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Agricultural and Forest Meteorology 104 (2000) 1323

Hydraulic constraints on plant gas exchange

John S. Sperry

Department of Biology, University of Utah, 257 S 1400E Salt Lake City, UT 84112, USA

Abstract

Stomatal conductance (gs) and transpiration (E) are often positively correlated with the hydraulic conductance of thesoilleaf continuum (ksl ). Interaction betweengs andksl helps regulate water potential (9) of leaves. When soil and plant9 decreases during water stress,ksl decreases. A well-documented cause of the decrease inksl is xylem cavitation. Theinteraction betweenk and9 in xylem creates physical limits on the range of9 andE over which gas exchange can occur.Differences in drought tolerance between species correlate with hydraulic limits. Safety margins from complete hydraulicfailure are often small enough to require stomatal regulation of9 andE. While stomatal regulation avoids complete hydraulicfailure, controlled decreases in plantk can be substantial during drought. Decreasing plantk amplifies the effect of waterstress on the leaves and effectively increases the sensitivity of the stomatal response to drought. Increased stomatal sensitivitymay promote drought survival. 2000 Elsevier Science B.V. All rights reserved.

Keywords:Drought stress; Hydraulic conductance; Stomatal regulation; Water relations; Water transport; Xylem cavitation

1. Introduction

In response to water stress, plants regulate their tran-spiration by decreasing their stomatal conductance.Although this reduces their photosynthetic potential,they do this to avoid dehydrative damage to their cellsand tissues. Mutants lacking the stomatal closure re-sponse wilt and die under stress conditions that arereadily survived by wild type (Tal, 1966). Water stressis relative; a water potential that induces stomatal clo-sure in one species may have little effect on another.This is presumably because dehydrative damage oc-curs at different water potentials in different plants. Atpresent we lack a clear understanding of exactly whatphysiological processes drive stomatal regulation ofgas exchange and how they differ between plants ofdifferent drought tolerances (Meinzer, 1993).

Fax: +1-801-581-4668.E-mail address:[email protected] (J.S. Sperry)

There would be several benefits of knowing withgreater precision the adaptive significance of stom-atal closure induced by water stress. On an ecologicalscale, this knowledge would increase our understand-ing of vegetation patterns with respect to water avail-ability, and allow better predictions of how vegetationwill respond to environmental change. In agriculture,our ability to model and predict the response of cropsto water deficits would improve. Perhaps most signifi-cantly, knowing the most limiting processes for gas ex-change would allow us to progressively remove thoselimits through directed breeding. The result could bemore drought tolerant crops and less dependence onirrigation.

There are many physiological functions that couldbe driving the stomatal response to drought. Consid-erable attention has focused on cell physiology andbiochemistry. While cell growth in shoots can be verysensitive to water deficits, its cessation is not limitingfor gas exchange because it can cease at water poten-

0168-1923/00/$ see front matter 2000 Elsevier Science B.V. All rights reserved.PII: S0168-1923(00)00144-1

14 J.S. Sperry / Agricultural and Forest Meteorology 104 (2000) 1323

tials much higher than those triggering stomatal regu-lation of water loss (Hsiao, 1973). Enzyme activity isinfluenced by decreasing water potential and accom-panying increases in ion concentrations (Kramer andBoyer, 1995). However, water potentials that causestomatal closure in most species can have little effecton cellular respiration (Huang et al., 1975) whichargues against any fundamental interaction betweenenzyme function and the physiological range of waterpotentials. In many mesic and/or herbaceous species,stomatal regulation appears necessary to maintainleaf water potentials above the turgor loss point, andosmotic adjustment can translate into correspondingadjustment of stomatal regulation (Morgan, 1984).However, in desert and chaparral species with sclero-phyllous leaves, the association between turgor main-tenance and gas exchange is ambiguous (Saruwatariand Davis, 1989).

The potential resiliency of the plant cell in responseto extreme dehydration is evident from resurrectionplants whose cells can survive air drying (Gaff,1981). These plants are best represented among thenon-vascular, and more primitive vascular, plants.The same tolerance of desiccation is seen among thealgae, where some species can continue metabolismat water potentials that would kill a sunflower plant(Kramer and Boyer, 1995). It is curious that the evo-lution of higher vascular plants was associated withthe loss of the seemingly innate potential of lowerplants to survive desiccation (the exception being atthe seed stage of the life cycle). Perhaps new phys-iological processes associated with the evolution ofa larger and more complex plant body became morelimiting to gas exchange than those occurring withinindividual cells.

The vascular tissue itself represents a vitalwhole-plant process which is impaired by waterstress: the supply of water to the photosynthetictissue. The supply is needed to sustain the tran-spiration associated with carbon uptake throughthe stomata. As water deficits develop, events inplant and soil make it increasingly difficult to keepthe hydraulic pipeline between soil and leaf intact.The transport characteristics of this pipeline imposephysical limits on the rate at which water can besupplied to the leaves, and on the potential rate oftranspiration allowed by stomata (Tyree and Sperry,1989).

In this paper, I will consider to what extent the ne-cessity for vascular plants to maintain hydraulic con-tact with soil water constitutes a limiting process thatis protected by stomatal regulation of transpiration.These limits to water supply are independent of thedehydration limits of individual cells. It is tempting,but naive, to assume there will be a single processdriving stomatal regulation of water status. The intentof this paper is not to determine which processes aremost limiting to gas exchange, but to explain the limitsimposed by one function, water transport, so that ulti-mately its importance can be placed in proper context.

2. Premise

Much of what I will be considering follows from asimple premise: that the ability of the plant to supplywater to the leaves will correspond with the ability ofthe leaves to lose water. As water supply capabilitybecomes threatened, stomatal regulation will insurethat water use will not exceed supply. In physiologicalterms, this premise states that the hydraulic conduc-tance of the soilleaf continuum will be functionallylinked to stomatal conductance of the leaves.

I will consider some evidence for this premise, andsome hypotheses for how hydraulic and stomatal con-ductances are linked. Most space, however, will be de-voted to the implications of this premise for stomatalregulation.

3. Stomatal and hydraulic conductances

The capability of the water uptake and transport sys-tem can be quantified by its hydraulic conductance(k) which is the change in flow rate of liquid waterthrough the system per change in hydraulic pres-sure driving the flow. Hydraulic conductance is of-ten expressed per leaf area. As explained by thecohesiontension theory, the pressures driving bulkflow of water from soil to leaf are negative. They aregenerated by capillary forces arising in cell wall poresas water evaporates from the wall surface (Pickard,1981). The water pressure of the transpiration streamusually approximates its total water potential (9)because the xylem water is dilute enough to have anegligible osmotic potential.

J.S. Sperry / Agricultural and Forest Meteorology 104 (2000) 1323 15

Fig. 1. Stomatal conductance (a, c) and transpiration rate (b, d) vs. hydraulic conductance from bulk soil to leaf. (a, b) Tropical trees(from Meinzer et al., 1995); (c, d) water birch (Betula occidentalis) juveniles and adults (from Saliendra et al., 1995); dashed line in (d)represents an estimate ofEmax (Fig. 5, Eq. (2)) based on the cavitation response ofB. occidentalisstem xylem.

The potential for water loss from the leaves is quan-tified by leaf diffusive conductance (gl ) which is thechange in transpiration rate (E) per change in vaporpressure difference between leaf and air (1w). Leafconductance consists of stomatal conductance (gs) andboundary layer conductances in series. When bound-ary layer conductance and1w are constant,gs andEare proportional. Bothgs andE are usually expressedper leaf area.

A number of observations have demonstrated a cor-relation between the liquid phase conductance fromsoil-to-leaf (ksl ; per leaf area), andgs or E (Fig. 1,Meinzer and Grantz, 1990; Meinzer et al., 1995;Saliendra et al., 1995). The correlation results from anactive response of stomata toksl because whenksl isexperimentally changed there is an almost immediate

change ings. Whenksl per leaf area was increasedby partial defoliation or shading,gs of the untreatedfoliage increased. Whenksl was decreased by rootpruning or stem notching,gs decreased (Meinzer andGrantz, 1990; Sperry et al., 1993; Whitehead et al.,1996; Pataki et al., 1998).

The stomatal response toksl has the consequenceof moderating changes in leaf water status that other-wise would occur. For example, a 65% decrease inkslcaused by notching the stem xylem would have causeda corresponding decrease in leaf9 at steady-state con-ditions. However, in response to this treatment, stom-atal closure reducedE by 50% resulting in no changein bulk leaf 9 (Sperry et al., 1993). Near homeosta-sis in mid-day leaf9 was also observed as a result ofthe proportionality betweenksl andgs through plant


development (Meinzer et al., 1992; Saliendra et al.,1995).

What is the mechanism couplinggs to ksl? Onehypothesis is that as hydraulic conductances changeduring plant development, associated changes inxylem sap composition and concentration are sensedin the leaf and result in corresponding changes ings(Meinzer et al., 1991). It is not clear, however, howthis explains the very rapid (


Fig. 2. Hydraulic conductance (log scale) vs.9 soil in soybean. (a) Soil-to-root and root-to-leaf hydraulic conductances (from Blizzardand Boyer, 1980) and (b) root-to leaf data from Blizzard and Boyer (1980) compared with the loss of hydraulic conductance in soybeanshoot xylem from cavitation (Alder and Sperry, unpublished). Cavitation data was scaled relative to the mean well-watered conductanceobtained by Blizzard and Boyer (i.e. conductances at9 soil >0.2 MPa).

The transpiration stream also flows in extra-xylarypathways in the root and leaf where cavitation doesnot occur. Changes in root and leaf tissues during wa-ter stress can have important consequences for plantk. The root has been particularly well-studied in thisregard (Steudle, 1994). However, with few exceptions(Nobel and North, 1993), the changes extra-xylaryk across a wide range of9 encountered during adrought have not been well documented. Furthermore,the mechanisms responsible for these changes are notfully understood.

In contrast, the mechanism of cavitation is rela-tively well known. According to the air-seeding hy-pothesis (Zimmermann, 1983), cavitation occurs whenxylem pressures drop low enough to aspirate air intowater-filled conduits from neighboring air spaces. Theair seeding pressure depends on the magnitude of thecapillary forces holding airwater menisci in the con-duit wall pores. The smaller the pores, the greaterthe pressure difference required to pull air throughthe wall. A number of studies show strong supportfor the air-seeding hypothesis, and indicate that thesite of air-seeding is at the pit membrane pores ofinter-conduit pits (Crombie et al., 1985; Jarbeau et al.,1995; Pockman et al., 1995; Sperry et al., 1996).

The cavitation response has been measured in thexylem of several species. Typically the response is

measured as the loss ink of the xylem (kx) versusminimum9 of the xylem (Fig. 3). Species adapted towell-watered habitats such as riparianPopulusspecies,cavitate at much higher9 than species adapted to se-vere droughts, such asCeanothusspecies of the Cal-ifornia chaparral that must endure droughts of 68months and can develop xylem pressures approach-ing 10 MPa (Fig. 3). Species adapted to intermedi-ate drought, such as great basin sagebrush (Artemisiatridentatassp.wyomingensis) are intermediate in theircavitation response (Fig. 3). The variation in cavitationresistance is attributable to differences in air-seedingpressure (Sperry et al., 1996) which in turn is a func-tion of the pore sizes in inter-conduit pit membranes(Jarbeau et al., 1995).

5. Cavitation and the transpiration constraint

The extensive documentation of the cavitation re-sponse in plants allows direct analysis of how it limitstranspiration (E). According to Darcys law

E = ksl(19sl) (1)for steady-state conditions where19sl is the differ-ence in pressure between water in the soil (9s) andin the leaf xylem (9 l ; assuming negligible osmotic


Fig. 3. The percentage loss of hydraulic conductance in stem xylem vs.9 xylem in three species of contrasting drought tolerance.Data was obtained using a centrifugal force technique (Alder et al., 1997). The relatively drought-susceptible cottonwood was a hybridof Populus trichocarpaP. deltoides(Alder and Sperry, unpublished). Hoary leaf ceanothus (Ceanothus crassifolius) is a shrub of thecalifornia chaparral (Davis and Sperry, unpublished). Wyoming sagebrush (Artemisia tridentatassp. wyomingensis) is a small shrub ofthe intermountain west (Kolb and Sperry, 1999). Arrows on the upper9 axis indicate minimum xylem pressures measured in the fieldfor each species (HC: ceanothus, WS: sagebrush, CT: cottonwood; cottonwood pressure based on measurements ofPopulus fremontii;Pockman and Sperry, 2000).

effects). Ifksl is constant, there is no hydraulic limitto E as 19sl is increased at constant9s (Fig. 5,dashed line). However,ksl is not constant, but variesbecause of cavitation, soil drying, and changes innon-xylary tissues. Assuming that cavitation dom-inates the changes inksl with 9 (as implied byFig. 2), Eq. (1) can be re-written as

E = [ksl(9)](19sl) (2)where [ksl (9)] is determined by the cavitation re-sponse (Jones and Sutherland, 1991). In Eq. (2),Ecannot increase without limit as19sl is increasedbecause this requires progressively more negative9 which will cause progressively lowerk. There isa maximumE for Eq. (2) (Emax) which is associ-ated with a minimum critical9 (9CT; Fig. 5, solidline).

The 9CT corresponds to the9 required to cause100% cavitation. This is still the case even whenchanges in soil conductivity are incorporated inEq. (2) indicating that the xylem is more limitingthan the soil under most circumstances (Sperry et al.,1998).

Although the soilplant continuum has a maximumpossible flow rate corresponding toEmax, there is nophysical reason why the stomata could not allowE toexceedEmax. However, ifEmax is exceeded, the pos-itive feedback between decreasingk and9 becomesuncontrolled and so-called runaway or catastrophiccavitation causes a complete loss of hydraulic conduc-tance in the xylem (Tyree and Sperry, 1988). Whetheror not this limit matters to the plant depends on themargin of safety the plant exhibits relative to failureof xylem transport.

An estimate of the safety margin can be obtainedby comparing the9CT (9at 100% loss of xylem con-ductivity) with the actual minimum9 experienced.For 73 species, there is a significant correlation be-tween9CT and minimum9 (Fig. 4, solid line). Plantsthat are more drought tolerant (experience and sur-vive lower 9) are also more resistant to cavitation.The safety margin between minimum actual and pos-sible9 for species on the mesic-to-hydric end of thespectrum (minimum actual9>1.6 MPa) in Fig. 4 is1.040.46 MPa (n=13). In contrast, minimum pres-sures in the xeric plants can be several Megapascals


Fig. 4. Minimum possible9 xylem based on the cavitation response vs. minimum actual9 xylem based on field observations for 73species. Dashed line is 1:1 relationship. Safety margins from complete hydraulic failure are the y axis difference between data and the1:1 line. Species to the right of the arrow at1.60 MPa minimum actual pressure are on the mesic/hydric end of the drought tolerancescale and average a safety margin of 1.040.46 MPa (n=13). Species to the left of the arrow are progressively more xeric-adapted andtend to have larger safety margins (average=3.281.96 MPa;n=60; Sperry, 1995, Pockman and Sperry, 2000).

Fig. 5. Transpiration rate (=xylem flow rate at steady state) vs.9 xylem for constant9 soil. Dashed line is Eq. (1) with constant hydraulicconductance (k) in the soil-to-leaf pathway. Solid line is Eq. (2) with hydraulic conductance as a decreasing function of decreasing9[k(9)]. In this example, thek (9) function of xylem inB. occidentaliswas used (Sperry and Saliendra, 1994). Eq. (2) gives a maximumxylem flow rate (Emax) associated with a minimum xylem pressure (9CT). If stomata allowE to exceedEmax uncontrolled loss of hydraulicconductance will develop (runaway cavitation, Tyree and Sperry, 1988).


below those in the mesic plants. A mesic plant in axeric habitat would be unable to conduct water to itsleaves because its safety margin would be exceededand it would be completely cavitated. Cavitation lim-its the gas exchange potential of these mesic speciesduring water stress.

The foregoing observations suggest that hydrauliclimits do constrain transpiration, particularly underwater stressed conditions. The stomatal response ofa number of species conforms to this expectation,although in many studies9CT is not explicitly de-fined. Adjustments ofgs to developmental or experi-mental manipulations ofksl in sugarcane (Saccharumspp. hybrid),Betula occidentalis, andFraxinus excel-sior were sufficient to avoid loss of hydraulic conduc-tance from cavitation (Meinzer et al., 1992; Sperryet al., 1993). Fig. 1d shows the consistently smallsafety margin betweenE andEmax maintained byBe-tula occidentalisacross a range ofkrl . Significantly,in a few instances, stomatal response to experimen-tal reductions inksl of Betula occidentaliswere notfast enough to avoid catastrophic cavitation and shootsdied within hours (Sperry et al., 1993).

Stomatal responses to soil drought inBetula occi-dentalis, Acer grandidentatum, Picea abies, andQuer-cus petraeawere also consistent with the need tomaintain a safety margin from excessive cavitation(Cochard et al., 1995; Saliendra et al., 1995; Alderet al., 1996; Lu et al., 1996). In the case ofA. gran-didentatum, gs declined to near zero during a naturaldrought when9 reached9CT of the root xylem. Stemxylem was more resistant to cavitation and still main-tained a sizable safety margin from9CT (Alder et al.,1996).

In Betula occidentalis, the stomatal response to soildrought, like the response to changingksl , was me-diated via leaf9 as determined from experimentswhere shoot9 was increased by root pressurizing(Saliendra et al., 1995). The same leaf-level responsewas seen for stomata ofAlnus rubraandPsuedotsugamenziesii(Fuchs and Livingston, 1996). This sug-gests that the stomatal response to hydraulic conduc-tance, and to drying soil, can both occur via the sameleaf-level mechanism. Although there is evidence inother plants for stomatal responses to root water statusvia xylem-borne chemicals (Davies and Zhang, 1991),clearly this is not the only mechanism by which stom-atal responses to drought occur.

6. Controlled cavitation and plant water use

The9CT andEmax defined in the previous sectionrepresent theoretical limits that the plant cannot exceedwithout losing all hydraulic transport. However, as thecurvature of the solid line in Fig. 5 indicates, substan-tial cavitation can occur before9 reaches9CT. Thiscontrolled cavitation reducesksl but without trig-gering runaway cavitation. The extent of controlledcavitation that can occur at a given9s is dependenton the shape of thekx (9) function: a steep, thresh-old cavitation response allows little controlled cavi-tation whereas a gradual cavitation response allowsmore (Jones and Sutherland, 1991). Controlled cavi-tation explains much of the observed decline inkslin soybean plants during drought (Fig. 2).

During soil drought, a controlled decline inksl willamplify the effect of declining9s on9 l . This is clearfrom solving Eq. (1) for9 l :

9l = 9s Eksl

(3)

where (9s9 l ) is substituted for19sl in Eq. (1).At a typical midday9 l of 1.5 for9=0.2 MPa, theratio E/ksl will equal 1.3 MPa. If9s decreased by0.8 MPa during a drought and there was no change inE or ksl then the droughted9 l would be2.3 MPa.In contrast, if a 0.8 MPa decline in9s caused a50% decline inksl and E remained unchanged, thedroughted9 l would be3.4 MPa: much more neg-ative than if hydraulic conductance had remainedconstant. Changes in plant hydraulic conductance (asopposed to soil) would have the dominant amplifyingeffect as long as conductances were lower in plantthan in soil (Fig. 2).

In reality, the stomatal response to decliningksl(e.g. Fig. 1) prevents the potentially disproportionatedecline in9 l . What ends up being amplified by de-creasing hydraulic conductance is not the change in9 l , but the regulatory response of stomata to drought.Stomatal conductance must be decreased more toachieve the same9 l whenksl decreases than ifkslwere constant. The greater the decline inksl , themore sensitive is the stomatal response to drought.

A simple experiment demonstrates the significanceof changes in the plant component ofksl for the reduc-tion in gs during drought. When plants are droughtedand then rewatered,9s and the soil component of


ksl quickly approach pre-drought levels. However, acomparable recovery ings is often not seen. Excisinga leaf and supplying it with water, however, causedcomplete recovery ofgs in sunflower suggesting thatthe after-effect of drought in this case was vascularblockage rather than a biochemical effect at the stom-atal apparatus (Boyer, 1971). In a similar experimentwith sunflower, simulated root pressure after a droughtcaused an abrupt increase ings. The root pressure pro-moted refilling of vessels in the root system that werecavitated during the drought (Saliendra and Sperry,unpublished data).

These and other observations suggest that much ofthe stomatal closure observed during drought is a re-sult of the amplifying effects of decliningksl in theplant rather than a strictly proportional response todrying soil. There is some evidence that most of thedecline inksl occurs in the xylem of the root systembecause roots can be substantially more susceptibleto cavitation than shoots (Sperry and Saliendra, 1994;Saliendra et al., 1995). On rewatering, there is the po-tential for considerable hysteresis in the recovery ofksl to pre-drought values. Recovery would occur byrefilling of cavitated vessels by root pressure (Mil-burn and McLaughlin, 1974), and by growth of newroots.

While decliningksl is often considered to be dis-advantageous to the plant because it increases waterstress on the leaves, it may actually be advantageous.If reducedksl does substantially amplify the stom-atal regulation ofE during drought, the consequencewould be a more gradual use of soil water than ifksl were constant. This would potentially extendthe survivable drought period for the plant. Whilecompetition for water between species could erasethis advantage, there is a limit to how fast water canbe extracted from soil before an uncontrolled loss ofhydraulic conductance in the soilroot contact zoneoccurs (Cowan, 1965). Declines in plantksl couldhelp tune the plants water uptake rate to avoid ex-cessive declines in rhizospherek and in this way drawthe most water from the soil over the longest time.

7. Conclusion

The opening premise that a plants ability to losewater from the leaves during gas exchange will be

associated with its ability to supply leaves with waterleads to an explicit definition of hydraulic constraintson water use and gas exchange. The interaction be-tweenk and 9 resulting from xylem cavitation cre-ates unambiguous limits on the range of9 over whichgas exchange can occur (Fig. 3). Gross differences indrought tolerance between species correlate with thesehydraulic limits (Fig. 4). In many cases, safety mar-gins from hydraulic failure are small enough that theywould be exceeded in the absence of stomatal regula-tion of 9 andE (Fig. 1d).

While stomatal regulation avoids complete hy-draulic failure, substantial decreases in plantk canoccur during soil drought because of cavitation andother processes in the extra-xylary tissues (Fig. 2).Decreases in plantk have the effect of amplifyingthe water stress and increasing the sensitivity of thestomatal response to drought. Increased stomatalsensitivity could promote drought survival.

Although a basic framework exists for understand-ing the interactions between changes in plant hy-draulic capacity and plant responses to stress, moreneeds to be learned within this framework. The9dependence ofk in the extra-xylary tissues of rootand leaf are incompletely understood (Steudle, 1994).The cavitation response of root xylem may be es-pecially important, yet little work has been done onroot xylem. Stomatal sensing mechanisms are stilldebated both in terms of root versus shoot signals andin terms of the molecular mechanisms linking stressto changes ings. Modeling studies need to incorpo-rate reasonablek(9) functions for the plant to moreaccurately predict changes in water use under waterlimited circumstances. Models also need to test howchanges in plantk influence plant water use duringdrought.

Beyond the focus on hydraulic constraints, we needto know to what extent these constraints influence theoverall drought tolerance of plants. As emphasized inSection 1, many other processes may limit gas ex-change besides water supply to leaves. A reasonableway to assess the importance of hydraulic propertieswould be to compare them between crop cultivars withdemonstrated differences in drought tolerance. Littlework has been done on the cavitation response of cropplants, and in many cases there is as yet no physio-logical explanation of observed differences in droughttolerance between cultivars.


Acknowledgements

I wish to thank Gaylon Campbell and the AmericanSociety of Agronomy for the opportunity to partici-pate in this special issue of Agriculture and ForestryMeteorology. Work described was funded in part byGrants NSF-IBN-931980, and USDA-95-37100-1615to J.S. Sperry.

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