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Sensor types in signal transduction pathways in plant cells responding

to abiotic stressors: do they depend on stress intensity?

Alina Kacperska

Institute of Experimental Plant Biology, Warsaw University, Warsaw, PL 02-096, Polande-mail: [email protected]

Received 5 February 2004; revised 14 May 2004

Despite the fast growing knowledge about the components of

the signalling pathways involved in the activation of drought-,

cold-, osmotic stress- and salt-responsive genes, relatively little

is known about the sensor types responsible for the induction ofthe pathways. It is thought that different signals have their own

cognate receptors which independently, or in cooperation, initi-

ate a downstream signalling cascade (Xiong and Zhu 2002). On

the other hand, the stress level-dependent activation of differentreceptors has been proposed in plants responding to osmotic

stress (Munnik and Meijer 2001). The question arises as to

whether the activation of different signalling systems will dependon the nature of the sensors or on the stress-induced primary

event, which may differ in cells subjected to moderate or severe

stress. In this article, a discussion is given of the available

literature data concerning this controversial question. It is pro-posed that, in plants responding to mild stress, a disturbance of

water balance is the primary stress-induced event affecting the

cell wall–plasma membrane interactions, resulting in the activa-

tion of receptor-like kinases, including wall-associated kinases,

cytoskeleton-related mechanosensors, stretch-dependent ion

(calcium) channels and redox-mediated systems. The mildstress-sensing systems, assisted by an increased supply of absci-

sic acid, seem to be involved in the activation of the pathways

that enable the adjustment of plant growth and metabolism to

the stressful conditions, i.e. allowing acclimation. Severe orsuddenly acting stressors are sensed by membrane destabiliza-

tion (membrane depolarization, alterations in ion transport

systems), which results in the triggering of phospholipidsignalling. This may lead to the increased production of reactive

oxygen species, the accumulation of H2O2, lipid peroxidation

and increased synthesis of hormones such as jasmonates and

ethylene. These are characteristic features of the alarmsituation, which may result in irreversible injury and cell

death, or in cell recovery, depending on stress impact.

Introduction

Potentially adverse environmental conditions (stressors)affect plant growth and development and trigger a widerange of responses, from altered gene expression andmodifications in cellular metabolism to changes ingrowth rate and crop yields. Signalling pathways operat-ing in stress-affected cells and mutual interactionsbetween these pathways are the main research problemsin many laboratories. This has resulted in spectacular

progress in this area in the last few years. Combinedpromoter analysis with genetic screening of Arabidopsismutants with aberrant transcriptional responses to lowtemperature, osmotic stress and/or abscisic acid (ABA)application (Ishitani et al. 1997) and large-scaletranscriptional profiling have identified many genesthat are regulated by drought, salinity or extreme tem-peratures (Seki et al. 2003; Wang et al. 2003). These

PHYSIOLOGIA PLANTARUM 122: 159–168. 2004 doi: 10.1111/j.0031-9317.2004.00388.x

Printed inDenmark – all rights reserved Copyright#PhysiologiaPlantarum2004

Abbreviations – ABA, abscisic acid; ABF/AREB, ABA-inducible bZIP transcription factor; AGPs, arabinogalactan proteins; AOS, activeoxygen species; CBF/DREB, C-repeat/dehydration-responsive element binding factor; CDPK, calcium-dependent protein kinase; DAG,diacylglycerol; EEE, excess excitation energy; GPCR, G-protein-coupled receptor; HOG, high-osmolarity glycerol response; H2O2,hydrogen peroxide; IAA, indolile-3-acetic acid; IP3, inositol-1,4,5-trisphosphate; MAPKs, mitogen-activated protein kinases; MBO, myelicbasic protein; PA, phosphatidic acid; PAR, photosynthetically active radiation; PG, polyethylene glycol; PLC, phospholipase C; PLD,phospholipase D; PIP2, phosphatidylinositol-4,5-bisphosphate; PSII, photosystem II; PtdOH, phosphatidylalcohol; PUFA, polyunsaturatedfatty acids; RLKs, receptor-like kinases; ROS, reactive oxygen species; RWC, relative water content; SAM, S-adenosyl-methionine; SOSpathway, salt overly sensitive pathway; TCH, touch-activated gene; TRP, transient receptor potential channel proteins; UV, ultraviolet;WAKS, wall-associated kinases.

Physiol. Plant. 122, 2004 159

studies have allowed the identification of early and lateresponse genes and have revealed interactions betweenwounding, pathogen, abiotic stress and hormonalresponses (Cheong et al. 2002). Oxidative stress, arisingfrom an imbalance in the generation and removal ofreactive oxygen species (ROS), is likely to be involvedin plant responses to drought, low and high tempera-tures, excess excitation energy, ultraviolet (UV) irradi-ation and ozone (Desikan et al. 2001), and may constitutethe basis for the phenomenon of cross-tolerance, inwhich exposure to one stress can induce tolerance toother stresses (Pastori and Foyer 2002). To link theperception of a stress signal with the stress-induced modi-fications in gene expression, different models of stress-responsive transduction pathways have been proposed(e.g. Shinozaki and Yamaguchi-Shinozaki 1997; Zhu2002). Xiong et al. (2002) classed the components ofthe signal transduction network into three generalizedsignalling types. Type I signalling involves the generationof ROS scavenging enzymes and antioxidant compon-ents as well as osmolytes. Type II signalling involvesthe production of stress-responsive proteins (mostly ofundefined function). Cold, drought, salt stress and ABAcan activate the respective genes through the stress-inducible transcription factors, CBF/DREB and DREB2(C-repeat/dehydration-responsiveelementbindingfactors),or by the ABA-inducible bZIP transcription factorsABF/AREB. Type III signalling involves the salt overlysensitive (SOS) pathway, including the SOS3 family ofCa21 binding proteins, SOS2 protein kinase and the ion(Na/H) transporter SOS1.Despite the fast growing knowledge about the compon-

ents of the signalling pathways, such as the secondmessengers, phosphoprotein cascades and transcriptionfactors involved in the activation of drought-, cold- andsalt-responsive genes, relatively little is known about thesensor systems responsible for the induction of the path-ways. The stress level-dependent activation of differentreceptors has been proposed in plants responding toosmotic stress (Munnik and Meijer 2001). On the otherhand, it has been proposed that different signals havetheir own cognate receptors, which can operate independ-ently, or in cooperation, to initiate a downstream sig-nalling cascade (Xiong and Zhu 2002). Three systemshave been proposed to operate in membranes of cold-,drought- or salt-stressed cells (Xiong et al. 2002): calciumchannels (responsible for Ca21 fluxes), histidine kinaseand/or a two-component histidine kinase (initiating phos-phorylation cascades), and G-protein-coupled receptors(GPCRs) (involved in the activation of phospholipaseC). In sensing low temperature, changes in membranefluidity have been suggested to play a central role (Murataand Los 1997), and two groups of possible cold sensorshave been identified: membrane-associated kinase(s)and transient receptor potential channel proteins, TRP(Sung et al. 2003).In the majority of current studies on the identification

and description of signal transduction pathways in plantsresponding to a given stress factor, a sudden change in

the environment is applied to induce a response: plantsor cells are rapidly transferred from high to low tempera-ture, from medium or low to high osmotic potential,from low to high salt concentration, etc. No attentionhas been paid to the fact that there are importantdifferences in plant responses to slow or rapidly actingstressors (Minorsky 1989) and to mild or severe ones(Hernandez et al. 2001; Watkinson et al. 2003). Themeasures of stress are usually given as dehydration levelor period, salt or osmoticum concentration, range oftemperature, etc. Practically no information has beenprovided on the range of the stress-evoked functionalor structural perturbations within cells, although theirextent and speed of occurrence may be decisive factorsin the induction of the pathways allowing for growth andmetabolic adjustments, or resulting in alarm responseseventually leading to cell death.According to the dynamic concept of stress, the organ-

ism under stress passes through a succession of charac-teristic phases (reviewed by Larcher 1995). During thealarm phase, functional and structural disturbances areobserved. They may be overcome and will result inincreased stress resistance if the intensity of the stressoris not too high and allows for the initiation of the accli-mation processes (i.e. modification of metabolic path-ways, de novo synthesis of certain proteins andprotective substances). Very severe stress or very rapidimpairment will result in an acute collapse of cell integ-rity before the defensive processes can take place.Taking the above into consideration, it may be

expected that the stress-induced signal transductionpathways and their outcomes (i.e. increased stress avoid-ance and/or tolerance or induction of a cell death pro-gramme) will differ in cells responding to moderate orsevere stressors. The question arises as to whether theactivation of different signalling systems will depend onthe nature of the sensors or on the stress-induced pri-mary event, which may differ in cells subjected to mild orsevere stress. The main aim of this article is to discussthis question.

Recognition of stress severity

Experimental evidence that moderate and severe stres-sors are recognized by different elements of the signal-sensing system in plant cells has been provided by severalresearch groups. In studies on the sensing and signaltransduction of salt stress in alfalfa cells (Munnik et al.1999), a 46-kDa protein kinase (identified as SIMK, amember of the family of mitogen-activated proteinkinases, MAPKs) was found to be activated by a mod-erate (above 125mM) NaCl concentration. In contrast,at a high salt concentration (above 750mM NaCl), a38-kDa protein kinase, but not the 46-kDa one, becameactivated. The activation of different stress level-dependentreceptors was then proposed in the triggering of dis-tinct lipid and MAPK signalling pathways (Munnikand Meijer 2001). In chilling-sensitive rice seedlings,

160 Physiol. Plant. 122, 2004

an 18-kDa polypeptide was shown to accumulate inresponse to 5�C treatment, but was not induced at15�C (Koga et al. 1991). In addition, the induction oftranscripts of OsMEK1 (encoding a protein with fea-tures characteristic of mitogen-activated protein kinasekinase) was observed in the anthers, shoots and rootsof rice seedlings treated at 12�C, whereas no OsMEK1transcript accumulation was found in seedlings treatedat 4�C. In contrast, rice lip19, encoding a bZIP protein(possibly involved in low-temperature signal transduc-tion), was induced at 4�C but not at 12�C (Wen et al.2002). The authors also found that the activation of a43-kDa protein kinase, which preferentially uses myelicbasic protein (MBO) as a substrate, was observed in12�C-treated but not in 4�C-treated shoots. These find-ings suggest that there are two distinctive signallingpathways for the two temperature ranges used in thestudies, and imply the existence of distinct sensors formoderate and severe temperature stress (Wen et al.2002). Interestingly, the exposure of rice seedlings tomoderate (12�C) or severe (4�C) low-temperature treat-ment results in male sterility (due to the failure ofanther development) or plant death (due to disturb-ances in cellular water content and metabolism),respectively. Recently, microarray analysis of the tran-script profiles of loblolly pine rooted plantlets sub-jected to mild or severe drought showed that differentmembers of individual gene families responded differ-ently to water stress of low or high intensity (Watkinsonet al. 2003). In mild stress-affected plantlets, droughtacclimation responses were associated with an upregula-tion of genes encoding heat shock proteins, late embryo-genesis abundant proteins, enzymes from the aromaticacid and flavonoid biosynthetic pathways and enzymesfrom carbon metabolism. In plants affected by severestress, the switch from polyamine biosynthesis to ethylenebiosynthetic pathways was indicated by the downregula-tion of arginine decarboxylase and S-adenosyl-methionine(SAM) decarboxylase genes.

Stress-sensing systems in plants

Based on current literature data, it can be proposed thatthere are two groups of membrane-dependent stress-sensing systems in plant cells. Briefly, they may bedescribed as the redox/H2O2-dependent systems andthose dependent on perturbations in cell wall–plasmamembrane interactions.

Redox/H2O2-mediated signalling

The concept that redox signals are key regulators ofplant metabolism, morphology and development iswidely accepted (Pastori and Foyer 2002). Redox home-ostasis results from an appropriate intracellular balancebetween the generation and scavenging of ROS (alsoknown as active oxygen species, AOS), such as super-

oxide, hydrogen peroxide and hydroxyl radical. It hasbeen proposed that the accumulation of H2O2, togetherwith changes in the thiol-disulphide status of the cell,provides the redox signal leading to changes in geneexpression (Foyer et al. 1997). Accelerated productionof ROS has been observed in plants responding to bioticand abiotic stresses, such as pathogen challenge, droughtstress, ABA (synthesized following loss of turgor), osmo-tic shock, wounding, low and high temperatures, highlight intensity, UV-B radiation and ozone (Desikan et al.2001; Pastori and Foyer 2002). Hydrogen peroxide caneasily diffuse from the sites of production to other com-partments. Its flux and accumulation are monitored byascorbate and glutathione, together with the antioxidantenzymes. Information on the downstream elements ofthe H2O2-induced signalling cascade is rather scarce. Arole of H2O2 in the activation of a specific class ofMAPKs, as well as interactions of H2O2 with othersecondary messengers, such as Ca21, and with hor-mones, have been described (Pastori and Foyer 2002).Taking the above into consideration, the sites at which

stress-induced alterations in of the redox status of a celland the generation of H2O2 molecules take place arelikely sensors of the stressful situation.

Chloroplast and mitochondrion in stress sensingThere is strong experimental evidence that componentsof the electron transport chains in chloroplasts and mito-chondria play a major role in the modulation of ‘redoxhomeostasis’ in plant cells (Surpin et al. 2002; Dutilleulet al. 2003).In chloroplasts, stress factors induce imbalance

between the ‘light energy absorbed through photochem-istry vs. the energy utilized through metabolism’ (Huneret al. 1998). This is sensed through alterations in photo-system II (PSII) excitation pressure (or, in other termin-ology, excess excitation energy, EEE; Karpinski et al.1999), which reflects the relative reduction state of thephotosystem. It has been observed that prolonged expo-sure of Arabidopsis plants to the conditions that causeEEE and result in redox changes in the proximity of PSIIand in the formation of H2O2 in the stressed chloroplastsalso promotes redox changes and induces antioxidantmechanisms in unstressed chloroplasts (Karpinski et al.1999). The phenomenon is called ‘systemic acquiredacclimation’. Modulation of the chloroplast redox statusappears to coordinate photosynthesis-related geneexpression and to influence the expression of certainstress-inducible nuclear genes (Huner et al. 1998;Pfannschmidt et al. 2001; Surpin et al. 2002). Threepossibilities have been proposed to explain the relaymechanism from a redox signal to the nucleus (reviewedby Surpin et al. 2002): (1) H2O2 may diffuse out of alight-stressed plastid down a concentration gradient andactivate a cytosolic redox-sensitive regulator; (2) highlight conditions may increase the photorespiration rate,leading to increased H2O2 concentrations in peroxi-somes; then, a putative redox sensor in the peroxisomes


may transmit a signal via increased flux through theglycolate pool; and (3) an electron transport chain inchloroplast envelope membranes with cytosolic oxygenas the terminal acceptor may transmit a redox signal outof the chloroplasts. Whatever the redox relay mechan-ism, it may be assumed that the chloroplasts are involvedin the perception of a mild stress signal at the verybeginning of its action.The control of oxidant–antioxidant balance in a plant

cell and the stress resistance also depend on the stress-induced alterations in the mitochondrial electron transportchain (reviewed by Møller 2001). The mitochondrion-specific redox signals are proposed to be relayed to thenucleus by transducers and result in an increasedabundance of transcripts of antioxidative enzymes thatprocess ROS, generated both locally and in other com-partments (Dutilleul et al. 2003). This, in turn, decreasesthe accumulation of ROS in the cell and enhances stressresistance. In plants, the rates of H2O2 generation inmitochondria are much lower than those in chloroplastsand peroxisomes. However, they are increased by oxida-tive stress, i.e. by exogenous H2O2 which may diffusefrom other compartments. It has been observed thatamplification of H2O2 production leads to programmedcell death, characterized by cytochrome c release fromthe mitochondrion (Tiwari et al. 2002). In addition, ahigh-temperature (55�C) shock resulted in an immediateburst in H2O2 and superoxide anion production due tothe impairment in mitochondrial energy metabolism(Vacca et al. 2004). It seems, therefore, that the role ofmitochondria in the recognition of the stress signal dependson the stress severity. In plants responding to mild stress,they play a secondary role, being an important elementin the stress signal network. In cells affected by severestress, a high production of H2O2 by mitochondria, notcounteracted by antioxidant systems, may constitute asignal activating programmed cell death (Vacca et al. 2004).

Cell wall-associated H2O2 formationH2O2 is also produced in the cell wall by several pro-cesses, including the activation of plasma membrane-located NADPH oxidases and cell wall peroxidases(Pastori and Foyer 2002). The strong oxidative signalon the apoplastic face of the plasma membrane causesmodifications in ion fluxes and in the plasma membrane-based electron transport systems (Pastori and Foyer 2002).The elicitors of the oxidative burst and H2O2 formation inthe cell wall are generally thought to be pathogen-derivedmacromolecules which activate NADPH oxidasethrough phosphorylation by a calcium-activated proteinkinase (Mehdy 1994). However, activation of the systemhas also been observed in suspension cells stimulated toproduce H2O2 by mechanical stress induced by directmechanical pressure or by a change in osmotic pressurein the medium (Yahraus et al. 1995). A mechanicaltransducer, detecting cell wall–plasma membraneperturbations, has been proposed to be involved in the

initiation of the response. Therefore, activation of theredox-controlling systems at the cell wall–plasma mem-brane interface (see below) is likely to be involved inabiotic stress sensing.In view of the above statements, it seems that the role

of ROS and H2O2 in the mediation of stress responsesmay depend on the severity of the stressor. This impliesthat not the sensor type, but rather quantitative effectsof the sensor-initiated modifications in the oxidant–antioxidant activities in different cell compartments, maybe responsible for the different effects of a mild vs. a severestressor. The suggestion is in line with observations thatrelatively small increases or localized bursts of H2O2allow the general enhancement of stress tolerance,whereas large increases in H2O2 trigger local responsesthat inevitably lead to programmed cell death (Pastoriand Foyer 2002).

Sensor systems at the cell wall–plasma membrane interface

There is no doubt that, in plant cells, the cell wall, theplasma membrane and the cytoskeleton constitute astrongly integrated entity (reviewed by Baluska et al.2003). Therefore, stress-induced alterations in plasmamembrane physical properties, resulting in modifiedactivity of membrane-located proteins of diverse func-tions, are likely to be affected by the presence and pro-perties of the cell wall. This suggestion is furthersupported by observations that lower responsiveness ofstress-acclimated cells to a variety of stressors is asso-ciated with reinforcement of the cell wall (Marshall et al.1999; Stefanowska et al. 1999).Water deficit has been proposed to be a common

ground for a complex of plant cell reactions todifferent stress factors (Bohnert et al. 1995). As turgorpressure is responsible for plasma membrane appressionagainst the extracellular material, a stress-dependentdecrease in turgor will affect the cell wall–plasma mem-brane interactions. Therefore, such interactions aresound candidates for the sensing of a variety of abioticstressors. Indeed, expression of turgor-responsive geneshas been observed in pea shoots when the turgor pressureis reduced to near zero (Guerro et al. 1990). Theexpression of these genes varies with respect to stressseverity, as estimated by shoot ability to recover fromwilting.There are several classes of proteins that have been

proposed to define or regulate the cell wall–plasma mem-brane interface (Kohorn 2000); these include the ara-binogalactan proteins (AGPs), cellulose synthase andreceptor-like protein kinases. All of these proteins arebound to both the plasma membrane and the extracellu-lar carbohydrates (cellulose, hemicellulose and pectins).The involvement of AGPs and cellulose synthases instress-induced alterations in the cell wall–plasma mem-brane interactions will not be considered here, despitetheir importance for the modulation of cell wall proper-ties (Baluska et al. 2003).


Receptor-like kinases (RLKs)The wall-associated kinases (WAKs) represent a uniqueclass of receptor-like protein kinase. They are thought toserve a signalling function between the cell wall andcytoplasm (Baluska et al. 2003). Each of the five knownWAKs has a cytoplasmic Ser/Thr protein kinase domain,spans the plasma membrane and extends into the cellwall (Kohorn 2000). Thus, the WAKs physically linkthe plasma membrane to the carbohydrate matrix,mainly cell wall pectins. They are involved in theresponse to pathogens and increase in plant resistanceto otherwise lethal levels of salicylic acid (He et al. 1998).However, heat and salt stress has no effect on WAK1mRNA, and wounding produces a decline in its steadystate level. Therefore, the function of WAKs in abioticstress signalling still awaits experimental verification.There is a growing body of evidence suggesting that, in

plants, another class of RLKs, not covalently bound tothe cell wall but composed of an extracellular domain, atransmembrane domain and a cytosolic kinase domain,is involved in sensing water deficiency evoked by differ-ent abiotic stressors. Expression of the RPK1 gene,encoding a receptor-like protein kinase, the structuralfeatures of which suggest that it may be a Ser/Thr pro-tein kinase, was found to be rapidly induced by dehydra-tion, high salt (i.e. low water potential) and coldtreatments in Arabidopsis thaliana (Hong et al. 1997).RPK1 was also induced by exogenous ABA, but wasindependent of endogenous ABA. Recently, a possibleinvolvement of a two-component system, composed of asensory histidine kinase and a response regulator, inosmosensing in plants has been described (Urao et al.2000). The hybrid histidine kinase, ATHK1, cloned fromArabidopsis, has been shown to be inactivated inresponse to high salinity (Urao et al. 1999) which, inturn, resulted in activation of the high-osmolarity gly-cerol response 1 (HOG1) MAPK. In Arabidopsis, thetwo-component histidine kinases, ETR1 and its homo-logues, function as ethylene receptors and negative regu-lators in ethylene-mediated phosphorelays (Urao et al.2000). It has been proposed that the upregulation of theethylene receptors would protect plants against theethylene-dependent responses (after Urao et al. 1999).It is known that the burst of ethylene evolution isinduced by wounding and other stress factors, resultingin plasma membrane dysfunction (Kacperska 1997).Taking the above into consideration, itmaybe supposed

that different RLKs may be activated by stressors ofdifferent impact. Unfortunately, no information on thedegree of cell dehydration and/or the range of turgor pres-sure decrease needed for the induction of the RLKs andhistidine kinases is available. Neither is it known whetherdifferent threshold values of a stress are required for theinduction of differentRLKs. Interestingly, the existence ofa threshold temperature has been proposed for the induc-tion of accumulation of CBF transcripts in cold-sensingArabidopsis plants (Zarka et al. 2003). Despite the lack ofinformation on the stress impact required to activatedifferent RLKs, it is now clear that the activation of

RLK-dependent phosphorelays allows for the synthesisof proteins involved in the counteraction of the stress-induced negative effects, i.e. for plant acclimation.

MechanosensorsThe expression of a small subset of genes, called the TCH(touch-activated) genes (the products of which includecalmodulin, calmodulin-related proteins and a xyloglu-can endotransglycosylase; Braam et al. 1997), is upregu-lated by three classes of stimuli (Braam 2000): (1) stimulithat directly cause mechanical perturbation, such as touch,wind and wounding; (2) growth-promoting stimuli, suchas darkness and hormones (indolile-3-acetic acid IAAand brassinolide); and (3) temperature shifts. TCH geneshave also been shown to be upregulated by cold shocks(Polisensky and Braam 1996). On the other hand,mechanical agitation has been found to induce rapidaccumulation of transcripts for the CBF1, CBF2 andCBF3 proteins that bind to the low-temperature-responsive element, CCGAC, in cold-sensing cells (Zarkaet al. 2003). Interestingly, in theTHC4 promoter, a 102-bpregion sufficient to impart cold and touch responsivenesshas been discovered (after Zarka et al. 2003). Within thisregion, there is a 24-bp segment that is 66% identical insequence to the CBF2 promoter segment. Mechanosensi-tive signalling has also been suggested to be involved inthe perception of the osmotic stress signal (Xiong andZhu 2002). These observations indicate that differentstressors, which affect turgor and evoke transientstretching or compression of membranes and walls,may activate mechanotransduction pathways leading tothe expression of not only TCH but also other genes.At least two different kinds of sensor are thought to be

involved in the perception of mechanical forces (Braam2000): (1) compression or stretching of membranes andchanges in wall tension can be relayed to the cytoskele-ton by integrin-like molecules, which leads to intracellu-lar signals; and (2) mechanical stress can be transducedas calcium or other ion fluxes, dependent on the openingof membrane channels that are gated by membranestretching. Rapid fluctuations in cytosolic calcium havebeen demonstrated in plants subjected to mechanicalperturbations (Haley et al. 1995). The activity of amechanosensitive calcium-selective channel has alsobeen shown to increase in response to decreased tem-perature (Ding and Pickard 1993). In cold-sensing cells,rigidification of microdomains on the plasma membrane,resulting in the induction of stretch-sensitive channelsand increased Ca21 flux into the cytosol, has been pro-posed as a main cause of actin cytoskeleton rearrange-ments (Orvar et al. 2000). Therefore, it seems that thestress-dependent induction of mechano- and cold-signalling pathways depends mainly on modifications inthe functioning of stretch-dependent calcium channels inthe plasmamembrane. A similar suggestion has been madeto explain increased CBF transcription in Arabidopsisplants responding to cold and mechanical stresses (Zarkaet al. 2003).


Calcium channels in stress sensingAn elevation in cytosolic free calcium, [Ca21]cyt, due toopening of stretch-dependent or voltage-gated calciumchannels, is the secondary signal caused by many differ-ent environmental stresses (reviewed by Sanders et al.2002). Calcium channels open when cells respond to asignal and calcium enters the cytoplasm down its electro-chemical gradient from two pools: from the cell wall andfrom cell organelles (Knight 2000). The interplaybetween influx through channels and efflux by theATP- or proton motive force-driven pumps and carriersdetermines the form of a Ca21 spike that is potentiallyspecific to the sensor relays (calmodulin and calcineurinB-like proteins), or to sensor responders, such as Ca21-dependent protein kinase (CDPK) (Sanders et al. 2002).Recent studies on transgenic Arabidopsis plants haveshown that calcineurin B-like protein functions as apositive regulator of salt and drought responses and anegative regulator of cold responses in plants (Cheonget al. 2003).The involvement of the plasma membrane stretch-

dependent calcium channels in mechano- and cold-sensitive signalling pathways has been discussed above.The voltage-gated channels also appear to be involved instress sensing. Transient depolarization of membraneswas observed in cucumber roots subjected to a suddentemperature decrease, whereas no such response wasnoted in tissues exposed to a slow temperaturechange (Minorsky 1989). In winter oilseed rape leavestouched with ice crystals at different freezing tempera-tures, changes in membrane potential were associatedwith calcium fluxes (Piotrowska et al. 2000). A weakmechanical stimulus was found to induce membranehyperpolarization in root cells (Monshausen and Sievers1998). Membrane hyperpolarization is known to activateCa21 permeable channels in the plasma membrane (Gelliand Blumwald 1997). There is also experimental evidencethat osmotic stress affects plasma membrane electricalproperties (Lew 1996). As the direct modulation of tur-gor pressure did not affect the membrane potential, theauthor concluded that, in cells responding to osmoticstress, an ‘osmosensor’ rather than a ‘turgor sensor’regulates the cells’ response to osmotic stress. In thiscontext, it is worth noting that, in all experiments indi-cating stress-induced changes in membrane potential, arapid change in the environment was applied to induceresponses determined within several seconds. This maymean that alterations in membrane potential are evokedby a rapid stress action (shock), as suggested for chillingstress (Minorsky 1989).The membrane potential depends on H1-coupled ion

transport systems in plant cell plasma membranes. Arapid alkalinization of the extracellular medium withconcomitant efflux of K1 has been observed in osmoti-cally shocked tomato cells (Felix et al. 2000). The invol-vement of plasma membrane ATPase in responses ofonion bulb scales to freezing has been proven experimen-tally (Arora and Palta 1991). Therefore, the plasmamembrane H1-ATPase can be taken into consideration

as one of the primary sensors involved in the perceptionof stressors affecting plasma membrane and cell wallinteractions in plant cells. The enzyme has five extracel-lular loop-forming domains, the conformation of whichis likely to be modified by osmotic stress-induced alter-ations in plasma membrane appression against the extra-cellular material. The cold-induced rigidification ofmembrane domains is also a probable reason for alter-ations in ATPase activity.A number of calcium release channels reside in the

vacuolar membrane. Two are gated by voltage, and twoothers are ligand-gated by inositol-1,4,5-trisphosphate(IP3) or cyclic ADP-ribose (Sanders et al. 2002).Recently, hyperosmotic stress has been shown to inducerapid changes in the electrical properties of vacuoles inroot hairs of Arabidopsis (Lew 2004). In addition, stress-induced release of IP3 from the plasma membrane hasbeen indicated (see below). Detailed studies are needed todetermine whether the vacuolar membrane can be con-sidered as a primary or a secondary stress sensor.It is now clear that certain changes in cellular Ca21may

reflect perturbations in Ca21 homeostasis that do nothave any specific signalling function. Amongst othereffects, sustained calcium elevation in the cytoplasm hasbeen shown to activate phospholipases, including phos-pholipase D (PLD), which, in turn, results in the degrada-tion of phospholipids (e.g. Yoshida 1979). The increase incytosolic Ca21 above a threshold was proposed to be thereason for irreversible injury in frost-thawed onion bulbscales (Arora and Palta 1989). Therefore, it seems that thefinal result of calcium channel activation (transient cal-cium spikes or sustained high calcium concentration inthe cytoplasm) may depend on the effectiveness of theATPase- and/or Ca21/H1 antiport-dependent control ofion efflux (Sanders et al. 2002). From studies on Arabi-dopsis mutants, which displayed reduced tonoplast Ca21/H1 antiport (CAX1) activity, it appears that CAX1 par-ticipates in the development of the cold acclimationresponse (Catala et al. 2003).Summingup the observations on stress-induced calcium

fluxes, it may be hypothesized that the main differencebetween the sensing of a mild, acclimation-inductive or asevere, injury-causing stress depends on the effectivenessof the systems restoring [Ca21]cyt to resting levels, ratherthan on differentmodes of stress action in the activation ofstretch- or voltage-dependent calcium channels. Thisaspect of stress signalling requires detailed studies.

Phospholipid signallingIn stress signalling, membrane phospholipids constitute asystem that generates important signalling molecules,such as IP3, phosphatidic acid (PA) and diacylglycerol(DAG) (Zhu 2002).Transient IP3 signals, involved in the opening of calcium

channels in tonoplasts, are generated by the phospholipaseC (PLC)-mediated hydrolysis of phosphatidylinositol-4,5-bisphosphate (PIP2). The enzyme is activated by changes incytosolic calcium in response to osmotic stress-evoked


primary signalling events, such as perturbations inelectrical or mechanical properties of the membranes(Heilmann et al. 2000). Several studies have shown that,in various plant systems, the IP3 level rapidly increasesin response to hyperosmotic stress and exogenousABA (reviewed by Zhu 2002). The induction of IP3transients has also been observed in leaves showing atime-dependent decrease in tissue water potential to acertain threshold level in response to polyethylene glycol(PG), freezing treatments or ABA (Smolenska andKacperska 1996). It appeared that IP3 release by PLCmight depend on two types of stress sensor systems:those activated by stress-induced membrane destabiliza-tion and those dependent on the supply of ABA fromother tissues. Therefore, it seems that PLC-mediated IP3formation is the secondary rather than the primarystress-induced event.In recent years, PLD has been identified as an import-

ant signalling enzyme that produces water-soluble free-head groups (e.g. choline, ethanolamine) and PA(reviewed by Meijer and Munnik 2003). Apart frombeing involved in various regulatory processes (reviewedby Wang 1999), the enzyme has been shown to beinvolved in plant responses to wounding (e.g. Ryu andWang 1996; Wang et al. 2000), osmotic stress (Munnikand Meijer 2001), dehydration (Frank et al. 2000) andcold shock (Ruelland et al. 2002). Stimulation of plantPLD has also been shown in response to treatments withABA, light, fungal elicitors and bacterial pathogens(reviewed by Wang 1999). The association of a special-ized PLD, p90, with the plasma membrane and micro-tubules has been proposed to be involved in thereorganization of the cytoskeleton in response to envir-onmental stimuli (Gardiner et al. 2001)Wound activation of PLD appears to result from its

translocation to membranes, which is mediated by anincrease in cytoplasmic Ca21 on wounding (Ryu andWang 1996). Accordingly, a rise in [Ca21]cyt from anextracellular origin was found to be a necessary elementin the activation of PLC and PLD (Ruelland et al. 2002).Whether the stress-dependent activation of PLD involvesheterotrimeric G proteins (Frank et al. 2000) remains tobe elucidated in further studies. At present, it seems verylikely that changes in the cell wall–plasma membraneinteractions, leading to increased calcium fluxes fromcell walls, as shown above, may be the primary stresssignal, triggering PLD activation.PLD-generated PA has been proposed to be a general

stress signalling molecule (Munnik 2001). In addition, itmay serve as an effector or a substrate for the productionof other mediators, such as DAG, polyunsaturated fattyacids and jasmonic acid, in wound and defence reactions(Wang 1999). PA is also a potent activator of NADPHoxidase, which is involved in the production of ROS. Itsrole in mediating superoxide production in PLDa-depleted Arabidopsis leaves has been demonstratedrecently (Sang et al. 2001).On the other hand, it seems that, in stress sensing, not

only the hydrolytic but also the transphosphatidylation

activity of PLD ought to be taken into consideration.Transphosphatidylation occurs in vivo (Yang et al. 1967)and results in the formation of phosphatidylalcohol(PtdOH). In this context, it should be noted that, inmost studies on PA involvement in stress responses, thedetermination of PA content is based on the in vitroassay of PtdOH formation in the presence of butanolas a reporter alcohol (e.g. Munnik 2001). Obviously, themethod does not allow for the discrimination betweenthe in vivo displayed hydrolytic and transphosphatidyla-tion activities of the enzyme. However, in cells showingincipient frost-induced membrane destabilization and anincreased level of glycerol, the transphosphatidylationreaction was promoted in vivo and the role of PLD incell recovery from the stress-induced injury was proposed(Sikorska and Kacperska 1982). Recently, a two-steptransphosphatidylation reaction has been proposed tobe involved in the PLD-triggered reorganization ofmicrotubules (Dhonukshe et al. 2003).In view of the above observations, it is proposed that

not only the impact of the stressor, as suggested byMunnik and Meijer (2001) for osmotically stressedcells, but also the availability of endogenous alcoholmay be a decisive factor for the activation of distinctphospholipid (PA- or PtdOH-dependent?) signallingpathways. The suggestion is further supported by theobservation that, in yeast cells exposed to hyperosmolar-ity, HOG1 MAPK pathway-mediated glycerol produc-tion was increased (Xiong and Zhu 2002). In addition, anaccumulation of polyalcohols is frequently noted in planttissues subjected to different stressors, but the role ofthese compounds is usually related to plant osmoticadjustment. The role of hydrolytic and transphosphati-dylation PLD activities in the initiation of different stresssignalling pathways calls for further studies, especially asPLD may operate as an enzyme involved in membraneremodelling (Munnik and Meijer 2001). Experimentalevidence that the activation of distinct phospholipid-triggered pathways may lead to cell structure remodellingor to cell death has recently been provided by studies onphospholipase A2- and lipoxygenase-mediated reactions,which may result in cell proliferation or in apoptosis andnecrosis, depending on the range of membrane changes(Spiteller 2003).

Conclusions

A survey of the literature data on the sensor typesengaged in plant responses to various abiotic stressorsindicates that the activation of sensors may depend onthe primary stress-induced event, which is different incells responding to a mild and slow-acting stressor thanin those responding to a sudden and/or acute stressor(Fig. 1). In the presence of a mild and slow-acting stressor,a decrease in cellular water content (relative water con-tent, RWC) and/or an increased excitation pressure(EEE) in chloroplasts (due to a relative surplus of photo-synthetically active radiation, PAR) bring about: (1)


activation of the redox-sensing systems located in thechloroplasts and mitochondria, as well as at the interfacebetween the plasma membrane and cell wall; this maylead to relatively small increases in H2O2 level andincreased antioxidant capacity of the cell; (2) alterationsin the cell wall–plasma membrane interactions which, inturn, activate cell wall-associated or plasma membranereceptor-like kinases (including histidine kinases) andsome mechanosensors in the plasma membrane; modifi-cations of these interactions may also be involved in theopening of calcium channels in the plasma membraneand in an increased calcium influx from the apoplast;the effectiveness of calcium antiport systems in cellsresponding to a mild stress requires further study. Inplants subjected to a mild stress, increased synthesisand accumulation of ABA take place, the hormonebeing engaged in cell signalling during cold, droughtand salt stresses (Xiong et al. 2002). The signalling path-ways induced by a mild and slow-acting stressor lead tothe induction of ‘early response’ and ‘delayed response’genes (reviewed by Denekamp and Smeeken 2003)involved in the control of cellular metabolism, allowingthe adjustment of plant growth and metabolism to thestressful conditions, i.e. plant acclimation.Severe or suddenly acting stressors are sensed by mem-

brane destabilization (membrane depolarization, alter-ations in ion transport systems), which results in increasedand often sustained calcium concentration in the cytosol.The stress-induced alterations in the calcium antiportsystems in severely stress-affected cells can be predicted(the problem requires further study). As a result of mem-brane destabilization, phospholipid signalling is put intooperation and may lead to increased production of ROS,

accumulation of H2O2 and lipid peroxidation, as well asto increased synthesis of hormones such as jasmonatesand ethylene (Wang 1999; Wang et al. 2000). As a con-sequence of these responses, defence pathways are acti-vated. This is the alarm situation, which may lead toirreversible injury and cell death or to cell recovery,depending on the impact of the stressor and, possibly,on the availability of a substrate for PLD transphospha-tidylation activity. The phospholipid-generated productsmay represent biological signals which do not require thepreceding activation of genes and do not need interac-tions with specific receptors, as recently proposed forlipid peroxidation products (Spiteller 2003).In further research on the signal transduction

pathways operating in stress-affected cells, the precisemeasurement of stress-evoked events (e.g. the range ofturgor changes and plasma membrane dysfunction,activity of photosystems in chloroplasts, level of H2O2accumulation, etc.) may help in the identification of thepathways and genes involved in plant acclimation oralarm responses.

Acknowledgements – The preparation of this article was inspiredby Dr G. C. Srivastava (Indian Agricultural Research Institute,IARI), who invited the author to present a lecture on a similartopic during the 2nd International Congress of Plant Physiology,New Delhi, India, 2003. In addition, the author would like toexpress her thanks to Dr J. Fronk (Institute of Biochemistry,Warsaw University, Warsaw, Poland) for correction of the Englishlanguage.

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Fig. 1. Simplified scheme of the signalling systems responding to mild or severe stressors. The involvement of stress hormones, such as abscisicacid (in mild stress responses) and ethylene and jasmonates (in alarm responses), is not shown for the sake of clarity. See the text for a fullexplanation of the proposed interrelationships. Abbreviations: EEE, excess excitation energy; IP3, inositol-1,4,5-trisphosphate; PA,phosphatidic acid; PLD, phospholipase D (phospholipid signalling); PtdOH, phosphatidylalcohol; PUFA, polyunsaturated fatty acids;RLKs, receptor-like kinases; ROS, reactive oxygen species; RWC, relative water content; WAKs, wall-associated kinases.


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