun Plants grown in 2% vs. 8% daylight Plants grown in low vs. high water supply Figure 3 Leaf hydraulic conductance is highly dynamic, as shown by the responses depicted here with respect to controls (color as a proportion of white bars). Note that the averaged responses shown are only indicative the responses vary strongly in magnitude according to the particular species and ranges of conditions observed. (a) Response to branch dehydration (13 species; 17, 19, 63, 83, 124, 125); (b) response to incident irradiance, during measurement over minutes to hours (14 species; 34, 47, 82, 101, 131); (c) response related to aging (9 tree species; 16, 18, 20, 64, 106); (d ) response to growth irradiance, including shade vs sun leaves (4 tree species; 99), and leaves of plants grown in 2% versus 8% daylight (2 species, 41); (e) response to water supply during growth (3 species; 1, 41). leaves remains to be investigated, as does the additional possibility of decline in conductance of the extra-xylem paths. A strikingly rapid and complete recovery of K during rehydration has been documented after rewatering droughted plants or rehydrating partially dehydrated leaves (62, 63, 75, 124). Such short-term increases in K result from a diversity of mechanisms. For example, conifers elastically recover their xylem geometry on rewatering (21, 33), whereas rice leaves reverse embolism through root pressure (122). Where root pressure is not operating, an active mechanism may exist for embolism refilling even when xylem tensions exist, involving ion pumping or transient pressures, associated with increasing starch degradation (25, 124, 149). Because the linkage of K and gas exchange is mediated by and species diverge in their responses, the extent to which K and g s remain coordinated during dehydration varies among species. The distance between at stomatal closure ( stomatal closure ) and the at which the xylem is irreversibly embolized is termed the safety margin (19, 119, 120). In species with a wide safety margin, the risk is minimal, as stomata close before K declines substantially (19, 30, 32, 83). However, in other species, with a narrow safety margin, g s declines by half only after K or K petiole decline by 20% or more (17 19, 25, 62, 63, 80, 105, 108, 125). High safety margins protect the xylem, but lower safety margins allow plants to maintain gas exchange closer to the level of irreversible K decline (19, 120). The decline in K would confer safety to the whole-plant hydraulic system by augmenting the decline in, accelerating 370 Sack Holbrook

11 stomatal closure, which would protect portions of the plant that are less easily replaced (18). The protection conferred will vary according to species, because species differ in whether whole leaves, petioles, and midribs are more (17, 22, 28, 49, 84, 105, 108, 125), equally (33), or less (32, 49, 83, 122) vulnerable to loss of conductance compared with the stem as declines (and xylem tensions increase). One of the most commonly investigated patterns in stem hydraulics is a trade-off between hydraulic efficiency (i.e., maximum hydraulic conductance) and resistance to drought-induced cavitation (135). This pattern is not found in leaves: The vulnerability of K to drought is not higher for leaves with high K max. In our analysis of the available data for 13 species of ferns, trees, and herbs varying 42-fold in K max, at 50% loss of conductivity ranged from 1.3 MPa to 3 MPa, and was uncorrelated withk max (r 2 = 0.07; P = 0.4; data of 17, 19, 63, 83, 124, 125). K is also reduced by herbivory and other forms of mechanical vein damage. The interruption of major veins was classically held to have no effect on function, as leaves often survive with a perfectly healthy appearance (29, 91). However, damage that interrupts primary veins in dicotyledonous leaves immediately produces massive declines in K, and in g s and photosynthetic rates, which persist weeks later, after the wounded tissue has scarred over; in some species, the leaves desiccate (4, 51, 81, 98). Whether major vein disruption leads to tissue death or not would depend at least as much on evaporative demand and on the s ability to reduce water loss (i.e., with an impermeable cuticle) as on the s vascular architecture. However, redundancy in the venation such as conduits in parallel within each vein, and multiple veins of each order would buffer K against both cavitation and damage, by providing pathways around damaged or blocked veins (29, 51, 84, 97, 137). Responses of Leaf Hydraulic Conductance to Changes in Temperature and Irradiance K max increases at higher temperatures, as shown in experiments conducted in vivo, determining gas exchange while manipulating temperature and controlling other microclimatic variables (46). This increase is only partially accounted for by the direct effects of temperature on the viscosity of water. Investigation of the temperature response of water flow through shoots and leaves showed an activation energy of kj mol 1, but when minor veins were severed, so that water was forced through only xylem, the activation energy dropped to 17 kj mol 1, which corresponds to changes in the viscosity of water (12, 102, 127, 128). Thus, the viscosity response applies to the xylem pathways, whereas an extraviscosity response applies to the pathways outside the xylem (102), consistent with the flow path crossing membranes (68). The temperature induced changes in K max can allow and g s to remain stable even as E increases due to higher VPD (46, 69). K max responds strongly to irradiance; for many species K is much lower when measured at low irradiance than at high irradiance (i.e., at <10 μmol photons m 2 s 1 versus at >1000 μmol photons m 2 s 1 )(Figure 3b) (82, 101, 131). The responses vary across species, and can range up to a several-fold increase from low to high irradiance. The kinetics of the K max response to irradiance differs sufficiently from that of stomatal aperture to suggest that the light response arises in the hydraulic pathways through the mesophyll (131), and involves activation of aquaporins (53, 82, 131). These same channels apparently follow an endogenous circadian rhythm: In sunflower, K max increases up to 60% from night to day, and the rhythm can be reversed if photoperiod is switched, and the rhythm continues for days even when plants are kept in constant darkness (82). The response can be removed by treatment with HgCl 2, and recovered by using mercaptoethanol, VPD: mole fraction vapor pressure difference between and outside air (units mol mol 1 ) Leaf Hydraulics 371

12 implying the agency of aquaporins (82). In sunflower, dark-acclimated leaves show a strong light response, but light-acclimated leaves do not, suggesting that their water channels are already activated (82). The deactivation of aquaporins in the dark would be adaptive, assuming the maintenance of activity requires energy expenditure. For plants kept in the dark for 1 h, or for 4 6 days, K max and shoot hydraulic conductances (measured under high irradiance) were reduced by 20% 75% on average (2, 117). The response of K max to irradiance implies the existence of a previously unknown level of control of a plant s response to environment; this response would facilitate the increases of stomatal aperture and gas exchange with increasing irradiance by improving water supply to the mesophyll. Diurnal Rhythms in Leaf Hydraulic Conductance K is dynamic diurnally, and its changes reflect simultaneous responses to multiple factors. As discussed above, K follows an endogenous circadian rhythm; K also increases with incident light over the scale of minutes and hours (64, 101, 131). Additionally, K increases with temperature. By contrast, K declines as leaves dehydrate under high midday temperatures and VPD. Thus, contrasting trends have been observed for the diurnal response of K. For sunflower, and for four tree species, K increased by up to two- to threefold over a few hours from morning to midday, as irradiance and temperature increased, and then declined by evening, in a similar pattern as g and E (64, 126). On the other hand, a midday decline in K by 30% to 50% has been observed for tree species as transpiration increased to high rates by midday (18, 83), apparently as a response to dehydration. Similar diurnal declines in conductance were found for tree petioles and for flow axially across rice leaves (25, 122, 149). In other species no diurnal patterns were observed (31, 149). Such variable patterns in diurnal responses of K are likely to reflect the particular combinations of irradiance, and air temperature, soil moisture, and VPD, as well as endogenous rhythms. Thus, one would expect K to increase each morning in response to internal cues, as well as increasing irradiance and temperature; but if E is driven high enough by a high VPD (and/or if soil is dry), low would result in significant declines in K and in g s, recovering by the end of the day. Trajectories of Leaf Hydraulic Conductance During Development and Leaf Aging K is also dynamic over the lifetime of the. K increases in developing leaves as the vasculature matures (1, 20, 67). Weeks or months after K reaches its maximum, it begins to decline, with reductions of up to 80 90% at abscission (Figure 3c) (1, 16, 18, 64, 100, 106). One factor contributing to this decline of K is the accumulation of emboli in the vein xylem, and eventual blockage by tyloses (106, 135). K would decline also owing to reduction of the permeability of cell walls or membranes (see 136). Decreases in K would cause progressive dehydration, potentially contributing to the observed decline in midday as leaves age (16, 65, 106). Reductions in K are coordinated with age-related declines in other functional traits, including nitrogen concentration, stomatal sensitivity to VPD, osmotic potential, and gas exchange (e.g., 56, 94). Some have hypothesized that the seasonal decline of K is a trigger for senescence (16, 106). Plasticity of Leaf Hydraulic Conductance Across Growing Conditions Although most studies of hydraulics have been performed on plants in high-resource conditions, K max is highly plastic across growing conditions, owing to developmental 372 Sack Holbrook

13 changes in vein density, conduit sizes or numbers (e.g., 3), and/or in the structure and conductivity of extraxylem pathways. Leaves expanded in shade or in crown positions liable to shade have low K max relative to sun leaves (Figure 3d) (99, 113), part of the complex of shade characters including lower vein densities, smaller stomata, thinner leaves, less dissected shape, and lower rates of gas exchange (e.g., 61, 144, 148). In mature sunflower plants, K max was linearly related to irradiance from basal to apical leaves (65); in this case an irradiance effect combines with an age effect. K max is also plastic across plant growing conditions. K max and shoot hydraulic conductance were lower for plants grown several months in lower irradiance (Figure 3d) (41), or in lower water or nitrogen supplies (Figure 3e) (1 3, 41). Such plasticity in K max runs in parallel with adaptive differences, as sun-adapted species tend to have several-fold higher K max than shade-adapted species on average, for temperate and tropical species sets (79, 104). These findings suggest that K max plays a potentially important role in determining plant resource responses and also in determining ecological preferences among species. SUMMARY POINTS 1. K max varies at least 65-fold across species, and scales with K plant ; the is a substantial resistance in the plant pathway, 30% and upward of whole-plant resistance. 2. The partitioning of resistances within the among petiole, major veins, minor veins, and pathways outside the xylem is variable across species. Substantial hydraulic resistances occur both in the xylem as well as in the flow paths across the mesophyll to evaporation sites. These components respond differently to ambient conditions, including irradiance and temperature, indicating an involvement of aquaporins. 3. K max is coordinated with maximum gas exchange rates for species of a particular life form and habitat. This coordination arises from convergence in water relations parameters, especially at peak transpiration. K max is also coordinated with a framework of other traits related to water flux, including stomatal pore area, midrib xylem conduit diameters, and palisade richness. However, K max is independent of the complex of traits linked with mass per area, and traits relating to drought tolerance. 4. K is highly dynamic varying diurnally, as leaves age, and in response to changes in hydration, irradiance, temperature, and nutrient supply. The decline in K in response to lower arises from reductions in xylem conductivity due to cavitation or collapse, and/or from changes in the conductivity of the pathways outside the xylem. Some short-term declines in K can be rapidly reversed. Dynamic changes in K impact gas exchange via stomatal regulation of and could play a role in senescence. FUTURE ISSUES 1. Still needed is a fully quantitative understanding of how K max is determined by the venation architecture and the extraxylem pathways, including the identity and behavior of aquaporins in these pathways. Leaf Hydraulics 373

14 2. The precise correlations that link K with gas exchange and structure among species of particular life forms and habitats need to be determined, as well as the shifts of this coordination across life forms and habitats. The patterns of general coordination will enable predictions of water relations behavior for whole sets of species from simply measured hydraulic parameters. 3. The mechanisms for the diurnal and developmental dynamics of K, and for the reversible K responses to irradiance and to dehydration need to be elucidated in detail. Understanding the mechanisms behind these changes will enhance the ability to model the influence of these dynamics on gas exchange over short and long time scales. Annu. Rev. Plant. Biol : Downloaded from arjournals.annualreviews.org ACKNOWLEDGMENTS We thank Kristen Frole for valuable assistance with the data compilation. LITERATURE CITED 1. Aasamaa K, Niinemets Ü, Sober A Leaf hydraulic conductance in relation to anatomical and functional traits during Populus tremula ontogeny. Tree Physiol. 25: Aasamaa K, Sober A Hydraulic conductance and stomatal sensitivity to changes of water status in six deciduous tree species. Biol. Plant. 44: Aasamaa K, Sober A, Rahi M Leaf anatomical characteristics associated with shoot hydraulic conductance, stomatal conductance and stomatal sensitivity to changes of water status in temperate deciduous trees. Aust. J. Plant Physiol. 28: Aldea M, Hamilton JG, Resti JP, Zangerl AR, Berenbaum MR, DeLucia EH Indirect effects of insect herbivory on gas exchange in soybean. Plant Cell Environ. 28: Altus DP, Canny MJ, Blackman DR Water pathways in wheat leaves. 2. Waterconducting capacities and vessel diameters of different vein types, and the behavior of the integrated vein network. Aust. J. Plant Physiol. 12: Barbour MM, Farquhar GD Do pathways of water movement and anatomical dimensions allow development of gradients in H 18 2 O between veins and the sites of evaporation within leaves? Plant Cell Environ. 27: Becker P, Tyree MT, Tsuda M Hydraulic conductances of angiosperms versus conifers: similar transport sufficiency at the whole-plant level. Tree Physiol. 19: Bohn S, Andreotti B, Douady S, Munzinger J, Couder Y Constitutive property of the local organization of venation networks. Phys. Rev. E Boyce CK Patterns of segregation and convergence in the evolution of fern and seed plant morphologies. Paleobiology 31: Boyce CK The evolutionary history of roots and leaves. In Vascular Transport in Plants, ed. NM Holbrook and MA Zwieniecki, pp Oxford: Elsevier/Academic 11. Boyce CK, Knoll AH Evolution of developmental potential and the multiple independent origins of leaves in Paleozoic vascular plants. Paleobiology 28: Boyer JS Water transport in plants: mechanism of apparent changes in resistance during absorption. Planta 117: Sack Holbrook

15 13. Boyer JS Regulation of water movement in whole plants. Symp. Soc. Exp. Biol. 31: Boyer JS Water transport. Annu. Rev. Plant Physiol. 36: Boyer JS, Silk WK Hydraulics of plant growth. Funct. Plant Biol. 31: Brodribb TJ, Holbrook NM Changes in hydraulic conductance during shedding in seasonally dry tropical forest. New Phytol. 158: Brodribb TJ, Holbrook NM Stomatal closure during dehydration, correlation with other physiological traits. Plant Physiol. 132: Brodribb TJ, Holbrook NM Diurnal depression of hydraulic conductance in a tropical tree species. Plant Cell Environ. 27: Brodribb TJ, Holbrook NM Stomatal protection against hydraulic failure: a comparison of coexisting ferns and angiosperms. New Phytol. 162: Brodribb TJ, Holbrook NM Leaf physiology does not predict habit; examples from tropical dry forest. Trees Struct. Funct. 19: Brodribb TJ, Holbrook NM Water stress deforms tracheids peripheral to the vein of a tropical conifer. Plant Physiol. 137: Brodribb TJ, Holbrook NM, Edwards EJ, Gutierrez MV Relations between stomatal closure, turgor and xylem vulnerability in eight tropical dry forest trees. Plant Cell Environ. 26: Brodribb TJ, Holbrook NM, Gutierrez MV Hydraulic and photosynthetic coordination in seasonally dry tropical forest trees. Plant Cell Environ. 25: Brodribb TJ, Holbrook NM, Zwieniecki MA, Palma B Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima. New Phytol. 165: Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Sternberg LDL Dynamic changes in hydraulic conductivity in petioles of two savanna tree species: factors and mechanisms contributing to the refilling of embolized vessels. Plant Cell Environ. 26: Buckley TN, Mott KA, Farquhar GD A hydromechanical and biochemical model of stomatal conductance. Plant Cell Environ. 26: Canny MJ What becomes of the transpiration stream? New Phytol. 114: Choat B, Lahr EC, Melcher PJ, Zweiniecki MA, Holbrook NM The spatial pattern of air seeding thresholds in mature sugar maple trees. Plant Cell Environ. 28(9): Cholewa E, Vonhof MJ, Bouchard S, Peterson CA, Fenton B The pathways of water movement in leaves modified into tents by bats. Biol. J. Linn. Soc. 72: Cochard H Xylem embolism and drought-induced stomatal closure in maize. Planta 215: Cochard H, Bodet C, Ameglio T, Cruiziat P Cryo-scanning electron microscopy observations of vessel content during transpiration in walnut petioles. Facts or artifacts? Plant Physiol. 124: Cochard H, Coll L, Le Roux X, Ameglio T Unraveling the effects of plant hydraulics on stomatal closure during water stress in walnut. Plant Physiol. 128: Cochard H, Froux F, Mayr FFS, Coutand C Xylem wall collapse in water-stressed pine needles. Plant Physiol. 134: Cochard H, Nardini A, Coll L Hydraulic architecture of blades: Where is the main resistance? Plant Cell Environ. 27: Comstock J, Mencuccini M Control of stomatal conductance by water potential in Hymenoclea salsola (T & G), a desert subshrub. Plant Cell Environ. 21: Comstock JP Hydraulic and chemical signalling in the control of stomatal conductance and transpiration. J. Exp. Bot. 53: Leaf Hydraulics 375

16 37. Cowan IR Electrical analog of evaporation from, and flow of water in plants. Planta 106: Davies WJ Transpiration and the water balance of plants. In Plant Physiology, ed. FC Steward, pp Orlando, FL: Academic 39. Davies WJ, Wilkinson S, Loveys B Stomatal control by chemical signalling and the exploitation of this mechanism to increase water use efficiency in agriculture. New Phytol. 153: Ehleringer JR, Cook CS Photosynthesis in Encelia farinosa Gray in response to decreasing water potential. Plant Physiol. 75: Engelbrecht BMJ, Velez V, Tyree MT Hydraulic conductance of two co-occuring neotropical understory shrubs with different habitat preferences. Ann. For. Sci. 57: Esau K Plant Anatomy. New York: Wiley. 2nd ed. 43. Farquhar GD, Raschke K Resistance to transpiration of sites of evaporation within the. Plant Physiol. 61: Field CB, Ball JT, Berry JA Photosynthesis: principles and field techniques. In Plant Physiological Ecology: Field Methods and Instrumentation, ed. RW Pearcy, JR Ehleringer, HA Mooney, PW Rundel, pp Dordrecht: Kluwer 45. Franks PJ, Brodribb T Stomatal control and water transport in the xylem. In Vascular Transport in Plants, ed. NM Holbrook and MA Zwieniecki, pp Oxford: Elsevier/Academic 46. Fredeen AL, Sage RF Temperature and humidity effects on branchlet gas-exchange in white spruce: an explanation for the increase in transpiration with branchlet temperature. Trees Struct. Funct. 14: Gascó A, Nardini A, Salleo S Resistance to water flow through leaves of Coffea arabica is dominated by extravascular tissues. Funct. Plant Biol. 31: Goldstein G, Andrade JL, Meinzer FC, Holbrook NM, Cavelier J, et al Stem water storage and diurnal patterns of water use in tropical forest canopy trees. Plant Cell Environ. 21: Hacke U, Sauter JJ Drought-induced xylem dysfunction in petioles, branches, and roots of Populus balsamifera L. and Alnus glutinosa (L.) Gaertn. Plant Physiol. 111: Hacke UG, Stiller V, Sperry JS, Pittermann J, McCulloh KA Cavitation fatigue. Embolism and refilling cycles can weaken the cavitation resistance of xylem. Plant Physiol. 125: a. Holbrook NM, Zwieniecki MA, eds Vascular Transport in Plants. Oxford: Elsevier/Academic. 564 pp. 51. Hüve K, Remus R, Lüttschwager D, Merbach W Water transport in impaired vein systems. Plant Biol. 4: Jones HG Plants and Microclimate. Cambridge: Cambridge Univ. Press. 428 pp. 2nd ed. 53. Kaldenhoff R, Eckert M Features and function of plant aquaporins. J. Photochem. Photobiol. B: Biol. 52: Katul G, Leuning R, Oren R Relationship between plant hydraulic and biochemical properties derived from a steady-state coupled water and carbon transport model. Plant Cell Environ. 26: Kikuta SB, LoGullo MA, Nardini A, Richter H, Salleo S Ultrasound acoustic emissions from dehydrating leaves of deciduous and evergreen trees. Plant Cell Environ. 20: Kitajima K, Mulkey SS, Samaniego M, Wright SJ Decline of photosynthetic capacity with age and position in two tropical pioneer tree species. Am. J. Bot. 89: Sack Holbrook

17 57. Kuppers M Carbon relations and competition between woody species in a central European hedgerow. 2. Stomatal responses, water-use, and hydraulic conductivity in the root- pathway. Oecologia 64: Larson PR The role of subsidiary trace bundles in stem and development of the Dicotyledoneae. In Contemporary Problems in Plant Anatomy, ed. RA White, WC Dickison, pp London: Academic 59. LaRue CD The water supply of the epidermis of leaves. Mich. Acad. Sci. Arts Lett. 12: Lersten NR Occurrence of endodermis with a casparian strip in stem and. Bot. Rev. 63: Lichtenthaler HK Differences in morphology and chemical composition of leaves grown at different light intensities and qualities. In Control of Leaf Growth, ed. NR Baker, WJ Davies, CK Ong, pp Cambridge: Cambridge Univ. Press 62. Linton MJ, Nobel PS Hydraulic conductivity, xylem cavitation, and water potential for succulent leaves of Agave deserti and Agave tequilana. Int. J. Plant Sci. 162: Lo Gullo MA, Nardini A, Trifilo P, Salleo S Changes in hydraulics and stomatal conductance following drought stress and irrigation in Ceratonia siliqua (carob tree). Physiol. Plant. 117: Lo Gullo MA, Nardini A, Trifilo P, Salleo S Diurnal and seasonal variations in hydraulic conductance in evergreen and deciduous trees. Tree Physiol. 25: Lo Gullo MA, Noval LC, Salleo S, Nardini A Hydraulic architecture of plants of Helianthus annuus L. cv. Margot: evidence for plant segmentation in herbs. J. Exp. Bot. 55: Martre P, Cochard H, Durand JL Hydraulic architecture and water flow in growing grass tillers (Festuca arundinacea Schreb.). Plant Cell Environ. 24: Martre P, Durand JL, Cochard H Changes in axial hydraulic conductivity along elongating blades in relation to xylem maturation in tall fescue. New Phytol. 146: Martre P, Morillon R, Barrieu F, North GB, Nobel PS, Chrispeels MJ Plasma membrane aquaporins play a significant role during recovery from water deficit. Plant Physiol. 130: Matzner S, Comstock J The temperature dependence of shoot hydraulic resistance: implications for stomatal behaviour and hydraulic limitation. Plant Cell Environ. 24: McClendon JH Photographic survey of the occurrence of bundle sheath extensions in deciduous dicots. Plant Physiol. 99: Meidner H Water vapor loss from a physical model of a substomatal cavity. J. Exp. Bot. 27: Meinzer FC Co-ordination of vapour and liquid phase water transport properties in plants. Plant Cell Environ. 25: Meinzer FC, Grantz DA Stomatal and hydraulic conductance in growing sugarcane: stomatal adjustment to water transport capacity. Plant Cell Environ. 13: Mencuccini M The ecological significance of long-distance water transport: shortterm regulation, long-term acclimation and the hydraulic costs of stature across plant life forms. Plant Cell Environ. 26: Milburn JA Cavitation in Ricinus by acoustic detection: induction in excised leaves by various factors. Planta 110: Mott KA, Buckley TN Stomatal heterogeneity. J. Exp. Bot. 49: Leaf Hydraulics 377

18 77. Murphy R, Smith JAC Determination of cell water-relation parameters using the pressure probe: extended theory and practice of the pressure-clamp technique. Plant Cell Environ. 21: Nardini A Are sclerophylls and malacophylls hydraulically different? Biol. Plant. 44: Nardini A, Gortan E, Salleo S Hydraulic efficiency of the venation system in sun- and shade-adapted species. Funct. Plant Biol. 32: Nardini A, Salleo S Limitation of stomatal conductance by hydraulic traits: sensing or preventing xylem cavitation? Trees Struct. Funct. 15: Nardini A, Salleo S Effects of the experimental blockage of the major veins on hydraulics and gas exchange of Prunus laurocerasus L. leaves. J. Exp. Bot. 54: Nardini A, Salleo S, Andri S Circadian regulation of hydraulic conductance in sunflower (Helianthus annuus L. cv Margot). Plant Cell Environ. 6: Nardini A, Salleo S, Raimondo F Changes in hydraulic conductance correlate with vein embolism in Cercis siliquastrum L. Trees Struct. Funct. 17: Nardini A, Tyree MT, Salleo S Xylem cavitation in the of Prunus laurocerasus and its impact on hydraulics. Plant Physiol. 125: Niinemets Ü Global-scale climatic controls of dry mass per area, density, and thickness in trees and shrubs. Ecology 82: Niinemets Ü, Sack L Structural Determinants of Leaf Light Harvesting Capacity and Photosynthetic Potentials. Berlin: Springer Verlag. Progr. Bot. 67. p Nonami H, Schulze ED Cell water potential, osmotic potential, and turgor in the epidermis and mesophyll of transpiring leaves: combined measurements with the cell pressure probe and nanoliter osmometer. Planta 177: Orians CM, Smith SDP, Sack L How are leaves plumbed inside a branch? Differences in -to- hydraulic sectoriality among six temperate deciduous tree species. J. Exp. Bot. 56: Osborne CP, Beerling DJ, Lomax BH, Chaloner WG Biophysical constraints on the origin of leaves inferred from the fossil record. Proc. Natl. Acad. Sci. USA 101: Pesacreta TC, Hasenstein KH The internal cuticle of Cirsium horridulum (Asteraceae) leaves. Am. J. Bot. 86: Plymale EL, Wylie RB The major veins of mesomorphic leaves. Am. J. Bot. 31: Raimondo F, Ghirardelli LA, Nardini A, Salleo S Impact of the miner Cameraria ohridella on photosynthesis, water relations and hydraulics of Aesculus hippocastanum leaves. Trees Struct. Funct. 17: Raschke K Leaf hydraulic system: rapid epidermal and stomatal responses to changes in water supply. Science 167: Reich PB Loss of stomatal function in aging hybrid poplar leaves. Ann. Bot. 53: Reich PB Oscillations in stomatal conductance of hybrid poplar leaves in the light and dark. Physiol. Plant. 61: Reich PB, Walters MB, Ellsworth DS From tropics to tundra: global convergence in plant functioning. Proc. Natl. Acad. Sci. USA 94: Roth-Nebelsick A, Uhl D, Mosbrugger V, Kerp H Evolution and function of venation architecture: a review. Ann. Bot. 87: Sack Holbrook

19 98. Sack L, Cowan PD, Holbrook NM The major veins of mesomorphic leaves revisited: tests for conductive overload in Acer saccharum (Aceraceae) and Quercus rubra (Fagaceae). Am. J. Bot. 90: Sack L, Cowan PD, Jaikumar N, Holbrook NM The hydrology of leaves: coordination of structure and function in temperate woody species. Plant Cell Environ. 26: Sack L, Frole K Leaf structural diversity is related to hydraulic capacity in tropical rainforest trees. Ecology 87: Sack L, Melcher PJ, Zwieniecki MA, Holbrook NM The hydraulic conductance of the angiosperm lamina: a comparison of three measurement methods. J. Exp. Bot. 53: Sack L, Streeter CM, Holbrook NM Hydraulic analysis of water flow through leaves of sugar maple and red oak. Plant Physiol. 134: Sack L, Tyree MT Leaf hydraulics and its implications in plant structure and function. In Vascular Transport in Plants, ed. NM Holbrook and MA Zwieniecki, pp Oxford: Elsevier/Academic Press 104. Sack L, Tyree MT, Holbrook NM Leaf hydraulic architecture correlates with regeneration irradiance in tropical rainforest trees. New Phytol. 167: Salleo S, Lo Gullo MA, Raimondo F, Nardini A Vulnerability to cavitation of minor veins: any impact on gas exchange? Plant Cell Environ. 24: Salleo S, Nardini A, Lo Gullo MA, Ghirardelli LA Changes in stem and hydraulics preceding shedding in Castanea sativa L. Biol. Plant. 45: Salleo S, Nardini A, LoGullo MA Is sclerophylly of Mediterranean evergreens an adaptation to drought? New Phytol. 135: Salleo S, Nardini A, Pitt F, Lo Gullo MA Xylem cavitation and hydraulic control of stomatal conductance in laurel (Laurus nobilis L.). Plant Cell Environ. 23: Salleo S, Raimondo F, Trifilo P, Nardini A Axial-to-radial water permeability of major veins: a possible determinant of the impact of vein embolism on hydraulics? Plant Cell Environ. 26: Santiago LS, Goldstein G, Meinzer FC, Fisher JB, Machado K, et al Leaf photosynthetic traits scale with hydraulic conductivity and wood density in Panamanian forest canopy trees. Oecologia 140: Sapozhnikova VV, Kamensky VA, Kuranov RV, Kutis I, Snopova LD, Myakov AV In vivo visualization of Tradescantia tissue and monitoring the physiological and morphological states under different water supply conditions using optical coherence tomography. Planta 219: Schaffner AR Aquaporin function, structure, and expression: are there more surprises to surface in water relations? Planta 204: Schultz HR, Matthews MA Xylem development and hydraulic conductance in sun and shade shoots of grapevine (Vitis vinifera L.): evidence that low light uncouples water transport capacity from area. Planta 190: Sheriff DW, Meidner H Water pathways in leaves of Hedera helix L. and Tradescantia virginiana L. J. Exp. Bot. 25: Siefritz F, Tyree MT, Lovisolo C, Schubert A, Kaldenhoff R PIP1 plasma membrane aquaporins in tobacco: from cellular effects to function in plants. Plant Cell 14: Sisó S, Camarero JJ, Gil-Pelegrín E Relationship between hydraulic resistance and morphology in broad Quercus species: a new interpretation of lobation. Trees Struct. Funct. 15: Leaf Hydraulics 379

20 117. Sober A Hydraulic conductance, stomatal conductance, and maximal photosynthetic rate in bean leaves. Photosynthetica 34: Sobrado MA Hydraulic conductance and water potential differences inside leaves of tropical evergreen and deciduous species. Biol. Plant. 40: Sperry JS Coordinating stomatal and xylem functioning an evolutionary perspective. New Phytol. 162: Sperry JS, Hacke UG, Oren R, Comstock JP Water deficits and hydraulic limits to water supply. Plant Cell Environ. 25: Sperry JS, Hacke UG, Wheeler JK Comparative analysis of end wall resistivity in xylem conduits. Plant Cell Environ. 28: Stiller V, Lafitte HR, Sperry JS Hydraulic properties of rice and the response of gas exchange to water stress. Plant Physiol. 132: Stratton L, Goldstein G, Meinzer FC Stem water storage capacity and efficiency of water transport: their functional significance in a Hawaiian dry forest. Plant Cell Environ. 23: Trifilo P, Gasco A, Raimondo F, Nardini A, Salleo S Kinetics of recovery of hydraulic conductance and vein functionality from cavitation-induced embolism in sunflower. J. Exp. Bot. 54: Trifilo P, Nardini A, Lo Gullo MA, Salleo S Vein cavitation and stomatal behaviour of sunflower (Helianthus annuus) leaves under water limitation. Physiol. Plant. 119: Tsuda M, Tyree MT Plant hydraulic conductance measured by the high pressure flow meter in crop plants. J. Exp. Bot. 51: Tyree MT, Benis M, Dainty J Water relations of hemlock (Tsuga canadensis). 3. Temperature dependence of water exchange in a pressure bomb. Can. J. Bot. 51: Tyree MT, Cheung YNS Resistance to water flow in Fagus grandifolia leaves. Can. J. Bot. 55: Tyree MT, Cruiziat P, Benis M, Lo Gullo MA, Salleo S The kinetics of rehydration of detached sunflower leaves from different initial water deficits. Plant Cell Environ. 4: Tyree MT, Nardini A, Salleo S Hydraulic architecture of whole plants and single leaves. In L Arbre 2000 the Tree, ed. M Labrecque, pp Montreal: Isabelle Quentin Publ Tyree MT, Nardini A, Salleo S, Sack L, El Omari B The dependence of hydraulic conductance on irradiance during HPFM measurements: any role for stomatal response? J. Exp. Bot. 56: Tyree MT, Sinclair B, Lu P, Granier A Whole shoot hydraulic resistance in Quercus species measured with a new high-pressure flowmeter. Ann. Sci. For. 50: Tyree MT, Sobrado MA, Stratton LJ, Becker P Diversity of hydraulic conductance in leaves of temperate and tropical species: possible causes and consequences. J. Trop. For. Sci. 11: Tyree MT, Yianoulis P The site of water evaporation from sub-stomatal cavities, liquid path resistances and hydroactive stomatal closure. Ann. Bot. 46: Tyree MT, Zimmermann MH Xylem Structure and the Ascent of Sap. Berlin: Springer 136. Van Fleet DS The cell forms, and their common substance reactions, in the parenchyma-vascular boundary. Bull. Torrey Bot. Club 77: Wagner WH Reticulate veins in the systematics of modern ferns. Taxon 28: Warrit B, Landsberg JJ, Thorpe MR Responses of apple stomata to environmental factors. Plant Cell Environ. 3: Sack Holbrook

21 139. Weatherley PE The pathway of water movement across the root cortex and mesophyll of transpiring plants. In The Water Relations of Plants, ed. AJ Rutter, FH Whitehead, pp New York: Wiley 140. Wei CF, Tyree MT, Steudle E Direct measurement of xylem pressure in leaves of intact maize plants. A test of the cohesion-tension theory taking hydraulic architecture into consideration. Plant Physiol. 121: Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, et al The worldwide economics spectrum. Nature 428: Wylie RB The role of the epidermis in foliar organization and its relations to the minor venation. Am. J. Bot. 30: Wylie RB Relations between tissue organization and vascularization in leaves of certain tropical and subtropical dicotyledons. Am. J. Bot. 33: Wylie RB Principles of foliar organization shown by sun-shade leaves from ten species of deciduous dicotyledonous trees. Am. J. Bot 38: Wylie RB The bundle sheath extension in leaves of dicotyledons. Am. J. Bot. 39: Yang SD, Tyree MT Hydraulic architecture of Acer saccharum and A. rubrum: comparison of branches to whole trees and the contribution of leaves to hydraulic resistance. J. Exp. Bot. 45: Zwieniecki MA, Boyce CK, Holbrook NM Functional design space of singleveined leaves: role of tissue hydraulic properties in constraining size and shape. Ann. Bot. 94: Zwieniecki MA, Boyce CK, Holbrook NM Hydraulic limitations imposed by crown placement determine final size and shape of Quercus rubra L. leaves. Plant Cell Environ. 27: Zwieniecki MA, Hutyra L, Thompson MV, Holbrook NM Dynamic changes in petiole specific conductivity in red maple (Acer rubrum L.), tulip tree (Liriodendron tulipifera L.) and northern fox grape (Vitis labrusca L.). Plant Cell Environ. 23: Zwieniecki MA, Melcher PJ, Boyce CK, Sack L, Holbrook NM Hydraulic architecture of venation in Laurus nobilis L. Plant Cell Environ. 25: Leaf Hydraulics 381

22 Contents Annual Review of Plant Biology Volume 57, 2006 Looking at Life: From Binoculars to the Electron Microscope Sarah P. Gibbs 1 Annu. Rev. Plant. Biol : Downloaded from arjournals.annualreviews.org MicroRNAs and Their Regulatory Roles in Plants Matthew W. Jones-Rhoades, David P. Bartel, and Bonnie Bartel 19 Chlorophyll Degradation During Senescence S. Hörtensteiner 55 Quantitative Fluorescence Microscopy: From Art to Science Mark Fricker, John Runions, and Ian Moore 79 Control of the Actin Cytoskeleton in Plant Cell Growth Patrick J. Hussey, Tijs Ketelaar, and Michael J. Deeks 109 Responding to Color: The Regulation of Complementary Chromatic Adaptation David M. Kehoe and Andrian Gutu 127 Seasonal Control of Tuberization in Potato: Conserved Elements with the Flowering Response Mariana Rodríguez-Falcón, Jordi Bou, and Salomé Prat 151 Laser Microdissection of Plant Tissue: What You See Is What You Get Timothy Nelson, S. Lori Tausta, Neeru Gandotra, and Tie Liu 181 Integrative Plant Biology: Role of Phloem Long-Distance Macromolecular Trafficking Tony J. Lough and William J. Lucas 203 The Role of Root Exudates in Rhizosphere Interactions with Plants and Other Organisms Harsh P. Bais, Tiffany L. Weir, Laura G. Perry, Simon Gilroy, and Jorge M. Vivanco 233 Genetics of Meiotic Prophase I in Plants Olivier Hamant, Hong Ma, and W. Zacheus Cande 267 Biology and Biochemistry of Glucosinolates Barbara Ann Halkier and Jonathan Gershenzon 303 v