Different stresses, similar morphogenic responses:integrating a plethora of pathways

GEERT POTTERS1, TARAS P. PASTERNAK2, YVES GUISEZ3 & MARCEL A. K. JANSEN4

1Department of Bioscience Engineering, University of Antwerp, Antwerp, Belgium, 2Institut für Biologie II/Botanik, Zentrumfür Angewandte Biowissenschaften, Universität Freiburg, Sonnenstr. 5, 79104 Freiburg, Germany, 3Plant Physiology,Department of Biology, University of Antwerp, Antwerp, Belgium and 4Plant Sciences (ZEPS), University College Cork,Distillery Field, North Mall, Cork, Ireland

ABSTRACT

Exposure of plants to mild chronic stress can cause induc-tion of specific, stress-induced morphogenic responses(SIMRs). These responses are characterized by a blockageof cell division in the main meristematic tissues, an inhibi-tion of elongation and a redirected outgrowth of lateralorgans. Key elements in the ontogenesis of this phenotypeappear to be stress-affected gradients of reactive oxygenspecies (ROS), antioxidants, auxin and ethylene. Thesegradients are present at the the organismal level, but areintegrated on the cellular level, affecting cell division, cellelongation and/or cell differentiation. Our analysis of theliterature indicates that stress-induced modulation of plantgrowth is mediated by a plethora of molecular interactions,whereby different environmental signals can trigger similarmorphogenic responses. At least some of the molecularinteractions that underlie morphogenic responses appear tobe interchangeable. We speculate that this complexity canbe viewed in terms of a thermodynamic model, in which notthe specific pathway, but the achieved metabolic state isbiologically conserved.

Key-words: auxin; morphogenesis; oxidative stress; reactiveoxygen species; redox.

STRESS-INDUCED MORPHOGENICRESPONSES (SIMRs)

Plants have a high level of physiological plasticity, enablingsurvival of a wide variety of environmental insults (Lusket al. 2008; Schmidt 2008). A key role in this plasticity isplayed by a range of protective responses. Many of thesestress-induced responses bestow protection against onespecific stress condition only; for example, photolyasesrestore DNA damage after exposure to UV-B radiation(Britt & Fiscus 2003), phytochelatins remove heavy metalsfrom the cytoplasm by transfering these into vacuoles(Sauge-Merle et al. 2003), proline accumulates in order to

counter drought stress (Patakas et al. 2002) and xantho-phylls protect photosystem II (PSII) from excessive lightand heat (Davison, Hunter & Horton 2002). In general,this kind of protective response to stress is relatively wellcharacterized at the molecular and biochemical levels (e.g.Becher et al. 2004; Parani et al. 2004). However, the ‘holygrail’ for stress physiologists, agronomists and breedersalike are generic defence responses, which confer a degreeof cross-tolerance against distinct stresses. Such cross-tolerance is often associated with changes in the metabo-lism of reactive oxygen species (ROS) (Noctor & Foyer1998). ROS are being produced during normal cell metabo-lism and are involved in the regulation of many physiologi-cal processes. However, following exposure to unfavourableenvironmental conditions, ROS are formed in excess,leading to a state of so-called oxidative stress (Apel & Hirt2004). The plant’s ROS defence network consists of enzy-matic components like superoxide dismutase or ascorbateperoxidase, and/or low molecular weight antioxidants likeascorbate (ASC) and glutathione (GSH) (Noctor & Foyer1998; Foyer & Noctor 2005a,b). This integrated system pre-vents oxidative damage in general. Moreover, ROS areimportant signalling molecules, involved in the perceptionof stress and mediating the plant responses following stressexposure (Apel & Hirt 2004; Laloi, Apel & Danon 2004).

A second generic stress response is the change in mor-phology that is observed in many plants exposed to sub-optimal environmental conditions. A recent survey of theliterature revealed SIMRs in many different plant species,and following exposure to many different stressors. It hasbeen proposed that these SIMRs constitute a generic,morphological response of plants to mild, chronic stressconditions (Potters et al. 2007). Examples of SIMRs arethe inhibition of root elongation and the simultaneousstimulation of lateral root formation, following exposureof roots to cadmium, copper, paraquat, hydrogen peroxideor low phosphate in the rhizosphere. Similarly, UV-B andmechanical stress inhibit shoot elongation and stimulateaxillary branching (Potters et al. 2007). This mixture ofgrowth-inhibiting and -activating responses is a character-istic of SIMRs (i.e. the stress-induced responses constitutegrowth redistribution rather than growth cessation). Ina previous paper (Potters et al. 2007), we have detailed

Correspondence: M. A. K. Jansen. Fax: +353 214 904 664; e-mail:M.Jansen@UCC.ie

This paper is dedicated to Professor Roland Caubergs on the occa-sion of his retirement.

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similarities in the responses of plants to different stressors,and concluded that SIMRs comprise inhibition of cellelongation, localized stimulation of cell division and alter-ations in cell differentiation status. In this paper, we focuson the mechanisms that are responsible for stress-inducedgrowth responses. Considering that distinct stresses inducesimilar growth redistributions (Potters et al. 2007), wehave asked the question whether there is a single molecu-lar mechanism underpinning morphogenic acclimation tostress. Literature analysis indicates putative roles forauxin, ethylene and ROS in mediating SIMR. Our surveytriggers the challenging question whether the same accli-mation state is reached by different, inter-exchangeablepathways, under different conditions.

MORPHOGENESIS – SYNTHESIS OFCELLULAR AND ORGANISMAL PERSPECTIVES

Plant morphogenesis is a complex process. Two distinctschools of thought have evolved with respect to analysis ofthe progression of this process. The first school of thought(reviewed by Prusinkiewicz & Rolland-Lagan 2006)emphasizes that morphogenesis is controlled by organ-and organism-wide gradients of signalling molecules, theso-called morphogenes. The morphogen gradients providepositional cues for individual cells, leading to a specificpattern of cell growth and cell elongation. Environmentalconditions that steer morphogenesis are translated into spe-cific patterns of morphogene distribution at the organism,organ or tissue scale, and this leads to super-cellular regu-lation of the processes that are linked to single cells. Rauch& Millonas (2004) expanded this model to incorporate thecellular signalling network. In this respect, the best docu-mented morphogens are the auxins.Auxin is involved in theestablishment of embryo polarity, phyllotaxis, organ forma-tion, root growth and development, root hair promotion,lateral root formation, controlling leaf thickness and veinpatterning, and its distribution relies on a network of bothdiffusion mechanisms and active transporters (Casimiroet al. 2001; Leyser 2005).

An alternative school of thought emphasizes that mor-phogenesis is a cellular process that is controlled by the rateof division and expansion of individual cells (Lindsey &Topping 1998; Sugimoto-Shirasu & Roberts 2003). Divisionincreases the number of cells in an organ. As the newlydivided cells exit the meristematic zone, cell expansionregulates the increase in cell size. Indeed, both cell divisionand elongation are the major cellular processes by which aplant expands, and any morphogenetic process roots inthese processes. Changes in morphology are the ultimateconsequence of changes in the division and/or expansionrate of the cells.

The organismal and the cellular school of thoughts reflectdifferent aspects of plant morphogenesis. An integratedvision of morphogenesis, whereby growth is being con-trolled at both the cellular and the organismal levels, hasalso been developed (Beemster, Fiorani & Inzé 2003).In this view, the growth and formation of organs are

coordinated through growth substance gradients and sig-nalling at the organ and organismal levels. Within growthzones, the expansion, division and differentiation of indi-vidual cells are coordinated at the cellular level, where cellsare continuously sensing and responding to the presence ofeach other, involving both regulatory interactions as well ascompetition for the flow of resources and signalling mol-ecules (Beemster et al. 2003).

SIMRs comprise: (1) inhibition of cell elongation; (2)localized stimulation of cell division; and (3) complex alter-ations in cell differentiation status, and these changes occurin a coordinated manner, leading to a change in plant mor-phology (Potters et al. 2007). Thus, there are clear cellularand organismal components in the control of the SIMRphenotype. For ease of analysis, we chose to analyse theSIMR concept through separate organismal and cellularlines of thought.

SIMR – AN ORGANISMAL VIEW

In this chapter, we will analyse the SIMR phenotype froman organismal perspective: we will pinpoint stress-re-sponsive physiological mechanisms that control plant mor-phology, on the organ or tissue level. Primarily, we will focuson three morphogenes (auxin, ethylene and ROS) that arepersuasively linked to signalling and response mediationunder a range of distinct abiotic stress conditions (Fig. 1).

A role for ROS in SIMRs

ROS have long been associated with the negative effects ofa broad range of stresses on plants. There is overwhelmingevidence that environmental parameters impact on ROSlevels, the concentration of antioxidants and their oxidationstate (Apel & Hirt 2004, and references quoted therein).Despite historic emphasis on the link between ROS andstress, ROS are actually of crucial importance in a broadrange of physiological processes associated with plantgrowth and development. For example, ROS are importantsignalling molecules (Van Breusegem et al. 2001; Vranovaet al. 2001), produced through different types of enzymes(Murphy, Asard & Cross 1998), the expression of which, inturn, is controlled by a broad range of different environ-mental cues. Hydrogen peroxide in particular is capable ofcrossing cellular barriers and activating gene expression indistant tissues (Mullineaux, Karpinski & Baker 2006).Moreover, concentration gradients of ROS (particularlyH2O2) can be formed across a cell (Coelho, Brownle &Bothwell 2008), a plant organ (Fryer et al. 2003) or even awhole plant (Songjie et al. 2006). Localization of H2O2 syn-thesis close to xylem vessels provides a physical path forH2O2 transport (Fryer et al. 2003). Indeed, (Songjie et al.2006) suggested that root-derived H2O2 may act as a signalthat triggers stomatal closure. Yet, the predicted half-life of1 ms for H2O2 (Van Breusegem et al. 2001; Vranova et al.2001) is likely to preclude a more general role for H2O2

diffusion in organismal stress signalling. Instead, Van Breu-segem et al. (2001) have hypothesized that local H2O2 levels

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are enhanced through increased local production, activatedvia a not yet identified, long-distance signalling method.

There is increasing evidence that ROS signals play a rolein controling developmental processes (Gapper & Dolan2006). ROS have been shown to influence cell development(e.g. xylem vessel formation; Ros-Barcelo et al. 2002), celldivision (i.e. temporarily inhibiting cell cycle activity; Reich-held et al. 1999), cell elongation (Schopfer 2001), somaticembryogenesis (Cui et al. 1999; Pasternak et al. 2007) andadventitious root formation (Li et al. 2007). Specifically, ithas been found that ROS generated by RHD2 NADPHoxidase (atrbohC) are required for root hair growth inArabidopsis (Foreman et al. 2003).

Thus, ROS are effective at the organismal scale, both assignalling molecules and as determinants of morphologicaldevelopment. A direct link between ROS and the SIMRphenotype has been demonstrated by Pasternak et al.(2005a,b) who found that Arabidopsis thaliana plantlets

subjected to either ROS-generating compounds (e.g.paraquat), or a hydrogen peroxide derivative (Pasternaket al. 2005a,b) had an SIMR-like phenotype, similar to thatinduced by, for example, copper. ROS treatments inducedlateral root formation, while inhibiting root elongation (i.e.ROS induced a redistribution of growth consistent withthe overall SIMR phenotype). Similarly, the ASC-deficientmutant (vtc1) is characterized (even under control condi-tions) by lack of rosette elongation and retarded flowering(Veljovic-Jovanovic et al. 2001), as well as by the formationof many lateral roots that fail to elongate (Pasternak,unpublished results). This mutant lacks the antioxidantASC and was specifically isolated because of its high sensi-tivity towards oxidative stressors. The adoption of an SIMRphenotype by the vtc1 mutant is likely to reflect changes inROS metabolism. Salicylic acid, a compound which accu-mulates in response to abiotic or biotic stresses and whichinterferes with ROS metabolism via inhibitory effects oncatalase and peroxidases activity, also induced the SIMRphenotype (Pasternak et al. 2005a). Based on these data, weconsider it very likely that ROS are playing a role, directlyor indirectly, in controlling the SIMR phenotype in stress-exposed A. thaliana seedlings.

A role for auxin in SIMRs

Morphogenesis is tightly linked to hormonal homeostasis,with several hormones controlling cell elongation, cell divi-sion and re-orientation of growth. Auxin [indole-3-aceticacid (IAA)] and its gradients are closely associated withlateral root formation and axillary branching, two key com-ponents of the SIMR phenotype of plants exposed to heavymetals or phosphorus starvation (Potters et al. 2007). Exo-geneous auxin applications result in formation of branchedroots that, however, do not elongate (Magidin et al. 2003).Similarly, mutants that accumulate high levels of auxin, ormutants with an altered auxin distribution, produce excesslateral roots (Boerjan et al. 1995; Marchant et al. 2002).2,3,5-Tri-iodobenzoic acid (TIBA) blocks lateral root for-mation (Tyburski, Jasionowicz & Tretyn 2006), and this isalso the case for several auxin-resistant mutants that havereduced numbers of lateral roots (Malamy & Benfey 1997).Clearly, the capacity and patterning for lateral organformation are directly related to auxin patterning and/ordistribution (Casimiro et al. 2001; Reinhardt et al. 2003).Considering that several soil-based abiotic stresses inducelateral root formation, auxin is a plausible intermediatebetween the action of a stressor and the realization of anSIMR phenotype. Indeed, phosphorus-starved lupins andArabidopsis produce large numbers of lateral roots, and thisresponse was linked to changes in auxin homeostasis(López-Bucio et al. 2002). Consistently, the formation oflateral roots in phosphorus-deficient plants can be inhibitedwith TIBA and N-(1-naphthyl) phtalamic acid (Gilbert et al.2000; López-Bucio et al. 2002). Several mechanisms havebeen proposed to explain stress-induced changes in auxinmetabolism and/or receptiveness; however, a survey of theliterature found predominantly evidence for stress-induced

Figure 1. Model of the general interactions leading to thestress-induced morphogenic response (SIMR) phenotype. Keycomponents are reactive oxygen species (ROS), auxins andethylene, which are all affected by changing environmentalparameters (stress), and in turn influence each other. Thecombination of these physiological parameters is integrated onthe cellular level, leading to changes in division, elongation anddifferentiation, leading to an SIMR phenotype (representationhere after Potters et al. 2007). Arrows indicate direct effects ofstress on ROS, auxins and ethylene, as well as subsequent effectson the organismal or local redox state, and cellular processes.

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changes in auxin transport and catabolism. For example,aluminium inhibits basipetal auxin transport, affectingauxin redistribution, and resulting in an inhibition of rootcell elongation (Kollmeier, Felle & Horst 2000). Similarly,water and osmotic stress impact on auxin transport (Dav-enport, Jordan & Morgan 1977; Sheldrake 1979). Two spe-cific molecular mechanisms may explain the changes inauxin transport: altered expression of PIN genes and/orinhibition of polar auxin transport by phenolics. Environ-mental parameters are known to affect expression of auxinefflux carrier genes (Schrader et al. 2003). Alloxan has beenshown to down-regulate expression of the PIN1 and PIN3genes (Pasternak et al. 2005b). The products of these PINgenes are responsible for auxin transport throughout theroot, and any change in their activity may result in analtered pattern of auxin distribution throughout the organ-ism (Leyser 2005; Paponov et al. 2005). However, stress-induced inhibition of polar auxin transport might notnecessarily require such specific changes in gene expres-sion. An alternative scenario centres on the inhibition ofpolar auxin transport by phenolics. Many distinct phenoliccompounds accumulate in response to stress exposure(Winkel-Shirley 2002) and are able to act as endogenousauxin transport inhibitors in vitro (Jacobs & Rubery 1988),as well as in situ (Brown et al. 2001). Indeed, Peer et al.(2004) were able to demonstrate an inverse relationbetween auxin transport and flavonoid content in a series ofArabidopsis flavonoid mutants. Consistently, expression ofMAX1, a positive regulator of the flavonoid synthesispathway, has been directly linked to repression of vegeta-tive axillary bud growth, which in turn is thought to beassociated with decreased auxin transport (Lazar &Goodman 2006). A similar model has been proposed byPeer & Murphy (2007), citing flavonoid and auxin reportergene expression patterns being similar as well as implicatingflavonoid synthesis in the regulation of lateral root forma-tion in response to phosphate availability (Misson et al.2005). Because regulation of the flavonoid pathway issubject to control by a large number of environmentaland stress-related factors, flavonoids and related phen-olics appear well positioned to link stress exposure tomorphogenesis.

The catabolism of IAA is also subject to modulation bystress conditions. Class III peroxidases are enzymes that arecapable of IAA degradation (Jansen et al. 2001). IAA isdegraded via a peroxidative mechanism coupled to a veryefficient branched-chain process in which organic peroxideis formed (Dunford 1999), or via an oxidative mechanism,using molecular oxygen as electron sink (Savitsky et al.1999). Many different stresses are known to induce theexpression of class III peroxidases (Hiraga et al. 2001).However, the link between peroxidase activity and IAAcatabolism is not as clear under in vivo conditions assuggested by in vitro experiments. For example, manyphenolic compounds, such as chlorogenic acid, caffeic acidor sinapic acid, inhibit the IAA oxidase activity of peroxi-dases, whereas other compounds (e.g. coumaric acid andferulic acid) rather stimulate this reaction (Jansen 2002).

Moreover, the levels of specific phenolic compounds them-selves may be altered under stress conditions (Winkel-Shirley 2002). For example, the quercetin to kaempferolratio increases in plants acclimated to UV-B (Olsson,Veit &Bornman 1999). This potentially affects IAA oxidase rates,as the peroxidase-catalysed oxidation of IAA is inhibitedby physiological concentrations of quercetin, but promotedby kaempferol.

Stress-induced changes in auxin conjugation can alterIAA activity, and hence impact on morphogenesis. IAAconjugate pools increased under salinity stress in Populuseuphratica (although not in P. ¥ canescens). Interestingly,overexpression of an auxin–amidohydrolase in Arabidopsisis associated with a decrease in salinity-induced inhibitionof root elongation (Junghans et al. 2006). These data implythat Arabidopsis uses the conjugate pool to balance out theeffects of salt on auxin metabolism, and thus modulateinduction of SIMR (Junghans et al. 2006). In addition, stressconditions (drought, cold, heat), abscisic acid as well assalicylic acid induce WES1 expression, a GH3 class gene,encoding an auxin-conjugating enzyme. Mutants of thisgene are resistant to stress (measured as survival, chloro-phyll content and expression of enzymes such as peroxi-dases) (Park et al. 2007). GH3 genes are also up-regulatedunder Cd stress as well (Minglin, Zhang & Chai 2005).

Finally, stress can modulate auxin sensitivity, and this caninvolve at least two different scenarios: nitric oxides orDELLAs. Nitric oxide acts downstream in auxin signalling,and is known to control several morphogenic responses.However, NO does not simply act as an auxin signal trans-ducer, but rather as the crossroads for several hormone andstress signals, thus integrating multiple signals into a singlemorphogenic response (Lamattina et al. 2003). DELLAsare nuclear proteins that impede cell proliferation andgrowth, following exposure to stress and/or phytohor-mones, including auxin, gibberellic acid and ethylene(Achard et al. 2006). More specifically, DELLA proteins areplaying a role in mediating the morphogenic alterationsseen in phosphate-starved plants (Jiang et al. 2007) where itwas observed that phosphate starvation responses can berepressed by exogenous GA or by mutations conferring asubstantial reduction in DELLA function. In contrast,an enhanced DELLA function caused plants to exhibitenhanced phosphate starvation responses.Thus, while expo-sure to salinity inhibits root elongation and leaf productionin Arabidopsis, no such inhibitory effect is visible in amutant lacking DELLA proteins (Achard et al. 2006).Other factors that are likely to modulate DELLA signallingare jasmonic acid and salicylic acid, both of which areknown to be stress responsive (Navarro et al. 2008).

A role for ethylene in SIMRs

Ethylene is another hormone which is often associated withstress, and which may play a role in the realization ofSIMRs. Ethylene is mostly associated with growth retarda-tion in plants (Dugardeyn & Van Der Straeten 2008) andstimulates root hair formation (Pitts, Cernac & Estelle

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1998). Ethylene is involved in the responses of several plantspecies to heat, drought or ozone stress (Larkindale &Knight 2002; Rao, Lee & Davis 2002). Ethylene emissionsprecede the inhibition of root growth, caused by aluminium,in bean plants (Massot et al. 2002). Inhibition of ethylenesynthesis or ethylene action prevents the occurrence ofwhat we described before as an SIMR phenotype underphosphate-deficient conditions (Zhang, Lynch & Brown2003). Ethylene inhibits root elongation in phosphate-deficient plants, but promotes elongation in control plants(Borch et al. 1999). This apparent contradiction is hypoth-esized to be caused by the fact that ethylene is involved inonly part of the mechanism leading up to an SIMR pheno-type. Consistently, ethylene is unlikely to be associated withall aspects of the SIMR phenotype (e.g. the increase in thedensity and the size of root hairs in phosphate-deficientplants is not controlled by ethylene) (Ma et al. 2001). Ingeneral, ethylene is thought to enhance auxin sensitivity inthe root (Visser et al. 1996; Takahashi, Kawahara & Inoue2003b). It is therefore plausible that, although ethylenetakes on a role in the SIMR process, it merely contributes toa change in the auxin responsiveness of plants.

Other hormones may contribute as well to the onset of anSIMR. However, while the case for involvement of ROS,auxin and ethylene in mediating SIMR is strong, there ismuch less literature to support involvement of otherhormones in a generic SIMR.

Cross talk between auxin and ROS signalling

Auxins and ROS are two molecular signals that impact onmorphogenesis and whose metabolism is affected by expo-sure to abiotic stress. However, these two signalling path-ways should not be seen in isolation, as they extensivelyimpact on each other. For instance, stress-induced changesin the cellular pH gradient (Murphy et al. 1998) will impacton chemiosmotically driven IAA uptake, transport andredistribution. Furthermore, ROS will act downstream ofIAA signalling (Kwak, Nguyen & Schroeder 2006), as dem-onstrated for gravitropic responses (Joo, Bae & Lee 2001).ROS may modulate auxin sensitivity, by down-regulation ofauxin-inducible gene expression, a process that involveschanges in MAPK activity (Kovtun et al. 2000). Moreover,the auxin-induced elongation of root cells is easily mim-icked using either superoxide or hydrogen peroxide(Schopfer et al. 2002). Conversely, auxins as well as cytoki-nins modulate H2O2 effects on stomatal closure, by regulat-ing H2O2 scavenging (cytokinins) or production (auxins)(Song et al. 2006). As a little aside, a possible role of nitricoxide and other reactive nitrogen species (RNS) inthe control of morphogenesis should be acknowledged(Besson-Bard, Pugin & Wendehenne 2008; Kolbert, Bartha& Erdei 2008). Similar to the cross talk between ROSand auxin, we note an association between nitric oxideand auxin in the control of, for example, cell division(Ötvös et al. 2005). However, the interaction of ROS and/ornitric oxide with plant hormones remains to be fullycharacterized.

BETWEEN ORGANISMAL AND CELLULARLEVELS: REDOX REGULATION OF GROWTH

Organismal gradients of ROS and phytohormones influ-ence local growth responses, among others, by acting uponthe redox state. The theoretical concept of redox state isdefined as the degree of oxidation of cellular (Dietz 2008),tissue (Jiang, Meng & Feldman 2003) or perhaps even organ(Benada 1967a,b) components. More commonly, the redoxstate is calculated by the redox state of antioxidantmolecules like ASC and GSH [i.e. the proportion of thereduced molecule relative to the total amount (reduced andoxidized) of that molecule in a tissue, cell or cell compart-ment]. In this respect, the redox state creates an interfacebetween the organismal and cellular stress response levels,integrating the stress signals the plant perceives with thecontrol of local, cellular redox equilibria (Jiang et al. 2003;Dietz 2008).

The redox state of ASC has been associated with theregulation of many physiological processes (Horemanset al. 2000; Pignocchi & Foyer 2003). Different biotic andabiotic stresses impact on the apoplastic redox state (Luwe1996), and it has been hypothesized that this results incross talk between different defence and growth pathways(Torres & Dangl 2005). Stress can impact on various pro-cesses, via increased production of ROS, and consequentchanges in the cell redox state as a result of the oxidation ofASC or GSH (Noctor & Foyer 1998). Both ASC and GSHhave specific functions in shaping and maintaining properroot morphology, with ASC stimulating lateral root forma-tion and inhibiting elongation of root cells, and GSH modu-lating root hair elongation (Sánchez-Fernández et al. 1997).The major antioxidant in the apoplast is ASC, which can beoxidized by the apoplastic enzyme ascorbate oxidase. Thisenzyme can also oxidize auxin, leading to its degradation(Kerk, Jiang & Feldman 2000). Ascorbate oxidase is acti-vated by auxin (Kerk & Feldman 1995), and it has beenhypothesized that ascorbate oxidase serves to modulate theredox state of the apoplast, which in turn influences signaltransduction processes regulating growth or defence pro-cesses (Pignocchi & Foyer 2003). Controlled oxidation ofthe apoplastic ASC pool by the action of ascorbate oxidasehas been predicted to have a similar effect on the apoplasticredox state as the sustained production of ROS (Pignocchi& Foyer 2003; Foyer & Noctor 2005a,b). Apparently, ascor-bate oxidase acts as a focal point for the interaction of auxinand redox signals, whereby auxin can alter the redox stateof ASC by, among others, changing the expression of theenzyme ascorbate oxidase (Kerk & Feldman 1995; Jianget al. 2003).

SIMR – A CELLULAR VIEW

Stress-induced changes in morphogenesis are ultimatelycaused by changes in the developmental programmesrunning at a cellular level. At this level, growth comprisesthree components: cell elongation, cell division and cell dif-ferentiation. SIMR constitutes a complex redirection of

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growth, whereby stress, in parallel, inhibits cell elongation,stimulates localized cell division and alters the cell differ-entiation status. Considering the complexity of these stress-induced alterations, it is likely that a number of distinctmolecular processes underpin SIMR.

Cell elongation acts as focal point for ROS,auxin and the cellular redox state

Particularly striking in the concept of SIMR is the inhibi-tion of cell elongation, as a result of the exposure to abioticstresses. This inhibitory effect has been extensively docu-mented both at the macroscopic level (e.g. Jansen, Gaba &Greenberg 1998; Schützendübel et al. 2001; Rodríguez et al.2004; Pasternak et al. 2005a; Verma & Mishra 2005) as wellas the microscopic level (Thomas, James & Humphreys1999; Neves-Piestun & Bernstein 2001; Ortega & Taleisnik2003; Pasternak et al. 2005a,b). For example, elongation ofmaize root cells is inhibited by aluminium in the apoplast,resulting in the stalling of root growth (Horst 1995). Simi-larly, petiole and leaf mesophyll cells remain significantlyshorter in A. thaliana plants treated with copper, cadmium,paraquat or alloxan compared to control plants (Pasternaket al. 2005a), while UV-B radiation inhibits elongation ofepidermal cells (Ruhland & Day 2000).

Cell elongation directly depends on cell wall flexibility,which in turn is controlled by a number of stress-induced andphytohormone-related physiological processes. For ex-ample, class III peroxidases are induced by a broad range ofabiotic stresses (Hiraga et al. 2001), and these enzymes cannegatively impact on cell wall flexibility. Using H2O2 gener-ated by redox reactions in the cell wall or at the plasmamembrane (Murphy et al. 1998), peroxidases catalyse cross-linking between phenolic compounds as well as the forma-tion of bonds with other cell wall components, leading to thestiffening of the cell wall. Several studies have shown thatthere is a negative correlation between peroxidase activitylevels and cell expansion (Chaoui & El Ferjani 2005). Thenegative effects of stress on cell wall flexibility may befurther enhanced because of stress-induced increases in thelevels of phenolic compounds present in the apoplast.

The antioxidant ASC also impacts on cell wall flexibility.This is important in an environmental context, as numerousstudies have reported decreases of cellular and apoplasticlevels of reduced ASC in plants exposed to abiotic stress(Pignocchi & Foyer 2003). In the apoplast,ASC can impedethe peroxidase-mediated stiffening of cell walls, via in-hibition of both soluble and wall-attached peroxidases(Cordoba-Pedregosa et al. 1996). Consistently, root elonga-tion is stimulated when seedlings are grown in the presenceof ASC, or the ASC precursor l-galactone-g-lactone. ASCcan also inhibit the peroxidative, covalent cross-linking ofwall polysaccharides and lignin polymerization by scaveng-ing hydrogen peroxide and monolignol radicals (see alsoTakahama 1994). Conversely, a decrease in the levels ofreduced ASC will result in increased wall stiffening anddecreased organ elongation. This inhibitory effect onelongation can be visualized using the ASC biosynthesis

inhibitor lycorine (Arrigoni, Arrigoni-Liso & Calabrese1975; Cordoba-Pedregosa et al. 1996), and is likely to be asignificant factor in stress exposed tissues.

Stress-induced changes in ASC redox state will alsoimpact on the structural cell wall-based extensins. ASC isessential for the post-translational formation of hydrox-yprolyl residues on these proteins, and hence for theirfunctionality (Arrigoni & De Tullio 2000). Additionally,the semi-oxidized, free radical form of ASC [monodehy-droascorbate (MDHA)] can also affect wall biology.MDHA acts as both electron donor and acceptor in trans-membrane electron transport (Asard, Horemans & Caub-ergs 1995). Transmembrane electron transport stimulatesH+-ATPase activity and leads to cell wall acidification, andconsequently cell wall loosening (Rayle & Cleland 1992).MDHA also causes an increased vacuolization, a processwhich drives cell elongation even more (Cordoba-Pedregosa et al. 1996). ASC can become oxidized as aconsequence of stress exposure, or as a result of ascorbateoxidase activity. The latter enzyme has long been con-sidered to control cell enlargement via the modulation ofredox control of the apoplast (Kato & Esaka 1999), and thisactivity is stimulated by auxin (Esaka et al. 1992). Theimpact of auxin on wall flexibility and cell elongation isfurther related to both cell wall acidification (acid growthhypothesis), and to an increased production of superoxideradicals (Schopfer 2001). These superoxide radicals will,upon further reduction, give rise to hydroxyl radicals, whichmay act as a wall-loosening factor and may so act as inter-mediate in auxin-mediated elongation.

A symplastic determinant of organ or tissue elongationis the microtubule network, which directly controls cellextension. This network is sensitive to aluminiumstress (Schwarzerová et al. 2002) and responsive to auxins(Baluska, Barlow & Volkmann 1996). It is thought thatplants are capable of responding to oxidative stress andauxin signals by activating specific MAP kinases (Kovtunet al. 2000) resulting in altered microtubule and cellelongation dynamics (Samaj et al. 2002). In the case of alu-minium stress, it is thought that metal ions can either inter-act directly or indirectly with the cytoskeleton (Sivaguruet al. 1999). Indirect effects, via oxidative stress, can bemediated by GSH which changes the orientation of micro-tubules in Picea (Urbanek et al. 2003), thereby offering apossibility to redirect growth (Dolan & Davies 2004).Microtubule orientation has also been linked to auxins (i.e.auxin is involved in the organization of microtubulenetwork, both in shoot and root cells) (Nick, Schäfer &Furuya 1992; Takahashi et al. 2003b). Auxin (in conjunctionwith ethylene) seems to be indispensable for randomizationof the cortical microtubules, a process necessary for roothair initiation (Takahashi et al. 2003a).

Oxidative stress and auxin modulatecell division

A common and important constituent of an SIMR is theredistribution of cell cycle activity. The cell cycle acts as a

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focal point for various stress and hormone signals. Thenetwork of interactions between ROS, antioxidants andphytohormones can provide a physiological modulation ofthe cyclin–cyclin-dependent kinase-related biochemicalsteps of the cell cycle. Both auxins and cytokinins affect thecell cycle, and these effects involve modulation of the activi-ties of cyclin–cyclin-dependent kinases (Stals & Inzé 2001).Oxidative stressors have also been shown to directly controlcell cycle progression (Francis 1998), leading to the postu-lation of the existence of an ‘oxidative stress checkpoint’(Reichheld et al. 1999; De Schutter et al. 2007). Rather thanexposing cells to oxidative stress, other groups have directlyaltered the cellular redox state by altering the cellular poolsof antioxidants, showing that both dehydroascorbate andGSH are also able to interfere with normal cell cycle pro-gression (Potters et al. 2002).

However, it needs to be emphasized that stress exposuredoes not necessarily impair cell cycle activity throughoutthe plant, but rather redistributes cell cycle activity. Forexample, while heavy metal exposure led to a cessation ofmeristematic activities in the main root apex, it also inducedcell division activity leading to the formation of new lateralroots (Pasternak et al. 2005a,b).A similar pattern was foundby Doncheva et al. (2005), who noticed that in aluminium-sensitive plants, cell division in the proximal meristem wasinhibited (even after 5 min of exposure), but that cell divi-sion was stimulated in the distal elongation zone, withlateral roots protruding after just 3 h. These observationsled Doncheva et al. (2005) to suggest that a short exposureto aluminium causes a fast change in cell patterning insteadof a general toxic effect. Similarly, effects of UV-B radiationon cell division are complex, with some studies reportingreductions in numbers of epidermal cells (Hopkins, Bond& Tobin 2002), and others increase in parenchymacells (Staxen & Bornman 1994). Again, these data suggestchanges in patterning rather than a general toxic effect.Positioning root primordia is a trait attributed to auxinaction, with several mutants defective in early auxinresponses forming no, or a reduced number, of lateral roots(Casimiro et al. 2003) and with a similar phenotype uponinhibition of active auxin transport (Casimiro et al. 2001). Itis therefore quite imaginable that by changing the distribu-tion of, par excellence, auxin (as a consequence of stress),architecture is altered.

Stress and cell development

The effect of stress on cell development is particularlycomplex, as abiotic stress is known to intervene in differentaspects of cell development. Cadmium-induced H2O2 pro-duction sets in motion a complex series of events com-prising an inhibition of elongation growth to, ultimately,programmed cell death, albeit the latter possibly only inalready committed cells (Schützendübel et al. 2001). InBY-2 cells, a concentration of 50 mm Cd induces massiveprogrammed cell death (Kuthanová et al. 2004). However,in many other cases, stress exposure induced dedifferentia-tion. For example, Pasternak et al. (2002) demonstrated the

induction of dedifferentiation of alfalfa cells by exposingleaf mesophyll cells to an excess iron in the culture medium.Similar results were obtained after addition of a lowamount of copper, cadmium, paraquat, hydrogen peroxideor alloxan to a leaf protoplast culture (Pasternak et al. 2002,2005b).

A PLETHORA OF PATHWAYS OR ATHERMODYNAMICAL EQUILIBRIUM?

SIMRs are observed in many different plant species, andfollowing exposure to many different stressors, indicatingthe generic character of these morphological responsesunder mild, chronic stress conditions (Potters et al. 2007).Based on our survey of the literature, we hypothesizethat stress-induced changes in auxin and ROS metabolismare likely to be important components of the mechanismunderlying SIMRs. Yet, the literature survey also revealsthat stress-induced changes in auxin and/or ROS levelscan impact on morphogenesis via a plethora of distinctpathways.

Different types of stress can induce similar SIMRs(Potters et al. 2007), an observation that is quite strikingconsidering the different modes of stress perception, targettissues and effects on cellular metabolism. For example,cadmium is taken up through the roots and changes calciumequilibria (Sanità di Toppi & Gabbrielli 1999; Perfus-Barbeoch et al. 2002), copper interacts with the redoxbalances in the apoplast (Kärkönen & Fry 2006; Sgherri,Quartacci & Navarri-Izzo 2007), UV-B impacts on DNAtranscription and replication, as well as photosynthesis(Jansen et al. 1998) and paraquat and alloxan directlyinduce the production of ROS. Yet, all these stressorsinduce morphogenic responses comprised of an inhibitionof elongation, localized stimulation of cell division andcomplex changes in cell differentiation. It has been arguedthat each specific stress is responsible for the induction of arange of seemingly unrelated stress defence pathways.Sanità di Toppi & Gabbrielli (1999) described such a ‘fan-shaped response pyramid’, detailing how cadmium causes awhole series of secondary stress responses, ranging fromthe activation of peroxidases, metallothioneins, phyto-chelatins to the production of ethylene. Microarray analysisof cadmium-stressed plants has shown how the expressionof numerous genes is altered, in a tissue-specific andconcentration-dependent manner following stress expo-sure, and this includes genes encoding enzymes involved inphotosynthesis, cell wall metabolism, signal transduction,sulphur metabolism and phenylpropanoid synthesis (Her-bette et al. 2006). Similar ‘fan-shaped’ responses in tran-scription pattern have been described for a wide range ofabiotic stresses. It is possible that distinct stresses activatea small core of conserved response elements, and thatthese are responsible for the generic character of SIMR.However, this is not necessarily the only explanation for thegeneric character of some of the SIMRs. Sanità di Toppi &Gabbrielli (1999) state that ‘the “fan-shaped” response doesnot dogmatically imply that all the processes involved (the

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rays of the fan) are always present in all plant systems,always equally important and always acting in co-operation.[. . .] Hence, the relative importance of each responsemechanism may appreciably differ’. Indeed, stress res-ponses seem to be interchangeable, at least to a certainextent. For example, catalase and ascorbate peroxidase canassume each other’s role in increasing oxidative defence(Kubo et al. 1999; Rizhsky et al. 2002;Asai et al. 2004), whileincreased cell elongation can compensate for lack of mitosisduring organ growth (Ferjani et al. 2007). Similarly, alter-ations in auxin synthesis, sensitivity, transport and catabo-lism are all interchangeable to some extent. Actually, theconcept of similar responses mediated by distinct environ-mental signals and pathways is well known. For example,similar gravitropic responses can be mediated by red light,calcium, touch, moisture, oxygen, temperature, ethylene andauxin, while stomatal opening can be driven by circadianrhythms, humidity, temperature, blue light, abscisic acid,potassium, carbon dioxide and nitrate. In analogy, wesuggest that a maze of interchangeable molecular processes,rather than a single pathway, is responsible for the induc-tion of an SIMR phenotype under different stress condi-tions. This idea agrees with the stress response concept byTsimilli-Michael, Kruger & Strasser (1996) and Gasparet al. (2002), who propose the existence of a set of distinctmetabolic (in the broadest sense of the word) state func-tions, based upon thermodynamic arguments (Fig. 2a).Under each given set of environmental restraints, there isan optimized metabolic state. If the controlling restraintsare altered (e.g. the environment changes; the plant is con-fronted with a mild stress), this state function shifts into anew optimal value. Translated into biological terms – theplant acclimates to its new environment. If the environmentbecomes too unfavourable, no optimalization is possibleand the plant (tissue, cell) will die. According to this ther-modynamic view, not the specific pathway by which thisstate function evolves, but solely its beginning and endpoints have any biological relevance. In a sense, this is anunusual way of describing the phenomenon of acclimation,especially for biochemically trained plant biologists that areused to think in terms of pathways and gene expression.Yet, this type of argument may help us decipher why aplethora of multiple, interchangeable pathways (Fig. 2b)can induce similar, conserved SIMR phenotypes in differentplant species following exposure to distinct environmentalstresses.

CONCLUSION

In this paper, we have explored how abiotic stresses caninterfere with the molecular pathways controlling plantmorphogenesis. We have reviewed how stress impacts onthe organismal gradients (like hormone redistribution andROS production) and cellular processes (like cell cycle andcell elongation).We hypothesize that a plethora of multiple,interchangeable pathways, rather than a single metabolicresponse, controls the SIMR phenotype under differentstress conditions.

ACKNOWLEDGMENTS

The authors would like to thank Inge van Dyck for helpwith the graphics. The authors acknowledge the support ofWoB (to M.A.K.J.) and BMBF (to T.P.P.).

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