ANRV274-PP57-14 ARI 27 March 2006 11:4

Leaf HydraulicsLawren Sack1 and N. Michele Holbrook2

1Department of Botany, University of Hawai‘i at Manoa, Honolulu, Hawaii 96822;email: LSack@hawaii.edu2Department of Organismic and Evolutionary Biology, Harvard University,Cambridge, Massachusetts 02138

Annu. Rev. Plant Biol.2006. 57:361–81

The Annual Review ofPlant Biology is online atplant.annualreviews.org

doi: 10.1146/annurev.arplant.56.032604.144141

Copyright c© 2006 byAnnual Reviews. All rightsreserved

First published online as aReview in Advance onJanuary 30, 2006

1543-5008/06/0602-0361$20.00

Key Words

aquaporins, cavitation, embolism, stomata, xylem

AbstractLeaves are extraordinarily variable in form, longevity, venation ar-chitecture, and capacity for photosynthetic gas exchange. Much ofthis diversity is linked with water transport capacity. The pathwaysthrough the leaf constitute a substantial (≥30%) part of the resistanceto water flow through plants, and thus influence rates of transpirationand photosynthesis. Leaf hydraulic conductance (Kleaf) varies morethan 65-fold across species, reflecting differences in the anatomy ofthe petiole and the venation architecture, as well as pathways beyondthe xylem through living tissues to sites of evaporation. Kleaf is highlydynamic over a range of time scales, showing circadian and develop-mental trajectories, and responds rapidly, often reversibly, to changesin temperature, irradiance, and water supply. This review addresseshow leaf structure and physiology influence Kleaf, and the mecha-nisms by which Kleaf contributes to dynamic functional responses atthe level of both individual leaves and the whole plant.

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Contents

INTRODUCTION. . . . . . . . . . . . . . . . . 362LEAF HYDRAULIC

CONDUCTANCE . . . . . . . . . . . . . . 362Relation to Whole-Plant Hydraulic

Conductance . . . . . . . . . . . . . . . . . . 363Maximum Leaf Hydraulic

Conductance Across Speciesand Life Forms . . . . . . . . . . . . . . . 364

PATHWAYS OF WATERMOVEMENT IN THE LEAF . . . 364Water Movement Through Leaf

Xylem: Petiole and Venation . . 364Water Movement Outside the

Xylem: Bundle Sheath andMesophyll . . . . . . . . . . . . . . . . . . . . 365

Partitioning the Leaf HydraulicResistance. . . . . . . . . . . . . . . . . . . . . 366

COORDINATION OF MAXIMUMLEAF HYDRAULICCONDUCTANCE WITH LEAFSTRUCTURE ANDFUNCTION . . . . . . . . . . . . . . . . . . . . 367Coordination with Gas Exchange . 367

Coordination with LeafFlux-Related Structural Traits . 368

Independence of Maximum Kleaf

and Traits Related to Leaf MassPer Area, or to Leaf DroughtTolerance . . . . . . . . . . . . . . . . . . . . . 369

DYNAMICS OF LEAFHYDRAULICS OVER SHORTAND LONG TIME SCALES . . . . 369Responses of Leaf Hydraulic

Conductance to Dehydrationand Damage . . . . . . . . . . . . . . . . . . 369

Responses of Leaf HydraulicConductance to Changes inTemperature and Irradiance . . . . 371

Diurnal Rhythms in LeafHydraulic Conductance. . . . . . . . 372

Trajectories of Leaf HydraulicConductance DuringDevelopment and Leaf Aging . . 372

Plasticity of Leaf HydraulicConductance Across GrowingConditions . . . . . . . . . . . . . . . . . . . . 372

Kleaf: leaf hydraulicconductance (unitsmmol m−2 s−1

MPa−1)

INTRODUCTION

The role of the hydraulic system in constrain-ing plant function has long been recognized(15, 37, 135), but until recently the hydraulicproperties of leaves had received little sus-tained attention. This is somewhat surprisinggiven that the leaf constitutes an importanthydraulic bottleneck. Research in previousdecades focused on the question of the majorpathways for water movement across leaves(14, 38). Current research on leaf hydraulicscontinues to elucidate these pathways, as wellas seeks to understand the influence of the wa-ter transport pathways on gas exchange rates,the coordination of hydraulic design with leafstructural diversity, and the dynamics of leafhydraulic conductance, diurnally, over the leaflifetime, and in response to multiple environ-mental factors (Figure 1).

LEAF HYDRAULICCONDUCTANCE

Kleaf is a measure of how efficiently water istransported through the leaf, determined asthe ratio of water flow rate (Fleaf) throughthe leaf (through the petiole and veins, andacross the living tissues in the leaf to the siteswhere water evaporates into the airspaces) tothe driving force for flow, the water potentialdifference across the leaf (�� leaf). Kleaf is typi-cally normalized by leaf area (i.e., Fleaf/�� leaf

is further divided by lamina area; units ofmmol water m−2 s−1 MPa−1). Hydraulic con-ductance is the inverse of resistance, Rleaf. Kleaf

is the more commonly used metric. However,because resistances are additive in series, Rleaf

is used in discussion of the leaf as a componentof whole-plant resistance, or when partition-ing the resistances within the leaf.

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Why does Kleaf have such a strong influ-ence on water movement through the wholeplant? The resistance of open stomata to vapordiffusion out of the leaf is typically hundredsof times greater than the hydraulic resistanceto bulk flow of the liquid moving throughthe plant (37). Transpiration rates are thusdictated by this diffusion process, which inturn depends on the stomatal and boundary-layer conductances and the difference in vaporpressure between the intercellular air spacesof the leaf and the atmosphere (Figure 1).However, the maintenance of open stomatadepends on having a well-hydrated leaf inte-rior, i.e., a high leaf water potential (� leaf).From the Ohm’s law analogy for the soil-plant-atmosphere continuum (52, 135),

�leaf = �soil − ρgh − E/Kplant, 1.

where E, �soil, ρ, g, h, and Kplant represent,respectively, transpiration rate, soil water po-tential, the density of water, acceleration dueto gravity, plant height, and the whole-planthydraulic conductance. Thus, at a given soilwater supply, � leaf declines with higher E, witha sensitivity that depends on Kplant. For a leaf tosustain � leaf at a level high enough to maintainstomata open (i.e., for the leaf to maintain ahigh E, or a high gs), Kplant must be sufficientlyhigh. Consequently, Kplant strongly constrainsplant gas exchange. As shown in the following,Kleaf is a major determinant of Kplant.

Relation to Whole-Plant HydraulicConductance

Leaves contribute a majority of the hydraulicresistance to water flow in shoots, and form asubstantial part of the hydraulic resistance inwhole plants (80, 132, 146). For 34 species ofa range of life forms, the leaf, including peti-ole, contributed on average ≈30% of Rplant

(Rplant = 1/Kplant) (99). However, there arecases in which the leaf is reported to con-tribute up to 80% to 98% of Rplant (23, 80).Notably, the contribution of Rleaf will varywith time of day; early in the day, when thereis net water movement from stem storage (48,

Kroot

Ksoil

Kstem

Kleaf

gs

gb

E

VPD

Ψleaf

Ψsoil

Irradiance Temperature

Waterstorage

Ψstem xylem

Kplant

Figure 1Leaf hydraulic conductance (Kleaf) as a component in a simplified electroniccircuit analog of the whole-plant system (modified after 52). Ksoil, Kroot,Kstem, and Kplant represent, respectively, the hydraulic conductance (inverseof resistance) of soil, root, stem, and plant; �soil, �stem xylem, and � leafrepresent the water potentials of soil, stem xylem, and leaf; gs, gb, E, andVPD represent the stomatal and boundary-layer conductances,transpiration rate, and leaf to air vapor pressure difference. This schema ismuch simplified, as � leaf will vary across a crown because of heightdifferences as well as differences in transpiration and hydraulic supply todifferent leaves (88, 130). Impacts of microclimate on gs and Kleaf are shownwith red arrows; thus, Kleaf, like gs and gb, is represented as a variableconductance; decreases in � leaf, an internal variable, “drive” declines inKleaf via its linkage with increasing xylem tensions.

123), leaves are likely to constitute a higherproportion of resistance than when water isobtained directly from the soil (Figure 1).Additionally, Rleaf changes with temperature,water supply, and irradiance, and as leaves age

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E: transpiration rate(units mmol m−2

s−1)

Ψsoil: soil waterpotential (units MPa)

Ψleaf: leaf waterpotential (units MPa)

Kplant: whole-planthydraulicconductance (unitsmmol m−2 s−1

MPa−1)

Kmaxleaf : maximum

leaf hydraulicconductance (i.e., forhydrated leaf; unitsmmol m−2 s−1

MPa−1)

(see section on Dynamics of Leaf HydraulicsOver Short and Long Time Scales), and canthus increase as a proportion of Rplant to be-come the dominant factor in defining whole-plant water transport capacity.

Maximum Leaf HydraulicConductance Across Speciesand Life Forms

Measurements of leaf hydraulic conductancefor hydrated leaves (K max

leaf ), made with sev-eral methods (103), indicate a dramatic vari-ability across the 107 species so far examined(Figure 2). K max

leaf ranges 65-fold from the low-est value (for the fern Adiantum lunulatum;0.76 mmol m−2 s−1 MPa−1) to the highest (forthe tropical tree Macaranga triloba; 49 mmolm−2 s−1 MPa−1). K max

leaf is highly variable withina life form, varying by tenfold among coexist-ing tree species (104), and on average tendsto be lowest for conifers and pteridophytes,higher for temperate and tropical woodyangiosperms, and highest for crop plants(Figure 2). The model species Arabidopsisthaliana and Nicotiana tabacum have moderate

Crop herbs

Temperate woody angiosperms

Tropical woody angiosperms

Conifers

Pteridophytes

All species average

0 10 20 3 400

Leaf hydraulic conductance(mmol m-2 s-1 MPa-1)

Figure 2Leaf hydraulic conductance averaged for contrasting life forms (forhydrated whole leaves, including petiole, and when possible for fullyilluminated sun leaves; data pooled across plant age and habitat;pteridophytes, 4 species, 19, 24; conifers, 6 species, 7, 24, 133; temperatewoody angiosperms, 38 species; 1, 24, 34, 47, 63, 64, 81, 83, 92, 99, 102,106, 130–133, 146; tropical woody angiosperms, 49 species, 7, 16–20, 24,41, 104, 118, 131, 133; crop herbs, 7 species, 65, 82, 115, 117, 124–126;all species average for 107 species also includes 2 grass species, 19, 66; andArabidopsis, 68) Error bars = 1 SE.

values of 12 and 26 mmol m−2 s−1 MPa−1, re-spectively (68, 115). Interspecific variation inK max

leaf reflects differences in the anatomy of thepetiole and venation, as well as pathways be-yond the xylem through living tissues to sitesof evaporation.

PATHWAYS OF WATERMOVEMENT IN THE LEAF

Water Movement Through LeafXylem: Petiole and Venation

On entering the petiole of a dicotyledonousleaf, the vascular bundles in the leaf tracesreorganize, differentially supplying midribbundles, which branch into the second- andthird-order veins (42, 58). Water exits the ma-jor veins into the surrounding tissue, or intothe minor veins, the tracheid-containing fineveins embedded in the mesophyll (5, 27). Indicotyledons the minor veins account for thepreponderance of the total vein length (e.g.,86%–97% in temperate and tropical trees)(91, 100). Thus, the bulk of transpired wa-ter will be drawn out of minor veins, resultingin the major and minor veins acting approxi-mately in series (99, 146).

Leaf vein systems are enormously variablein many aspects: in vein arrangement and den-sity; and in the number, size, and geometryof the vascular bundles in the veins; and ofthe xylem conduits within the bundles (97).These structural characteristics play a criti-cal role in how water is distributed across theleaf, and thus an increasing number of stud-ies focus on the relationship of K max

leaf to ve-nation architecture. K max

leaf correlates with thedimensions of conduits in the midrib (1, 3,79, 100), and for ten species of tropical trees,correlated strongly with the midrib conduc-tivity calculated from the Poiseuille equationfor the xylem conduits (100). This correlationdoes not imply that the midrib is a substantialconstraint on the conductance of the vena-tion, or on K max

leaf , but rather implies a scaling ofhydraulic resistances throughout the leaf (seebelow) (100). Higher minor vein density in

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general corresponds to a higher supply capac-ity (or K max

leaf ), not by increasing the conduc-tance through the vein xylem system per se(34), but rather primarily by increasing thesurface area for exchange of xylem water withsurrounding mesophyll, and reducing the dis-tance through which water travels outside thexylem (97, 100). By contrast, the arrangementand density of major veins is not related toK max

leaf (100). However, major vein arrangementplays an essential role in distributing waterequitably across the lamina (97, 150), and re-dundancy of major veins could buffer the im-pacts of damage and/or cavitation (discussedbelow).

Water Movement Outside the Xylem:Bundle Sheath and Mesophyll

Water movement pathways outside the xylemare complex and potentially vary stronglyacross species that diverge in leaf mesophyllanatomy. Important progress has been madeon this critical topic, although a full under-standing will likely require new approaches.

Once water leaves the xylem, it enters thebundle sheath, made up of parenchymatouscells wrapped around the veins (42). A num-ber of early studies concluded that water exitsthe xylem through cell walls, moving aroundthe bundle sheath protoplasts, because mem-branes were thought to be too resistive tooccur in the transpirational pathways (e.g.,12, 13). However, the presence of aquaporinsand the high surface area for water transportacross the membranes of bundle sheath cellsmeans that intercellular water movement is,in fact, plausible (53, 68, 102, 112). Indeed,in some species, water seems constrained toenter bundle sheath cells by suberized per-pendicular walls, a barrier analogous to theroot Casparian strip (60, 136). Dye exper-iments suggest movement into the bundlesheath cells; in leaves transpiring a solutionof apoplastic dye, crystals form in the minorveins (27). Other evidence comes from thetemperature response of measured Kleaf (69,102) and the recently demonstrated role of

aquaporins (82, but see 68), both consistentwith crossing membranes (see below). Thebundle sheath cells may be a “control center”in leaf water transport, the locus for the strik-ing temperature and light responses of Kleaf.

What happens to water once it passes outof the xylem into the bundle sheath and be-yond? Although this is clearly a question ofgreat importance, current evidence remainsindirect. A large portion of the mesophyll vol-ume is airspace, with limited cell-to-cell con-tact, but spongy mesophyll cells are in con-tact to a far greater degree than palisade cells,and thus would seem better suited to con-duct water (142, 143). The epidermis has sub-stantial cell-to-cell contact, and water couldmove directly there from the minor veins,in species with bundle sheath extensions—tightly packed, chloroplast-free cells that con-nect the bundle sheath that surrounds the mi-nor veins to the epidermides in many species(70, 145). In those species, the epidermis canremain hydrated despite having little verti-cal contact with the photosynthetic meso-phyll (59, 138). In species lacking bundlesheath extensions, water must move acrossthe mesophyll. Whether water moves prin-cipally apoplastically (i.e., in the cell walls),transcellularly (i.e., crossing membranes), orsymplastically (i.e., cell-to-cell via plasmo-desmata) is not yet known, and probably dif-fers among species and conditions. The firstexperimental studies on sunflower suggestedthat apoplastic movement dominates duringtranspiration, and that water crosses mes-ophyll membranes only during rehydrationor growth (13, 139). However, other exper-iments showed that movement through sym-plastic routes was plausible (129, 134); the cellpressure probe has indicated significant sym-plastic water transport among mesophyll cellsin succulent Kalanchoe leaves (77).

Finally, there is the question of wherein the leaf water evaporates, important be-cause the resistances in the pathways to thosesites will determine overall Rleaf. Mathemat-ical and physical models predict that evap-oration inside the leaf will occur principally

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near the stomata—from surrounding epider-mal cells, and/or from the mesophyll directlyabove the stomata, and/or from the guard cellsthemselves (71, 134). However, such modelsdo not account for the fact that in at leastseveral species, the cuticle extends into thesubstomatal cavity, potentially reducing evap-oration (90 and references therein). An alter-native scenario is that most water evaporatesdeep within the mesophyll, close to the veins(13, 14). Circumstantial support for this ideacomes from the fact that the measurement ofresistance to helium diffusion across an am-phistomatous leaf equaled about twice thatof water vapor out of the leaf—which trav-els half the distance (43), suggesting that wa-ter begins its diffusion deep within the leaf(14). A third scenario is that water evapo-rates relatively evenly throughout the mes-ophyll (87). This scenario predicts a vapordiffusion pathway similar to that of CO2 as-similated during photosynthesis (though op-posite in direction). Indeed, the computationof intercellular CO2 concentration using typ-ical photosynthesis systems relies on this as-sumption (44), as does the use of the pres-sure bomb to estimate the driving force fortranspiration (103, 146). Where water princi-pally evaporates within the leaf is not clear;the data from modeling, dye studies, bio-physics, and gas exchange measurements donot provide a coherent story. A definitive an-swer is likely to require new approaches, suchas the use of in vivo imaging to track changesin cell dimensions within transpiring leaves(e.g., 111).

A complete understanding of water flowpathways will illuminate several important as-pects of leaf function, including the enrich-ment of oxygen isotopes (6), and the responseof stomata to leaf water status. Guard cellscan respond within seconds (93, 95, 98, 114);their movement depends on cell water poten-tial and turgor pressure, which in turn de-pends on where precisely the bulk of waterevaporates in the leaf, and on the hydraulicconductances from the veins to epidermis andguard cells (e.g., 26, 45). Quantifying these

parameters should help explain the onset ofpatchy behavior of stomata at small scales(76).

Partitioning the Leaf HydraulicResistance

How is Kleaf determined from these complexpathways of water movement? This questionis especially important because the way inwhich the leaf hydraulic resistance ( = 1/Kleaf)is partitioned between the xylem and acrossthe extraxylem pathways will strongly influ-ence the responsiveness of Rleaf to changingconditions. If the resistance of the leaf xylem(Rxylem) is a major component of Rleaf, thenthe enormous variation in venation architec-ture across species could reflect strong differ-ences in Rleaf. That would be very unlikely,however, if Rxylem were negligible relative tothe extraxylem resistance (Routside xylem); in thatcase, even large relative differences in Rxylem

among species would have little impact onoverall Rleaf. Additionally, the larger Rxylem is,relative to Routside xylem, the greater the effecton Rleaf of changes in Rxylem due to environ-ment (e.g., drought-induced cavitation; see72). Thus, substantial discussion surroundsthe issue of where the major resistances towater flow occur within leaves (e.g., 34, 47,82, 102, 104). Some of this controversy re-sulted from methodological differences, in-cluding the failure to take into account theeffect of irradiance on Rleaf (see below) andthe use of treatments to determine Rxylem thatopened up pathways for water to move outof low-order veins, bypassing conduit endingsand higher-order veins that contain higher re-sistance; using those methods resulted in esti-mates of Rxylem as 27% of Rleaf, averaged for theten species tested (12, 34, 109, 125, 128–130,146). Recent studies conducted under high ir-radiance, in which only minor veins were sev-ered, found Rxylem to be 59% of Rleaf, averagedfor 14 species (47, 82, 102, 104).

The current consensus is that the hydraulicresistance of the leaf’s xylem is about the sameorder as in the extraxylem pathways (47, 79,

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82, 102, 104; but see 34), and that species varyin their partitioning. Indeed, among tropi-cal trees, the % of Rleaf in the xylem dif-fered significantly between species (rangingfrom 26% to 89%); species that establish inhigh-light environments had 70% of Rleaf inthe xylem on average, whereas those fromlow irradiance had 52% (104). Despite thisvariation, across the range of species’ values,Rxylem, Routside xylem and Rleaf were linearly cor-related across species (104). The implicationsof this finding are that differences in vena-tion architecture reflect strong differences inRleaf, and also that Rleaf will be sensitive tochanges in the conductance of both the xylemand extraxylem pathways. Indeed, the ratioof Rxylem to Routside xylem is dynamic. For ex-ample, Rxylem will increase if vein xylem em-bolizes during drought, whereas Routside xylem

changes according to an endogenous circa-dian rhythm, and also increases under low ir-radiance (82, 101, 131); both resistances in-crease at lower temperatures, with Routside xylem

increasing more strongly (69, 102; seebelow).

Because leaf vein systems consist of watermovement through a well-defined arrange-ment of fixed tubes, they should be amenableto quantitative methods used in the studyof biological (and other) networks (e.g., 8,34, 66, 102, 140, 147). In the most anatom-ically explicit model to date, Rxylem is esti-mated for dicotyledonous leaves by assumingPoiseuille flow through a network parame-terized with measured venation densities andconduit numbers and dimensions (34). How-ever, contrary to empirical data, which showedthat Rxylem constitutes on average over 50% ofRleaf (see above), the model suggested from thexylem conduit measurements that Rxylem wasonly ≈2% of Rleaf. Thus, anatomical featuresnot included in the model, for example, theresistance to water movement between xylemconduits, must play an important role (34,121). Next generation studies will improveour ability to scale up from anatomical mea-surements to accurate prediction of venationnetwork Rxylem.

gs: stomatalconductance to watervapor (units mmolm−2 s−1)

COORDINATION OF MAXIMUMLEAF HYDRAULICCONDUCTANCE WITH LEAFSTRUCTURE AND FUNCTION

The coordination of hydraulics with leafstructure and gas exchange is likely to haveplayed a critical role in the early evolu-tion of the laminate leaf. Lower CO2 levelsand cooler temperatures during the Devo-nian would have allowed large leaves to avoidoverheating, but the higher stomatal densities,which evolved to maintain CO2 assimilation,would have led to more rapid transpiration(89) and thus required concomitant increasesin leaf hydraulic capacity (9–11). The coordi-nation among leaf hydraulic supply and de-mand and leaf form remains a key design ele-ment among modern plants.

Coordination with Gas Exchange

Recent work demonstrates correlations acrossspecies between liquid phase (hydraulic) con-ductances of stems, shoots, or whole plantsand vapor phase (stomatal) conductance (gs)and maximum rates of gas exchange (e.g.,3, 54, 57, 73, 74, 80, 110). Consistent withthis matching of hydraulic supply and demandis the strong coordination across species be-tween K max

leaf and stomatal pore area per leafarea, maximum gs, and photosynthetic capac-ity (3, 19, 24, 99, 104).

What is the basis for the interspecific co-ordination of leaf hydraulic properties andgas exchange? The coordination of Kplant (andKleaf) and maximum gs and E would arisefrom convergence among species in � leaf,�soil, boundary-layer conductance and leaf-to-air vapor pressure difference (see Equation1 and Figure 1) (104). Given that hydraulicconductances scale through the plant (99),species would converge also in the water po-tential of the stem xylem proximal to the leaf(�stem xylem), the water potential drop acrossthe leaf (�� leaf = � leaf − �stem xylem ), andthat across the whole plant (��plant = � leaf −�soil; 74). The linkage indicates a “standard-ization” of water relations among plants of

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a given life form and vegetation type duringpeak transpiration, when soil is moist. There isevidence of strong convergence in water rela-tions parameters � leaf, �stem xylem, �� leaf, and�soil during peak transpiration for plants of agiven system in moist soil during the grow-ing season (23, 24, 55, 80, 123). The typicallymodest range in these parameters (typically± <0.5 MPa) occurs despite variation withina vegetation type in plant size and age, root-ing depth and vulnerability to cavitation, aswell as divergence among species in the sea-son during which they manifest peak activ-ity, which would further destabilize the co-ordination (104). The convergence in �� is

Table 1 Leaf structural and functional traits, sortedby putative association with maximum water flux perarea (and Kleaf), leaf mass per area, or droughttolerancea across species

Maximum flux-related traitsLeaf hydraulic conductanceStomatal pore areaStomatal conductanceNet maximum photosynthesis per areaLeaf midrib xylem conduit diametersMesophyll area/leaf areaThickness of leaf and palisade mesophyllLeaf chlorophyll concentration per areaLeaf nitrogen concentration per areaLeaf shape (margin dissection)Leaf water storage capacitance per area

Leaf mass per area-related traitsLeaf densityLeaf thicknessLeaf lifespanLeaf chlorophyll concentration per mass (negativelyrelated)Leaf nitrogen concentration per mass (negatively related)Leaf water content per mass (negatively related)

Leaf drought tolerance traitsCuticular conductance (negatively related)Modulus of elasticity (variably related)Leaf density (variably related)Leaf water storage capacitance per areaOsmotic potentials at full and at zero turgorResistance to leaf xylem cavitation

aAssociations are positive except when noted.

analogous to the range of household appli-ances in a given country being designed torun at a given voltage—from lamps to ovens—with the current through the appliance de-pendent on the electric conductance, orresistance.

The finding of narrowly constrained wa-ter relations in a given vegetation type pro-vides a potentially powerful basis for a gen-eral relationship between Kleaf and maximumrates of gas exchange. In addition, increasedunderstanding of how the coordination ofK max

leaf and gas exchange shifts across life formsand habitats will allow prediction of perfor-mance differences for plants adapted to dif-ferent zones around the world. One study sofar has demonstrated that the coordinationbetween hydraulics and gas exchange variesamong vegetation types: Tropical rainforesttrees as a group have higher potential gas ex-change relative to Kleaf than temperate decid-uous trees, consistent with their adaptation tohigher � leaf and �soil, and/or lower VPD dur-ing peak activity (104).

Coordination with Leaf Flux-RelatedStructural Traits

Leaves vary tremendously in area, thickness,shape, nutrient concentrations, and capac-ity for gas exchange. The intercorrelationof many traits places some bound on thisdiversity, for instance among those relatedto carbon economy, including leaf mass perarea (LMA; leaf dry mass/area), leaf lifespan(e.g., 96, 141), and nitrogen concentration permass and net maximum photosynthetic rateper mass (Amass; 141), and provides a frame-work for understanding the integrated func-tion of clusters of traits. Similarly, coordina-tion among traits related to water flux throughleaves exists for plants of a particular lifeform and habitat (99) (Table 1). In additionto their higher total maximum stomatal porearea and gas exchange per area (see above; 3,19, 99), leaves with high K max

leaf tend to havewider xylem conduits in the midrib and highervenation densities (3, 102). K max

leaf correlated

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with palisade thickness, and palisade/spongymesophyll ratio for tropical rainforest treespecies (100), and with total leaf thicknessand water storage capacitance per area fortemperate woody species (99). These correla-tions arose due to structural coordination—the sharing of an anatomical or devel-opmental basis—and/or due to functionalcoordination—the coselection of charactersfor benefit in a particular environment (99,116).

Independence of Maximum Kleaf andTraits Related to Leaf Mass Per Area,or to Leaf Drought Tolerance

Certain leaf traits show a disproportionatenumber of linkages with other traits (86).LMA is one such “hub” trait (Table 1). How-ever, K max

leaf , a hub trait in its own right (beinglinked with many water-flux traits), is unre-lated to LMA (Table 1) (20, 78, 99, 104, 133).Because this complex of water flux–relatedtraits is coordinated with net maximum pho-tosynthesis per leaf area, which is equal toLMA in its driving differences in Amass acrossspecies globally (data in 141), and becauseAmass generally scales up to whole-plant rel-ative growth rate, water flux–related traits in-cluding Kleaf are a potentially fundamental de-terminant of species performance differences.However, K max

leaf is apparently independent ofa partially interrelated complex of traits as-sociated with leaf drought tolerance, i.e., theability to maintain positive turgor and gas ex-change at low � leaf (Table 1). These traits areevidently coselected by desiccating conditions(85, 107), and include low osmotic potentialsat full and at zero turgor, and low cuticularconductance (99, 100).

DYNAMICS OF LEAFHYDRAULICS OVER SHORTAND LONG TIME SCALES

Kleaf is highly dynamic, varying over a widerange of time scales, from minutes to months,and according to microclimate and growing

LMA: leaf mass perarea (leaf drymass/area; unitsg m−2)

conditions. The dynamics of Kleaf are typicallyclosely correlated with those of gas exchange(Equation 1 and Figure 1) (32, 35, 36, 69,72). As Kleaf declines (e.g., owing to dehydra-tion), � leaf will similarly decline, and stomatawill close as, or before, � leaf becomes damag-ing, leading to reduction of gs and E (32, 108).In droughted plants such a mechanism oper-ates in tandem with chemical signals from theroots to close the stomata (36, 39). Associateddeclines in intercellular CO2 concentration(ci) drive a reduction in photosynthetic rate(46, 69). Declines in � leaf can also directly re-duce photosynthetic rate metabolically (40).Why is Kleaf dynamic, given that its declinedrives such loss of function? Kleaf reductionduring water stress would protect the xylemby driving stomatal closure, thus alleviatingthe tensions in the transpiration stream. Also,membrane channels important in maintain-ing a high Kleaf require metabolic energy forexpression and potentially for activation.

Responses of Leaf HydraulicConductance to Dehydrationand Damage

The hydraulic conductance of the petiole(Kpetiole) and of the whole leaf declines dur-ing drought, correlating in vivo with declinesin 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 con-tributing to the decline of Kleaf at low � leaf

is xylem cavitation (55, 83, 149). Petioles withlower conductance take up dye into fewer ves-sels (25, 149), and dehydrated leaves take updye into fewer minor veins in the network (83,105, 124, 125). The xylem can become in-creasingly vulnerable with increasing dryingiterations—i.e., “cavitation fatigue,” as shownin petioles of Aesculus hippocastanum (50).However, cavitation is not the only poten-tial source of Kleaf decline during dehydration.Dehydrating conifer leaves decline in Kleaf

owing to collapse of xylem conduits, whichprecedes cavitation (21, 33). The potentialcollapse of xylem conduits in dicotyledonous

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Mean reduction of leaf hydraulic conductance ingiven conditions

0% 20% 40% 60% 80% 100%

a

Ψleaf = -1 MPa

Ψleaf = -2 MPa

Ψleaf = -3 MPa

Leaf dehydration

b Leaf measured under low vs. high irradiance

c Older leaf vs. younger leaf

dShade vs. sun leaf

Plants grown in 2% vs. 8% daylight

e Plants grown in low vs. high water supply

Figure 3Leaf hydraulic conductance is highly dynamic, as shown by the responses depicted here with respect tocontrols (color as a proportion of white bars). Note that the averaged responses shown are onlyindicative—the responses vary strongly in magnitude according to the particular species and ranges ofconditions 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 leaf aging (9 tree species; 16, 18, 20, 64, 106); (d ) response to growthirradiance, 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 doesthe additional possibility of decline in con-ductance of the extra-xylem paths. A strik-ingly rapid and complete recovery of Kleaf

during rehydration has been documented af-ter rewatering droughted plants or rehydrat-ing partially dehydrated leaves (62, 63, 75,124). Such short-term increases in Kleaf re-sult from a diversity of mechanisms. For ex-ample, conifers elastically recover their xylemgeometry on rewatering (21, 33), whereas riceleaves reverse embolism through root pres-sure (122). Where root pressure is not op-erating, an active mechanism may exist forembolism refilling even when xylem tensionsexist, involving ion pumping or transient pres-sures, associated with increasing starch degra-dation (25, 124, 149).

Because the linkage of Kleaf and gas ex-change is mediated by � leaf and species di-

verge in their � leaf responses, the extent towhich Kleaf and gs remain coordinated dur-ing dehydration varies among species. Thedistance between � leaf at stomatal closure(�stomatal closure) and the � leaf at which thexylem is irreversibly embolized is termed thesafety margin (19, 119, 120). In species witha wide safety margin, the risk is minimal,as stomata close before Kleaf declines sub-stantially (19, 30, 32, 83). However, in otherspecies, with a narrow safety margin, gs de-clines by half only after Kleaf or Kpetiole de-cline by 20% or more (17–19, 25, 62, 63,80, 105, 108, 125). High safety margins pro-tect the xylem, but lower safety margins al-low plants to maintain gas exchange closerto the level of irreversible Kleaf decline (19,120). The decline in Kleaf would confer safetyto the whole-plant hydraulic system by aug-menting the decline in � leaf, accelerating

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stomatal closure, which would protect por-tions of the plant that are less easily replaced(18). The protection conferred will vary ac-cording to species, because species differ inwhether whole leaves, petioles, and midribsare more (17, 22, 28, 49, 84, 105, 108, 125),equally (33), or less (32, 49, 83, 122) vulner-able to loss of conductance compared withthe stem as � leaf declines (and xylem tensionsincrease).

One of the most commonly investigatedpatterns in stem hydraulics is a trade-offbetween hydraulic efficiency (i.e., maximumhydraulic conductance) and resistance todrought-induced cavitation (135). This pat-tern is not found in leaves: The vulnerabil-ity of Kleaf to drought is not higher for leaveswith high K max

leaf . In our analysis of the avail-able data for 13 species of ferns, trees, andherbs varying 42-fold in K max

leaf , � leaf at 50%loss of conductivity ranged from –1.3 MPa to–3 MPa, and was uncorrelated withK max

leaf (r2

= 0.07; P = 0.4; data of 17, 19, 63, 83, 124,125).

Kleaf is also reduced by herbivory and otherforms of mechanical vein damage. The inter-ruption of major veins was classically held tohave no effect on leaf function, as leaves oftensurvive with a perfectly healthy appearance(29, 91). However, damage that interrupts pri-mary veins in dicotyledonous leaves immedi-ately produces massive declines in Kleaf, andin gs and photosynthetic rates, which per-sist weeks later, after the wounded tissue hasscarred over; in some species, the leaves des-iccate (4, 51, 81, 98). Whether major vein dis-ruption leads to tissue death or not would de-pend at least as much on evaporative demandand on the leaf’s ability to reduce water loss(i.e., with an impermeable cuticle) as on theleaf’s vascular architecture. However, redun-dancy in the venation—such as conduits inparallel within each vein, and multiple veinsof each order—would buffer Kleaf against bothcavitation and damage, by providing pathwaysaround damaged or blocked veins (29, 51, 84,97, 137).

VPD: mole fractionvapor pressuredifference betweenleaf and outside air(units mol mol−1)

Responses of Leaf HydraulicConductance to Changes inTemperature and Irradiance

K maxleaf increases at higher temperatures, as

shown in experiments conducted in vivo, de-termining gas exchange while manipulatingtemperature and controlling other microcli-matic variables (46). This increase is only par-tially accounted for by the direct effects oftemperature on the viscosity of water. Inves-tigation of the temperature response of waterflow through shoots and leaves showed an ac-tivation energy of 26–27 kJ mol−1, but whenminor veins were severed, so that water wasforced through only xylem, the activation en-ergy dropped to ≈17 kJ mol−1, which corre-sponds to changes in the viscosity of water (12,102, 127, 128). Thus, the viscosity responseapplies to the xylem pathways, whereas an ex-traviscosity response applies to the pathwaysoutside the xylem (102), consistent with theflow path crossing membranes (68). The tem-perature induced changes in K max

leaf can allow� leaf and gs to remain stable even as E increasesdue to higher VPD (46, 69).

K maxleaf responds strongly to irradiance; for

many species Kleaf is much lower when mea-sured 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 acrossspecies, and can range up to a several-fold in-crease from low to high irradiance. The kinet-ics of the K max

leaf response to irradiance differssufficiently from that of stomatal aperture tosuggest that the light response arises in thehydraulic pathways through the mesophyll(131), and involves activation of aquaporins(53, 82, 131). These same channels appar-ently follow an endogenous circadian rhythm:In sunflower, K max

leaf increases up to 60% fromnight to day, and the rhythm can be reversedif photoperiod is switched, and the rhythmcontinues for days even when plants arekept in constant darkness (82). The responsecan be removed by treatment with HgCl2,and recovered by using mercaptoethanol,

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implying the agency of aquaporins (82). Insunflower, dark-acclimated leaves show astrong light response, but light-acclimatedleaves do not, suggesting that their waterchannels are already activated (82). The de-activation of aquaporins in the dark would beadaptive, assuming the maintenance of activ-ity requires energy expenditure. For plantskept in the dark for 1 h, or for 4–6 days,K max

leaf and shoot hydraulic conductances (mea-sured under high irradiance) were reduced by20%–75% on average (2, 117). The responseof K max

leaf to irradiance implies the existence ofa previously unknown level of control of aplant’s response to environment; this responsewould facilitate the increases of stomatal aper-ture and leaf gas exchange with increasingirradiance by improving water supply to themesophyll.

Diurnal Rhythms in Leaf HydraulicConductance

Kleaf is dynamic diurnally, and its changesreflect simultaneous responses to multiplefactors. As discussed above, Kleaf follows anendogenous circadian rhythm; Kleaf also in-creases with incident light over the scale ofminutes and hours (64, 101, 131). Addition-ally, Kleaf increases with temperature. By con-trast, Kleaf declines as leaves dehydrate underhigh midday temperatures and VPD. Thus,contrasting trends have been observed for thediurnal response of Kleaf. For sunflower, andfor four tree species, Kleaf increased by up totwo- to threefold over a few hours from morn-ing to midday, as irradiance and temperatureincreased, and then declined by evening, in asimilar pattern as g and E (64, 126). On theother hand, a midday decline in Kleaf by 30%to 50% has been observed for tree species astranspiration increased to high rates by mid-day (18, 83), apparently as a response to leafdehydration. Similar diurnal declines in con-ductance were found for tree petioles and forflow axially across rice leaves (25, 122, 149).In other species no diurnal patterns were ob-served (31, 149). Such variable patterns in di-

urnal responses of Kleaf are likely to reflect theparticular combinations of irradiance, leaf andair temperature, soil moisture, and VPD, aswell as endogenous rhythms. Thus, one wouldexpect Kleaf to increase each morning in re-sponse to internal cues, as well as increasingirradiance and temperature; but if E is drivenhigh enough by a high VPD (and/or if soil isdry), low � leaf would result in significant de-clines in Kleaf and in gs, recovering by the endof the day.

Trajectories of Leaf HydraulicConductance During Developmentand Leaf Aging

Kleaf is also dynamic over the lifetime of theleaf. Kleaf increases in developing leaves asthe vasculature matures (1, 20, 67). Weeksor months after Kleaf reaches its maximum,it begins to decline, with reductions of upto 80–90% at abscission (Figure 3c) (1, 16,18, 64, 100, 106). One factor contributing tothis decline of Kleaf is the accumulation of em-boli in the vein xylem, and eventual block-age by tyloses (106, 135). Kleaf would declinealso owing to reduction of the permeability ofcell walls or membranes (see 136). Decreasesin Kleaf would cause progressive dehydration,potentially contributing to the observed de-cline in midday � leaf as leaves age (16, 65,106). Reductions in Kleaf are coordinated withage-related declines in other functional traits,including leaf nitrogen concentration, stom-atal sensitivity to VPD, leaf osmotic poten-tial, and gas exchange (e.g., 56, 94). Somehave hypothesized that the seasonal declineof Kleaf is a trigger for leaf senescence (16,106).

Plasticity of Leaf HydraulicConductance Across GrowingConditions

Although most studies of leaf hydraulics havebeen performed on plants in high-resourceconditions, K max

leaf is highly plastic acrossgrowing conditions, owing to developmental

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changes in vein density, conduit sizes or num-bers (e.g., 3), and/or in the structure andconductivity of extraxylem pathways. Leavesexpanded in shade—or in crown positions li-able to shade—have low K max

leaf relative to sunleaves (Figure 3d) (99, 113), part of the com-plex of shade leaf characters including lowervein densities, smaller stomata, thinner leaves,less dissected leaf shape, and lower rates ofgas exchange (e.g., 61, 144, 148). In maturesunflower plants, K max

leaf was linearly related toirradiance from basal to apical leaves (65); inthis case an irradiance effect combines withan age effect. K max

leaf is also plastic across plant

growing conditions. K maxleaf and shoot hydraulic

conductance were lower for plants grown sev-eral months in lower irradiance (Figure 3d)(41), or in lower water or nitrogen supplies(Figure 3e) (1–3, 41). Such plasticity in K max

leafruns in parallel with adaptive differences, assun-adapted species tend to have several-foldhigher K max

leaf than shade-adapted species onaverage, for temperate and tropical speciessets (79, 104). These findings suggest thatK max

leaf plays a potentially important role in de-termining plant resource responses and alsoin determining ecological preferences amongspecies.

SUMMARY POINTS

1. K maxleaf varies at least 65-fold across species, and scales with Kplant; the leaf is a substantial

resistance in the plant pathway, 30% and upward of whole-plant resistance.

2. The partitioning of resistances within the leaf among petiole, major veins, minorveins, and pathways outside the xylem is variable across species. Substantial hydraulicresistances occur both in the leaf xylem as well as in the flow paths across the mesophyllto evaporation sites. These components respond differently to ambient conditions,including irradiance and temperature, indicating an involvement of aquaporins.

3. K maxleaf is coordinated with maximum gas exchange rates for species of a particular

life form and habitat. This coordination arises from convergence in water relationsparameters, especially � leaf at peak transpiration. K max

leaf is also coordinated with aframework of other traits related to leaf water flux, including stomatal pore area,midrib xylem conduit diameters, and palisade richness. However, K max

leaf is independentof the complex of traits linked with leaf mass per area, and traits relating to leaf droughttolerance.

4. Kleaf is highly dynamic—varying diurnally, as leaves age, and in response to changesin leaf hydration, irradiance, temperature, and nutrient supply. The decline in Kleaf inresponse to lower � leaf arises from reductions in xylem conductivity due to cavitationor collapse, and/or from changes in the conductivity of the pathways outside thexylem. Some short-term declines in Kleaf can be rapidly reversed. Dynamic changesin Kleaf impact gas exchange via stomatal regulation of � leaf and could play a role inleaf senescence.

FUTURE ISSUES

1. Still needed is a fully quantitative understanding of how K maxleaf is determined by the ve-

nation architecture and the extraxylem pathways, including the identity and behaviorof aquaporins in these pathways.

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2. The precise correlations that link Kleaf with gas exchange and leaf structure amongspecies of particular life forms and habitats need to be determined, as well as theshifts of this coordination across life forms and habitats. The patterns of generalcoordination will enable predictions of water relations behavior for whole sets ofspecies from simply measured hydraulic parameters.

3. The mechanisms for the diurnal and developmental dynamics of Kleaf, and for thereversible Kleaf responses to irradiance and to dehydration need to be elucidated indetail. Understanding the mechanisms behind these changes will enhance the abilityto model the influence of these dynamics on gas exchange over short and long timescales.

ACKNOWLEDGMENTS

We thank Kristen Frole for valuable assistance with the data compilation.

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Contents ARI 5 April 2006 18:47

Annual Reviewof Plant Biology

Volume 57, 2006Contents

Looking at Life: From Binoculars to the Electron MicroscopeSarah P. Gibbs � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

MicroRNAs and Their Regulatory Roles in PlantsMatthew W. Jones-Rhoades, David P. Bartel, and Bonnie Bartel � � � � � � � � � � � � � � � � � � � � � � � � � �19

Chlorophyll Degradation During SenescenceS. Hortensteiner � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �55

Quantitative Fluorescence Microscopy: From Art to ScienceMark Fricker, John Runions, and Ian Moore � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �79

Control of the Actin Cytoskeleton in Plant Cell GrowthPatrick J. Hussey, Tijs Ketelaar, and Michael J. Deeks � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 109

Responding to Color: The Regulation of Complementary ChromaticAdaptationDavid M. Kehoe and Andrian Gutu � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 127

Seasonal Control of Tuberization in Potato: Conserved Elements withthe Flowering ResponseMariana Rodríguez-Falcón, Jordi Bou, and Salomé Prat � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 151

Laser Microdissection of Plant Tissue: What You See Is What You GetTimothy Nelson, S. Lori Tausta, Neeru Gandotra, and Tie Liu � � � � � � � � � � � � � � � � � � � � � � � � � � 181

Integrative Plant Biology: Role of Phloem Long-DistanceMacromolecular TraffickingTony J. Lough and William J. Lucas � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 203

The Role of Root Exudates in Rhizosphere Interactions with Plantsand Other OrganismsHarsh P. Bais, Tiffany L. Weir, Laura G. Perry, Simon Gilroy,

and Jorge M. Vivanco � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 233

Genetics of Meiotic Prophase I in PlantsOlivier Hamant, Hong Ma, and W. Zacheus Cande � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 267

Biology and Biochemistry of GlucosinolatesBarbara Ann Halkier and Jonathan Gershenzon � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 303

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Bioinformatics and Its Applications in Plant BiologySeung Yon Rhee, Julie Dickerson, and Dong Xu � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 335

Leaf HydraulicsLawren Sack and N. Michele Holbrook � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 361

Plant Uncoupling Mitochondrial ProteinsAnıbal Eugenio Vercesi, Jiri Borecky, Ivan de Godoy Maia, Paulo Arruda,

Iolanda Midea Cuccovia, and Hernan Chaimovich � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 383

Genetics and Biochemistry of Seed FlavonoidsLoıc Lepiniec, Isabelle Debeaujon, Jean-Marc Routaboul, Antoine Baudry,

Lucille Pourcel, Nathalie Nesi, and Michel Caboche � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 405

Cytokinins: Activity, Biosynthesis, and TranslocationHitoshi Sakakibara � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 431

Global Studies of Cell Type-Specific Gene Expression in PlantsDavid W. Galbraith and Kenneth Birnbaum � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 451

Mechanism of Leaf-Shape DeterminationHirokazu Tsukaya � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 477

Mosses as Model Systems for the Study of Metabolism andDevelopmentDavid Cove, Magdalena Bezanilla, Phillip Harries, and Ralph Quatrano � � � � � � � � � � � � � � 497

Structure and Function of Photosystems I and IINathan Nelson and Charles F. Yocum � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 521

Glycosyltransferases of Lipophilic Small MoleculesDianna Bowles, Eng-Kiat Lim, Brigitte Poppenberger, and Fabian E. Vaistij � � � � � � � � � � � 567

Protein Degradation Machineries in PlastidsWataru Sakamoto � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 599

Molybdenum Cofactor Biosynthesis and Molybdenum EnzymesGunter Schwarz and Ralf R. Mendel � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 623

Peptide Hormones in PlantsYoshikatsu Matsubayashi and Youji Sakagami � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 649

Sugar Sensing and Signaling in Plants: Conserved and NovelMechanismsFilip Rolland, Elena Baena-Gonzalez, and Jen Sheen � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 675

Vitamin Synthesis in Plants: Tocopherols and CarotenoidsDean DellaPenna and Barry J. Pogson � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 711

Plastid-to-Nucleus Retrograde SignalingAjit Nott, Hou-Sung Jung, Shai Koussevitzky, and Joanne Chory � � � � � � � � � � � � � � � � � � � � � � 739

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The Genetics and Biochemistry of Floral PigmentsErich Grotewold � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 761

Transcriptional Regulatory Networks in Cellular Responses andTolerance to Dehydration and Cold StressesKazuko Yamaguchi-Shinozaki and Kazuo Shinozaki � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 781

Pyrimidine and Purine Biosynthesis and Degradation in PlantsRita Zrenner, Mark Stitt, Uwe Sonnewald, and Ralf Boldt � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 805

Phytochrome Structure and Signaling MechanismsNathan C. Rockwell, Yi-Shin Su, and J. Clark Lagarias � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 837

Microtubule Dynamics and Organization in the Plant Cortical ArrayDavid W. Ehrhardt and Sidney L. Shaw � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 859

INDEXES

Subject Index � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 877

Cumulative Index of Contributing Authors, Volumes 47–57 � � � � � � � � � � � � � � � � � � � � � � � � � � � 915

Cumulative Index of Chapter Titles, Volumes 47–57 � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 920

ERRATA

An online log of corrections to Annual Review of Plant Biology chapters (if any, 1977 tothe present) may be found at http://plant.annualreviews.org/

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