Abiotic Stress Signalling Pathways_cross-talk

TRENDS in Plant Science Vol.6 No.6 June 2001262 Review

http://plants.trends.com 1360-1385/01/$ see front matter 2001 Elsevier Science Ltd. All rights reserved. PII: S1360-1385(01)01946-X

Heather Knight*Marc R. KnightDept Plant Sciences,University of Oxford,Oxford, UK OX1 3RB.*e-mail:[email protected]

Plants encounter a wide range of environmentalinsults during a typical life cycle and have evolvedmechanisms by which to increase their tolerance ofthese through both physical adaptations andinteractive molecular and cellular changes that beginafter the onset of stress. The first step in switching onsuch molecular responses is to perceive the stress as itoccurs and to relay information about it through asignal transduction pathway. These pathwayseventually lead to physiological changes, such asguard cell closure, or to the expression of genes andresultant modification of molecular and cellularprocesses. Our knowledge about the signallingpathways leading from stimulus to end response inplants has increased over recent years. It isincreasingly apparent that the linear pathways thatwe have been studying are actually only part of amore complex signalling network and that there ismuch overlap between its branches, with, forinstance, many genes inducible by more than oneparticular stimulus.

In this article, we discuss two aspects of theseabiotic stress signalling networks, namely cross-talkand specificity. We define cross-talkas any instanceof two signalling pathways from different stressorsthat converge. This might take the form of differentpathways achieving the same end or of pathwaysinteracting and affecting each others outcome,including the flux through one pathway affectinganother. These might act in an additive or negativelyregulatory way, or might compete for a target (Fig. 1).We define specificity as any part of a signallingpathway that enables distinction between two ormore possible outcomes and that thus might link aparticular stimulus to a particular end response andnot to any other end responses. Opportunities for bothcross-talk and specificity can occur within aparticular pathway.

Cross-talkWhen stress signalling pathways are examined in thelaboratory, they are usually considered in isolationfrom other stresses to simplify interpretation. In

nature, however, the plant encounters stresscombinations concurrently or separated temporallyand must present an integrated response to them. Inthe case of phytochrome signalling, the two pathwaysleading to red-light-induced CHS and CAB geneexpression negatively regulate flux through oneanother1,2. Seemingly separate abiotic stress signallingpathways are also likely to interact in a similarmanner. In addition, several abiotic stress pathwaysshare common elements that are potential nodes forcross-talk. Cross-talk can also occur between pathwaysin different organs of the plant when a systemic signalsuch as hydrogen peroxide moves from a stimulatedcell into another tissue to elicit a response3.

SpecificityIn spite of considerable overlap between many abioticstress signalling pathways, there might, in someinstances, be a benefit to producing specific, inducibleand appropriate responses that result in a specificchange suited to the particular stress conditionsencountered. One advantage would be to avoid thehigh energy cost of producing stress-toleranceproteins, exemplified by the dwarf phenotype ofplants constitutively overexpressing the frosttolerance protein DREB1A (Ref. 4). In some cases, thesignal transduction pathways triggered by differentstresses are common to more than one stress type.One possible reason for this is that, under certainconditions, the two stresses cannot be distinguishedfrom one another. Alternatively, each stress mightrequire the same protective action (or at least somecommon elements). The discovery of separate sensingmechanisms for each stress would invalidate the firstsuggestion but the second is true in several cases. Forexample, dehydration protection is required in plantsundergoing either freezing or drought and theproduction of antioxidants and scavenging enzymes(e.g. catalase and peroxidases) that protect againstoxidative damage affords protection against a varietyof different abiotic (and biological) stresses5.

Most abiotic stresses tested have been shown toelicit rises in cytosolic free calcium levels ([Ca2+]cyt)and to involve protein phosphatases and kinases[including mitogen-activated protein kinase (MAPK)cascades]. However, are any of these componentstruly specific to one stress and which of them arenodesat which cross-talk occurs? In the followingsections, we consider different classes of signallingcomponent in turn, and examine their potential

Plants exhibit a variety of responses to abiotic stresses that enable them totolerate and survive adverse conditions. As we learn more about the signallingpathways leading to these responses, it is becoming clear that they constitutea network that is interconnected at many levels. In this article, we discuss thecross-talk between different signalling pathways and question whether thereare any truly specific abiotic stress signalling responses.

Abiotic stress signalling pathways:specificity and cross-talkHeather Knight and Marc R. Knight

TRENDS in Plant Science Vol.6 No.6 June 2001

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263Review

contribution to specificity and cross-talk betweenabiotic stress signalling pathways.

Sensing systemsSpecificity might occur at the point of initial stressperception itself. In the case of osmotic stress, theputative osmosensor AtHK1 (Ref. 6), a transmembranehistidine kinase, is thought to be the first component torelay changes in osmotic potential outside the cell to thetransduction pathway(s) inside the cell that regulatesdrought-inducible gene expression. If specific stressesare actually sensed by dedicated receptor molecules,

these molecules themselves have the potential toencode specificity of response. An early event in theresponse to many different environmental stresses is anelevation in [Ca2+]cyt (Refs 7,8), which is thought to bethe primary stimulus-sensing event for several stresses(e.g. cold)911. If this is the case then mechanisms couldexist for encoding the information that relates to theparticular stress through the calcium signature (seebelow). Alternatively, the stress might be sensedthrough other components either in parallel to orupstream of Ca2+ in the pathway. It has been postulatedthat cold is sensed via changes in membrane fluidity12

and cytoskeletal reorganization13 affecting calciumchannels.

CalciumThe precise kinetics, magnitude and cellular source ofstimulus-induced [Ca2+]cyt elevations (the calciumsignature) have been proposed to encode informationabout the particular stimulus, and to determine thespecific end response elicited14. Biphasic elevations,responses lasting from two seconds to tens of minutesand repeated oscillations are among the responsesobserved after abiotic stress.

Studies using animal cells showed that theCa2+-induced activation of particular transcriptionfactors could be specified by the magnitude andkinetics of an artificially induced [Ca2+]cyt elevation

15.This suggests that cells can decode specificinformation in the [Ca2+]cyt elevation that refers toparticular stimuli, and relate this to an appropriatechange in response. However, such data do not provethat this system of encoding specificity is actuallyused by cells. Also, these measurements were allmade on populations of cells, obscuring thecomplexity of individual cell responses.

In plants, the principle of specificity through calciumsignatures has been difficult to show because ofproblems in generating artificial [Ca2+]cyt elevations tomeet specific designs. In some cases, [Ca2+]cyt has beensuccessfully elevated in the absence of an abiotic stressby using a Ca2+ ionophore or Ca2+ channel agonists16,17.The correlation of such [Ca2+]cyt elevations with changesin the end responses usually associated with exposureto the stress shows a requirement for Ca2+ in thetransduction of these stimuli. However, it also supportsthe argument that specificity is not encoded through thecalcium signature because it is most unlikely that theartificial [Ca2+]cyt elevations could have the samesubcellular source and calcium signature as thosenormally provoked by that particular stress. It is morelikely that the [Ca2+]cyt elevation must achieve aminimum (and perhaps maximum) threshold peakvalue or total elevation (magnitude time). Ozoneexposure elicits a brief [Ca2+]cyt peak followed by a moreprolonged elevation18. Only the second of these isnecessary for the induction of GST gene expression andso, even though these data might imply the significanceof the calcium signature, they might also imply that themagnitude timehypothesis is true.

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TRENDS in Plant Science

Fig. 1. Cross-talk in signalling pathways. (a) Two different stimuli (1 and 2) evoke the same endresponse via different signalling pathways, using different signalling intermediates (AD and WZ,respectively). (b) Positive and negative reciprocal control. Two different stimuli (A and B) activate twosignalling pathways (broken arrows), leading to different end responses. (i) Pathways operatingtotally independently of each other. (ii) Flux through the stimulus-A-mediated pathway negativelyregulates the stimulus-B-mediated pathway and inhibits its flux. An example of this is inphytochrome-mediated expression of a chlorophyll a/b binding protein gene (CAB) and a chalconesynthase gene (CHS) by independent pathways, each negatively regulating the other. (iii) Fluxthrough the stimulus-A-mediated pathway positively regulates the stimulus-B-mediated pathway andpromotes its flux. (c) (i) Signalling pathway leading from a stimulus (stimulus 1) using a specificsignalling component (green) to effect response X. (ii) Stimulus 2 uses this same signallingcomponent to mediate its end response (response Y) and, by out-competing the stimulus-1 pathway,inhibits it. Calcium is an example of this: one stimulus might exhaust a specific pool of calcium andmake it unavailable for use by another stimulus.



264 Review

In stomatal guard cells, variation in the timing ofstimulus-induced Ca2+ oscillations has beencorrelated with the intensity of both the stimulus andthe resultant end response, with alterations in thesignature associated with loss of aperture closure14,19.External Ca2+ or oxidative stress elicited Ca2+

oscillations followed by stomatal closure in the wildtype, but cells of the det3 Arabidopsis mutant (whichhas impaired endomembrane energization) failed toshow normal wild-type oscillations and did not close.However, det3 cells responded normally to cold andabscisic acid (ABA) stimulation, indicating that thereare specific Ca2+-dependent pathways for differentstresses. Concurrent addition of external Ca2+ andrepeated depolarization of the plasma membraneinduced artificial Ca2+ oscillations in det3 cells andinitiated stomatal closure. These data suggest thatCa2+ oscillations are required for stomatal closure tooccur in response to certain signals. Interestingly, thenon-oscillatory stimulus-induced [Ca2+]cyt elevationsseen in det3 mutants constituted a larger overall totalincrease in [Ca2+]cyt than did the wild-typeoscillations. This might support the idea that theresponse is not achieved if the total [Ca2+]cyt elevationexceeds a certain level15. It should also be borne inmind that the det3 [Ca2+]cyt elevation might occur inthe wrong cellular location. Various plant abioticstress [Ca2+]cyt responses use Ca

2+ from differentsubcellular sources, including the extracellularcompartment, vacuole20 and mitochondria21. The Ca2+

signature reflects the source used22 and might encodeinformation of specific relevance to the cellularmachinery based in those organelles.

It is possible that effectiveCa2+ signatures onlyoccur in those cell types that are required to respond.[Ca2+]cyt elevations occur globally in plantsresponding to cold but only in the root after drought22

(S. Scrase-Field and M.R. Knight, unpublished).Within the Arabidopsis root, the [Ca2+]cyt responses ofepidermal, endodermal, pericycle and cortex cellsdiffer from each other when challenged with cold,drought and salt23. These tissue-specific differencesmight correlate with different stress proteinproduction or other responses.

Although plants exhibit recognizable [Ca2+]cytelevations in response to particular stresses, theseare altered markedly after previous stressexperiences8,24, indicating cross-talk between abioticstress signal transduction pathways occurring at thelevel of Ca2+. Whereas an oxidative stress encounterabolished future responses to drought stimulus inArabidopsis24, it increased the sensitivity of responseto low temperature levels8. Drought pretreatmentincreased the magnitude of subsequent drought-induced [Ca2+]cyt transients and increased the level of drought-inducible Ca2+-regulated gene expressionand stress tolerance24. In summary, the Ca2+ signal is ubiquitous in abiotic stress signalling and it istherefore an important node at which cross-talk can occur.

Calcium-regulated proteins[Ca2+]cyt elevations achieve control of variousprocesses via Ca2+-regulated effector proteins.Sometimes referred to as calcium sensors, theseinclude calmodulin, calcium-dependent proteinkinases (CDPKs) and calcium-regulatedphosphatases. Calmodulin has been implicated inplant responses to cold25, mechanical stimulation25,26

and oxidative stress27. The use of different isoformscould be involved in control of specificity betweenthese pathways, as has been observed withcalmodulin isoforms in specificity to biotic stressessuch as salicylic-acid-mediated defence responses28.In animal cells, anchoring proteins located indifferent parts of the cell compartmentalize kinases totheir site of action29. It is possible that specificity ofresponse in plant systems, too, is introduced bylocalizing calcium sensors in this way.

Only two out of eight Arabidopsis CDPK isoformsintroduced into maize protoplasts induced expressionof a specific stress-inducible gene, suggesting thatthere are specific CDPK isoforms for different stresssignalling pathways17. However, these experimentsinvolved the overexpression of constitutive versions ofCDPK isoforms, which, lacking all but the kinasedomains of the proteins, might not targetappropriately. Also, because they are ectopicallyexpressed, they might phosphorylate illegitimatesubstrates. Therefore, these results might not reflectthe in vivo situation in Arabidopsis. There are manydifferent CDPKs in Arabidopsis [~40 (Ref. 30)],therefore there is ample scope for partitioning ofspecific CDPK function between isoforms. The genesfor some isoforms are induced in response to specificstresses, implicating these CDPKs in particularsignalling pathways; thus, for example, AtCDPK1 andAtCDPK2 are implicated in salt and drought stresssignalling17,31. In rice, expression of OsCDPK7 at themRNA level is inducible by cold or salt stress32.However, overexpression of OsCDPK7 enhanced salt-and drought-induced, but not cold-induced, expressionof target genes, suggesting that the effect of this CDPKis specific to salt and drought signalling.

Another group of proteins identified as interactingwith Ca2+ to effect an end response includeserine/threonine phosphatases33 (PPases). The type-2CPPases include a group of proteins with similarities tothe calcium sensor protein calcineurin B (Refs 34,35)that are referred to in Arabidopsis as calcineurin-B-like (AtCBL) proteins. One of these, SOS3, is involvedspecifically in salt stress tolerance34 and the geneencoding another, AtCBL1 (but not those of otherfamily members), is highly upregulated by cold anddrought. Specificity through AtCBL isoforms mightresult from variation in the N-terminal sequence ofAtCBL proteins, meaning that only some membershave the potential to be targeted to membrane sites36.

As well as achieving specificity through the use ofdifferent isoforms, calcium sensors might also serve asnodes at which cross-talk can occur. [Ca2+]cyt elevations



265Review

elicited by a specific stress could regulate phosphatasesand kinases involved in the transduction of anotherstimulus. In alfalfa cells, cold-induced inactivation of protein phosphatase 2A (PP2A) is controlled by Ca2+ influx37, but it is conceivable that PP2A activitycould also be modulated via other stress-induced[Ca2+]cyt elevations.

The ABI1 and ABI2 proteins (identified throughthe abi1 and abi2 mutations) are homologous to type-2C PPases38,39 and have been implicated as negativeregulators in the early stages of ABA signaltransduction40,41. These proteins are potential nodesfor cross-talk between different signalling pathwaysinvolving ABA (e.g. cold and drought). Recently, atobacco homologue of the Arabidopsis PP2C genes hasbeen identified, NtPP2C1, transcript accumulation ofwhich is upregulated by drought treatment butinhibited by oxidative stress or heat42. If NtPP2C1functions as a negative regulator in a similar way toArabidopsisABI1 and ABI2, it is possible thatdownregulation of its expression by oxidative andheat stresses could increase cellular sensitivity toABA during drought treatment.

MAPK cascadesMAPK cascades are activated by numerous abioticstresses43 but they can introduce specificity into thesystem. AMAPK kinase kinase (MAPKKK)phosphorylates a MAPK kinase (MAPKK), which inturn phosphorylates a MAPK. Three major types ofMAPKKK have been identified in Arabidopsis: CTR1,ANP1-3 and the AtMEKK class. AtMEKK1 (Ref. 44) isexpressed in response to abiotic stresses including cold,drought and mechanical stimulation. Of six targetMAPKs, only two (AtMPK3 and AtMPK6) showedevidence of being phosphorylated in response to the

addition of a constitutively active ANP1 (via endogenousMAPKKs)45. Hydrogen peroxide (oxidative stress)increased the activation of MPK3 above the levelachieved with the constitutively active ANP1. Furtherexperiments showed that active ANP1 could activatehydrogen-peroxide-inducible promoters but notdrought- or cold- or ABA-responsive promoters, implyingprimary signal-specificity encoded within ANP1.

Reconstruction of the AtMEKK1 kinase cascade inyeast indicates that there is selectivity in the partnersthat associate with it. Using a combination of two-hybridand yeast mutant complementation, it was found thatAtMEKK1 preferentially associated with and activatedthe closely related MAPKKs, AtMKK2 and MEK1,which, in turn, associated with and activated the MAPKAtMPK4 (Refs46,47). Thus, specificity could be encodedby only allowing certain MAPKKKMAPKKMAPKcombinations in complexes, like chordsin a piece ofmusic (H.Hirt, pers. commun.). There is evidence ofcross-talk between these chordsduring abiotic stress,such as between MAPK cascades leading separately toATMPK4 and ATMPK6 (Ref. 48).

Transcription factorsLow positive temperatures increase the level offreezing tolerance in many plant species through coldacclimation49, but this state can also be achieved inresponse to drought or by application of thephytohormone ABA (Ref. 50). Many genes that areinduced by cold are also induced by drought or ABA(Ref. 51), probably because many cold-inducible genesencode proteins to protect the plant from theconsequences of freezing stress, which includedehydration. The gene RD29A (also known as LTI78or COR78) has been used in several studies examiningthe convergence of these pathways. RD29A is one ofmany cold- and drought-regulated genes that havebeen found to contain the so-called DRE or CRT(drought-responsive or C-repeat element) in theirpromoters52. In Arabidopsis, two groups oftranscription factors, DREB1 (also known as CBF)and DREB2, bind to this cis-acting element4,51,53. TheDREB1 and DREB2 genes encode structurallydifferent proteins and are induced specifically by lowtemperature and by salt or drought, respectively(Fig. 2). DREB2A and DREB2B are produced in theroot only in response to salinity, but are produced inthe stem and the root after drought treatment54,offering a further level of specificity of response.

Overproduction of either DREB1 or DREB2proteins in protoplasts increased expression of anartificial RD29A-promoter GUS fusion gene4,indicating that the DRE promoter element is a pointat which drought or salt and cold signal transductionpathways converge and that it can integrateinformation about these two stimuli (Fig. 2). It doesseem strange that two entirely separate signallingpathways lead to the action of these two sets oftranscription factors (Fig. 2) simply for them to resultin the activation of the same cis-acting element in the

1

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Fig. 2. The DREB1 and DREB2 transcription factors, key components in cross-talk between cold anddrought signalling in Arabidopsis. Cold and drought activate the expression of the DREB1 and DREB2families of drought-responsive-element-binding (DRE-binding) transcription factors, respectively.Both sets of transcription factors alight on the same cis-acting element in the promoters of genes suchas RD29A (also known as LTI78) called the DRE element. Therefore, the DRE element is an integrationpoint for cross-talk between cold and drought signalling in Arabidopsis. For simplicity, the abscisic-acid-responsive element is not shown on this diagram.



266 Review

same genes. It might well be that, in other species, theDREB1 and DREB2 factors control the expression oftwo different sets of genes and that Arabidopsis has,during evolution, rationalized these two functions.

An ABA-responsive promoter element (ABRE) hasbeen identified and a family of basic leucine zipper(bZIP) DNA-binding protein interact with it55,56. Genessuch as RD29A contain both DRE and ABRE elementsin their promoters and can be activated by ABA-dependent and ABA-independent pathways.AsingleABRE element cannot function independently56, forinstance, RD29B has two copies. RD29Ahas both anABRE and a DRE, suggesting that, in promoterscontaining both elements, the ABRE requires the DREfor ABA-induced expression. This suggestion issupported by data from the sfr6 cold acclimation mutant

of Arabidopsis57, which is deficient in the expression ofcold-regulated genes that contain a DRE element butexpresses non-DRE-regulated cold genes normally.Interestingly, in sfr6, DRE-containing genes also failedto be expressed fully in response to stimulation by ABA,suggesting that there is cross-talk between the ABREand DRE.

The interactions between these different pathwayshave been investigated in Arabidopsis through theanalysis of mutants defective in the induction of RD29Aby salt, cold, ABA or a combination of these58. TheHOS1 and HOS2 loci encode signalling componentsthat negatively regulate gene expression in responsespecifically to cold and not to other stress stimuli59,60.Conversely, HOS5 reduces expression in response toABA and osmotic stresses but not to cold61. Combinedcold and ABA or salt and ABA treatments have beenshown to have a synergistic effect on RD29ALUCexpression62, in contrast with the reduced levels ofexpression in response to combined cold and salttreatment. The results of these studies have suggestedthat ABA-dependent and ABA-independent osmoticand cold stress pathways might converge at severalhitherto unexpected points (Fig. 3). If they do, thisincreases opportunities for coordination between stresssignals and ABA in the regulation of gene expression.

PerspectivesStudying abiotic stress signalling pathways inisolation is valuable but it can be misleading becausethey form part of complex networks. In future, theonus will be on taking this fact into account, bothintellectually and in terms of technologydevelopment. A perfect example of this is theavailability of microarray technology. This enablesresearchers to examine the expression of not only alltheir particular stress-induced genes of interest butalso thousands of others, without prejudice andwithout extra effort63. This will lead to a greaterunderstanding of the effect that abiotic stresspathways have on each other as well as on pathwaysand processes that were not known to be connected.

The recent completion of the Arabidopsis genomeproject means that identifying the genes involved inspecificity and cross-talk will be more rapid. This willthen lead into work on the proteins themselves, to askhow exactly these proteins operate to encode specificityor to act as communicators or nodes in cross-talk.Finally, signalling components whose genes areinduced by abiotic stress, and hence implied in abioticstress signalling, can be directly tested for specificity orcross-talk (problems of redundancy aside) byphenotypic analysis of knockout mutants.

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Fig. 3. Cold, osmotic stress and abscisic acid (ABA) signal transduction, as determined by the use oflos, cos and hos mutants of Arabidopsis. The positions of HOS, COS and LOS gene products in thesignalling pathways are indicated by pale blue arrows. The abscisic acid (ABA)-dependent pathway(red) interacts and eventually converges with ABA-independent pathways (dark-blue and green) toactivate the expression of RD29A (also known as LTI78) and other genes containing the droughtresponsive and abscisic-acid-responsive promoter elements (DRE and ABRE) (black). Broken arrowsindicate pathways (or parts of pathways) that cannot directly induce the expression of these genes butthat require interaction with other pathways or branches of pathways. (Modified from Ref. 58.)

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