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Integrated Responses of Plants to Stress Author(s): F. Stuart Chapin, III Source: BioScience, Vol. 41, No. 1 (Jan., 1991), pp. 29-36 Published by: American Institute of Biological Sciences Stable URL: http://www.jstor.org/stable/1311538 Accessed: 05/03/2009 15:42 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/action/showPublisher?publisherCode=aibs. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit organization founded in 1995 to build trusted digital archives for scholarship. We work with the scholarly community to preserve their work and the materials they rely upon, and to build a common research platform that promotes the discovery and use of these resources. For more information about JSTOR, please contact [email protected].

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IntegratedResponses of to

Plants

Stress

A centralizedsystemof physiologicalresponses F. StuartChapinIII

both natural and agricultural communities,the environmentis seldom optimal for plant growth. Environmentalstress limits the overall productivityof US agricultureto 25% of its potential(Boyer1982). All mesic environmentsexperiencelarge seasonal fluctuations in light, moisture, temperature,and nutrients,often to levels that are suboptimalfor plant growth, so the plant is continuously encounteringnew combinations of environmentalstresses.Moreover, most natural environmentsare continuously suboptimalwith respectto one or more environmentalparameters, such as water or nutrientavailability. The nature of controls over plant growthin suboptimalenvironmentsis of particularinterest, because these are the only habitatsinto which agriculturecan expand in most developing countries, and impendingglobal climatechangewill alter the suitability of most terrestrial habitats for plant growth. Consequently,we need to understand the physiological mechanismsthat enableplantsto survive and reproduceundersuboptimal conditions. To date, most researchon the physiological responsesof plants to environmentalstress has focused on the responsesof plantsto specificstresses (Osmond et al. 1987). For example, In

All plants respond to stress of many types in basically the same way

plants adjust osmoticallyin response to salt and water stress (Morgan 1984), increasetheir potentialto absorb nutrientsin responseto nutrient stress (Lee 1982), and alterthe quantity and balance of photosynthetic enzymesin responseto shade or light stress (Evans1989). However,two linesof researchsuggest that plants also have a centralized system of stress response that enablesthem to respondto any physiological stress, regardlessof the nature of that stress. First, ecologists have noted that certainsuitesof traits characterize plants from all lowresource environments(e.g., deserts, tundra,shadedunderstory,and infertile soils). These traits include slow growth, low photosyntheticrate, and low capacityfor nutrientuptake(e.g., Chapin 1980, Grime 1977, Parsons 1968). Second, physiologists have observedthat individualplants respond to most environmental stresses by changingtheirhormonalbalance,frequentlyproducingmore abscisicacid and often less cytokinins(e.g., Chapin et al. 1988b). Recent research sugF. StuartChapin III is a professorin the gests that these hormonalchangesare Departmentof IntegrativeBiology, Uni- the triggerthat directlyelicitsreduced versityof California,Berkeley,CA 94720. growth in responseto environmental ? 1991 AmericanInstituteof Biological stress; low availabilityof a resource Sciences. simply activates this stress-response January 1991

system. The purpose of this article is to summarize and integrate these two lines of research and to propose that there is a basic physiological framework that regulates plant growth in response to environmental stress. This framework is complex, involving changes in hormonal balance, water relations, carbon balance, and nutrient use. Broad multidisciplinary approaches may now provide new insights into plant responses to environmental stress. This idea contrasts with the general trend in plant physiological research toward increasing biochemical detail of specific physiological processes. I emphasize the response of barley to nutrient stress as an example of the integrated nature of carbon, water, nutrient, and hormonal balances of plants.

Traits common to plants in low-resource environments The central feature of plants adapted to low-resource environments is that they grow slowly, even when provided with an optimal supply and balance of resources. This slow growth is seen in plants that are adapted to infertile soils (Chapin 1980, Clarkson 1985), dry or saline environments, or deep shade (Grime 1977, Parsons 1968). Associated with this slow growth is a low capacity to acquire certain resources. Plants from infertile soils have a low capacity to absorb phosphate (but not nitrogen; Bloom 1985) and to photosynthesize (Chapin 1980). Similarly, understory and many desert plants have an inherently low photosynthetic potential 29

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Plantsgrowingin stressedconditions.(a)Alaskantussocktundra,whichis limitedprimarily andnitrogen.(b)New by temperature Zealandtussockgrassland,whichis limitedprimarilyby phosphorus.(c) Californiachaparral, whichis limitedprimarilyby moisture.(d)California Thetwo grasscommunities havea similarstructure, pygmyforest,whichis limitedprimarily by nutrients. environmental stresses. despitethe factthattheyexperience quitedifferent

(Caldwell 1985, Sims and Pearcy 1989). There are at least three physiological mechanisms that could explain the slow growth of low-resource-adaptedplants. First, the slow growth even under optimal conditions may reflecta low capacityto capture resources.Plants from infertilesoils are often relatively inflexiblein root:shootratio and may allocateinsufficientbiomassto leaves underhigh-nutrientconditionsto acquire sufficient photosynthate to grow rapidly (Chapin et al. 1982). Moreover,as describedabove, plants from low-resourceenvironmentsoften have a low physiologicalcapacity to acquireresourcesper gram tissue. Second, plants from low-resource environmentsmay allocate fewer resourcesto growth becauseof propor30

tionally greater allocation to functions that improve survivorship in harsh environments (Mooney and Gulmon1982). Plantsgrow exponentially in weight as long as they allocate new biomass to organs, such as leaves and roots, that increase the plant's capacityto acquireresources. Plants that divert resourcesto functions other than growth (e.g., to defense or storage) will grow more slowly than individualsthat allocate functions. only to resource-acquiring Chemical defenses against pathogens and herbivoresare most strongly developedin species adaptedto lowresourceenvironmentssuch as infertile soils, deep shade, and drought (Bryantet al. 1983, Coley 1983). In these environments,plants are less able to acquireresourcesnecessaryto

replacetissueslost to herbivores(Bryant et al. 1983) and because a given amount of tissue loss represents a larger proportion of the productive capacity of the plant (Coley et al. 1985). Similarly,storageis well developed in perennialplants that occupy lowresourceenvironmentsboth as insurance against catastrophictissue loss and as a support for rapid growth duringbrief periodswhen conditions are favorable (Chapin et al. 1990). Annuals,which allocaterelativelyfew resourcesto storageor defense,show no consistent pattern of growth rate with respectto environment(Chapin et al. 1989). Thus there is good evidence that differencesin allocationto growth versus nongrowth functions explain why many perennial plants BioScienceVol. 41 No. 1

from harsh environments grow slowly. Third, plants from low-resource environments may grow slowly because of internally imposed constraints on growth. Perhaps these plants produce less of the growth hormones or are less sensitive to growth hormones. This possibility has, to my knowledge, not been explored. However, it seems reasonable, because plants from infertile soils maintain higher tissue nutrient concentrations than rapidly growing, high-nutrient-adapted plants under nutrient-limiting conditions (Chapin 1980, Chapin et al. 1982), suggesting that the low-resource plants are not growing to the absolute limit of their tissue nutrient supply. Similarly, shade plants maintain higher tissue carbohydrate concentrations under deep shade than do plants adapted to high light. Regardless of the mechanisms responsible for the slow growth of plants from low-resource environments, it is clear that these species share a common suite of physiological traits such as slow growth, low potential for resource capture, effective chemical defense, and a welldeveloped capacity for reserve storage. This observation implies a common physiological basis for slow growth, despite its evolution in response to quite different selective forces.

A centralized mechanism of stress response

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NUTRIENT UPTAKE AND MOBILIZATION. When deprived of external ni-

trogen supply, barley plants increase their potential to absorb nitrogen as measured per gram of root (Figure 1). This change is also observed in most other plants tested (Harrison and Helliwell 1979, Lee 1982). The increased absorption potential with nitrogen stress probably reflects a change in the quantity or activity of

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Figure 1. Nitrate absorptionrate (measuredunder standardconditions),root:shoot ratio, and nitrateand organicnitrogenconcentrationsof old leaves of barleygrown with 10 mM nitrate(filledcircles)and withoutnitrate(opencircles).Data are means? SE, expressed per gram fresh weight (Chapin et al. 1988a, 1988b). Significant differencesfrom controlat p < 0.05, 0.01, and 0.001 are indicatedby *, **, and ***, respectively. membrane of roots (Glass 1983). Plants also rapidly increase their proportional allocation to root growth in response to inadequate nutrient supply (Figure 1; Brouwer 1966). The

physiologicalmechanismby whichallocation is altered remains unclear. However, it is probably more complex than Brouwer's(1966) hypothesis that the organ closest to the

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Growth response to nutrients. A common perception is that plant response to insufficient nutrient supply involves physiological changes that are unique to nutrient stress. However, the nutritional response of plants exhibits many features that are similar to responses of plants to other environmental stresses.

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January 1991

31

idence is that the CO2 concentration inside the leaf tends to be high under conditions of insufficient nitrogen supply, indicating that stomates are relatively open and that photosyn0.2 -I.Or J-I thetic potential is the primarylimita* tion on photosynthetic rate (Evans -0 0 1983, von Caemmererand Farquhar Cl) 1981, but see Chapin et al. 1988b). I O.I1 2 -0.5On the otherhand, thereis a low rate E 0 of photosynthesisper unit of nitrogen :in plants with low tissue nitrogen concentrations,indicatingthat either O.oL 0.0 much of the nitrogen present in a +N -N low-nitrogen leaf is not involved in or that some other photosynthesis Figure3. Root hydraulicconductance,stomatalconductanceof old leaves,and water factor stomatal conductance) (e.g., of leaves of potential young barleyat the time (day3) thatgrowthbeginsto declineafter tends to limit photosynthesisunder removalof nitrogensupply (Chapinet al. 1988b). Statisticsas in Figure1. these conditions (Field and Mooney 1986). GROWTH. There are several lines of growth-limitingresource(rootsin the sumably because a low nitrogen supcase of nitrogenstress, shoots in the ply results in a low concentration of evidencesuggestingthat a low photocase of carbon stress)has first access photosynthetic enzymes, which in synthetic potential per gram of leaf to the growth-limitingresource.Hor- turn causes a low rate of photosyn- does not directly cause the slow mone balance is probably involved thesis per gram of leaf. However, growth of nitrogen-limited plants. (Joneset al. 1987). nitrogenstressalso causesa declinein First, plants whose growth is nitroA second major mechanism for stomatal conductance, which could gen-limitedalways have high concenmaintaininggrowthratein the face of also explain the decline in photosyn- trations of carbohydrates(Figure2; incipient nutrient deficiency is a with- thesis. In most plants, stomatal con- Brady1973, White 1973), suggesting drawalof tissue nitrogenstores, par- ductance and photosynthetic poten- that it is not the availabilityof photicularlyfrom old leaves. Barleyhas tial are so closely matchedthat both tosynthatethatdirectlyrestrictsgrowth high vacuolar nitrate concentrations parameterssimultaneouslylimit pho- underconditionsof nitrogenlimitation. (22%of total nitrogenin old leavesof tosyntheticrate (von Caemmererand Second, in barley and other species (Radinand Eidenbock1986), the deplants grown underoptimal nitrogen Farquhar1981). Photosyntheticpotential probably clinein leafgrowthratedueto nutrient supply). These tissue nitrate reserves are drawn down rapidlyin response drivesstomatalconductance.The ev- limitationpreceedsthe declinein total to inadequateexternal supply of niplantweightgain.Third,in barley,leaf trogen (Figure 1). However, the nigrowthdeclinesbeforethereis a major BARLEY (450+86) * tratestores are not largeenough,nor changein photosyntheticrateof young can they be mobilizedrapidlyenough leaves (i.e., those that provide most 80 - OLDLEAF / carbon to support continued shoot (60% of the total nitrate reservein two days),to meet the nitrogenneeds growth; Rawson et al. 1983). Thereof the plant growing at a maximal fore, to the extentthat nitrogeneffects rate for more than a few hours. 40on photosynthesisare important,they Therefore, organic nitrogen is also probablyact initiallythrougheffectson withdrawn from old leaves under leaf weight and quantityof photosyn** conditionsof nitrogenstress,presum- Cc thetictissue(a consequenceof changing I I fI U ably through breakdown of a wide growthand allocation)and on sourcesink interactions,which govern devariety of photosynthetic and non- 0 80- YOUNGLEAF mand for carbohydrate,rather than photosyntheticproteins(Evans1989) ** and through declines in rate of pro- 0() through direct effects on photosyntein synthesisunderconditionsof nitheticpotentialper gramof leaf. 0 40trogen stress (Cooke et al. 1979). Changes in plant-water relations Similar mobilization of nitrogen have been suggestedas the physiologstores to bufferplants from incipient ical mechanism by which nitrogen . --.> ._*.X0 limitation causes a reduction in nitrogenstress is found in most spe1 O I I cies studied (Chapin1980). growth (Radin 1983, Radin and K0 0 5 PHOTOSYNTHESIS. Photosynthetic 1982). Evenin hydroponicsysBoyer DURATION OF N STRESS (cd) rate correlatesclosely with leaf nitrotems, where water availability to gen content in barley and other spe- Figure4. Abscisic acid concentrationof plants is unlimited, nitrogen stress cies (Chapin et al. 1988b, Evans leaves of barley grown with (0) and quickly causes a decline in hydraulic 1989, Field and Mooney 1986), pre- without(@)nitrate(Chapinet al. 1988b). conductanceof roots (and therefore

HYDRAULIC STOMATAL WATER CONDUCTANCECONDUCTANCEPOTENTIAL

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BioScience Vol. 41 No. 1

water uptake) and an associated decline in stomatal conductance (and therefore transpirationalwater loss; Figure3). In some cases, particularly in plants grown under high irradiance,plant waterpotentialdeclinesin response to nitrogen stress because root hydraulic conductance is more sensitive to nitrogen stress than is stomatal conductance (Radin and Boyer 1982). In such situations, decreased turgor may be one mechanism by which leaf growth is inhibited. In other cases, the changes in water uptake and loss are in balance, with no net change in plant water potential(Figure3). Thus, although nitrogen stress causes substantialreductionin water uptakeand loss, the resultingchanges in tissue water relations are not necessarilythe directcause of the decline in leaf growth. Because at least two mechanismsallow nutrient stress to reduce growth rate, there is redundancy, ensuring that the plant will respond sensitively to its environment. The water relations of expanding cells, not the water relations of mature tissues (which most plant researchers, including myself, have measured),are importantin controlling growth (Boyer et al. 1985, Michelena and Boyer 1982). Nonetheless,patternsof water potentialin expanding cells often correlate with patternsin entireleavesor in adjacent matureleaveswhen plantsexposedto differentdegrees of water stress are compared (Barlow 1986). I cannot precludethe possibilitythat nitrogen stressreducesgrowthby reducingturgor of expanding cells, but current evidence suggests that there are also other mechanismsby which nitrogen stress reduces the rate of plant growth. HORMONAL BALANCE. Insufficient nitrogensupplyconsistentlyresultsin an increasein abscisic acid (ABA)in leaves (Figure4; e.g., Chapin et al. 1988b, Radin et al. 1982). The decline in stomatal conductancecaused by ABA (Schulze1986) could be part of the mechanismby which photosynthesis declines with nitrogen stress (Figures2, 3). ABAcontentof roots may decrease (Angelovaand Georgieva1983, Ansimov and Bulatova1982, Safarlievaet al. 1979), increase, or remain unJanuary 1991

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changed (Chapinet al. 1988a) in response to low nitrogen supply. ABA causes a large increase in hydraulic conductanceof roots (Chapin et al. 1988a, Ludewiget al. 1988), so any decreasein root ABA in response to nitrogen stress could explain the decline in root hydraulicconductancein nitrogen-stressedplants. A decline in leaf growth could reflect slower cell division or enlargement. Normally, cell enlargementis affectedearlierandto a greaterdegree by nitrogenstressthan is cell division (Milthorpeand Moorby 1974). A decline in cell enlargement, in turn, could reflecteithera changein turgor, a change in the resistanceof the cell wall to expansion (yield threshold), or a change in cell wall extensibility (Cleland 1986). ABA is known to reduce cell wall extensibility (Van Volkenburghand Davies 1983) and could explainthe observedchangesin leaf growth (QuarrieandJones 1977, Watts et al. 1981). Cytokinins also tend to decline under conditions of low nitrogen supply and could be involvedin controlsover cell division and expansion.

nism by which insufficientnitrogen supply leads to reducedgrowth (Figure 5). Insufficientnitrogen supply triggers a change in hormonal balance, including an increase in leaf ABA. The increase in leaf ABA reducescell wall extensibilityand therefore causes a decline in leaf elongation. Alternatively,in some plantsthe altered hormonal balance could reduce root hydraulicconductance,reduce turgor, and therebyreduceleaf growth. Regardlessof the mechanism by which it is achieved,the declinein growth reduces the demand of the plant for carbon, so carbohydrates accumulate and photosynthesis declinesto matchthe lower requirement of the plant for carbohydrate.The mechanismsby which photosynthesis declines probably include ABAinduced decline in stomatal conductance (Schulze 1986) and decline in concentrationsof photosyntheticenzymes (Evans1989). Thus the decline in leaf elongationand carbonrequirement probablylead to the decline in photosynthesis,ratherthan the other way around. Why should plants devise an elabTHE MECHANISM.I suggest the fol- orate hormonalmechanismto reduce lowing scenarioas a possible mecha- growth if direct nitrogen effects on 33

ENVIRONMENT

SOURCE

SINK

stressed plants, presumablybecause of a declinein nutrientdemand.Concentrations of photosynthetic enzymesdeclinein responseto drought, as does photosynthetic rate (Kluge LIGHT 1976). There are, however, two observations suggesting that this decline in photosynthesisis not directlyresponCO2 sible for drought-inducedgrowth declines. First, mild drought stress causes carbohydrate concentrations to increase (Hsiao et al. 1976). Second, the decline in leaf growth preceeds the decline in dry weight accumulation (Munns et al. 1982, WATER UPTAKE Wardlaw 1969). Together these obFLUX servations indicate that drought causes a reduction in growth most .....FEEDBACK directly by altering hormonal balFigure 6. The direct environmentalcontrols and source-sinkfeedbacks affecting ance, but that associated with this resourceacquisitionand growthby plants. decline in growth are interconnected changes in plant nutrition, carbon concentrationsof photosyntheticen- through a direct effect of turgor on balance,and water relations. zymes would eventuallydo the same cell enlargement. As with nutrient stress, water and Growth response to flooding stress. job? Perhapsthe rapid effects of incipientnitrogenstresson leaf elonga- salinity stress cause changes in virtu- As with nutrientstress and drought, tion (acting through altered turgor ally all physiological systems in the water-loggingcauses an increase in and/orcell wall extensibility)serveas plant. Potential of roots to absorb ABA that could be responsible for an early warningsystemthat enables nutrients generally declines in water- changes in growth (Wadman-van the plant to reduce growth and change patternsof allocation before thereis a severeimbalanceof carbonP-DEFICIENT P-SUFFICIENT and nitrogen-containingmetabolites. Day 12 Day 5 Day 12 By maintaining a balance between (a) Day 5 carbon and nitrogen reserves,plants 30minimizethe cost of growth (Bloom et al. 1985). ') I

20 -

Growthresponseto water stress.ReE cent studies suggest that water stress and osmotic stress cause a reduction 0E in growth throughbasicallythe same E mechanismimplicatedabove for nu0 K trient limitation. They cause a deC S G C S G C S G C SG crease in cytokinin transport from (b) in roots to shoots and/or an increase leaf ABA; these changes in hormone 30r C=Control I balance cause changes in cell wall L=Leaves Removed extensibility and therefore growth z 20 (Blackmanand Davies 1985). In exC C LLI C root chamwhere periments pressure U) bers or split-rootsystemsare used to 0 10 maintain a constant leaf turgor, 0 a in leaf drought still causes decline growth (Blackmanand Davies 1985, CL oL Matthewset al. 1984, Michelenaand C L C L C L C L Boyer 1982, Schulze 1986, Termaat et al. 1985; but see Neumann et al. TREATMENT 1988). Thus droughtcauses a reduction in leaf growth through a hor- Figure7. Photosyntheticratein responseto phosphorusdeficiencyandmanipulationof monal signal from roots and not sink strength(Chapinand Wardlaw1988). Statisticsas in Figure1. 34

BioScienceVol. 41 No. 1

Schravendijk and van Andel 1985). As with other stresses, growth is inhibited at the same time that ABA increases but before there are detectable changes in water or nutrient status of plants. After the reduction in growth rate, there are decreases in potential to absorb nutrients, concentrations of photosynthetic enzymes, rate of photosynthesis, root hydraulic conductance, tissue water potential, and turgor (Wadman-van Schravendijk and van Andel 1985). These observations suggest a syndrome of physiological responses quite similar to that described for plant responses to other stresses.

Physiologicalintegration A single common mechanism by which plants respond to diverse environmental stresses may explain how stress reduces plant growth, but it does not explain how plants reduce their rate of acquisition of other nonlimiting resources to maintain a reasonable balance of internal resources. Theoretical arguments based on economic analogies suggest that plants minimize the cost of growth if allocation is adjusted such that all resources are equally limiting to growth (Bloom et al. 1985). In other words, under conditions of nutrient limitation, plants should restrict carbon gain, and under low-light conditions plants should restrict nutrient uptake (Figure 6). Consequently, for resources that do not directly limit growth, the plant demand for resources (sink strength) should be more important than resource availability in the environment in determining the rate of resource acquisition (source activity). Nitrogen limitation of plant growth provides support for this hypothesis. Under conditions of high nitrogen availability,plants have a low potential to absorb nitrogen (Figure1) and a low allocation to roots (Figure 3). Under these circumstances, nitrogen demand by the plant has more effect on nitrogen uptake than does nitrogen availability in the soil (Clarkson 1985). By contrast, when growth is nitrogen-limited, nitrogen uptake is controlled by the rate of supply from the soil. Under conditions of low nitrogen availability, there is a decline in leaf allocation, photosynthesis (Figure 3), and water uptake (Figure 4), due to decreased January 1991

demandby the plant. Similarpatterns are observed in most other studies (Chapin1980, Clarkson1985). However, plants do not compensateperfectly. Nitrogen-limitedplants have high carbohydratestatus (Figure3), and light-limitedplants have high tissue-nitrogen concentrations (Evans 1989). Onlyexperimentscanprovidea true test of the hypothesisthat source-sink interactions control acquisition of nonlimiting resources. Experiments with the flag leaf (a well-defined sourceof carbon)and the developing grains(a well-definedsink for carbon) of barley provide one such test. The photosynthetic rate of phosphatedeficientbarley plants was increased by manipulationsthat increasedplant demandfor carbohydrates(shadingof the ear or removal of other leaves; Figure7). Similarly,small flag leaves (i.e., those having large sinks relative to their own size) had high rates of photosynthesis(Chapinand Wardlaw 1988); this relationshipwas most pronounced under conditions of phosphate deficiency. In other words, source-sink interactions controlled photosynthesis most strongly under conditions. nutrient-limiting

Conclusions The resultsdescribedsuggest that all plants respond to environmental stress in basically the same way: througha declinein growth rate and in the rate of acquisition of all resources. These same traits are observed in species that have adapted evolutionarilyto low-resource environments and in any plant that has adjustedphysiologicallyto a low resource supply. It appearsthat plantsexhibit a centralizedsystemof stressresponsethat can be triggeredby a diverserangeof stresses. This centralized stress response system is hormonally mediated but involves integratedchanges in nutrient,water, carbon, and hormonal balances of plants. Further studies of these stress responses should considerthe integratednature of these differentsystemsratherthan focusing on a single environmental resource.This integrationwill require a broad interdisciplinaryapproach that drawson the skillsof manytypes of physiologists and ecologists.

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