Class III peroxidases in plant defence reactions

Journal of Experimental Botany, Vol. 60, No. 2, pp. 377–390, 2009doi:10.1093/jxb/ern277 Advance Access publication 10 December, 2008

REVIEW PAPER

Class III peroxidases in plant defence reactions

L. Almagro1,*, L. V. Gomez Ros1,*, S. Belchi-Navarro1, R. Bru2, A. Ros Barcelo1 and M. A. Pedreno1,†

1 Department of Plant Biology, Faculty of Biology, University of Murcia, Campus de Espinardo, E-30100 Murcia, Spain2 Departamento de Agroquimica y Bioquimica, Universidad de Alicante, Campus de San Vicente del Raspeig, E-03080 Alicante, Spain

Received 12 August 2008; Revised 8 October 2008; Accepted 14 October 2008

Abstract

When plants are attacked by pathogens, they defend themselves with an arsenal of defence mechanisms, both

passive and active. The active defence responses, which require de novo protein synthesis, are regulated through

a complex and interconnected network of signalling pathways that mainly involve three molecules, salicylic acid

(SA), jasmonic acid (JA), and ethylene (ET), and which results in the synthesis of pathogenesis-related (PR) proteins.

Microbe or elicitor-induced signal transduction pathways lead to (i) the reinforcement of cell walls and lignification,

(ii) the production of antimicrobial metabolites (phytoalexins), and (iii) the production of reactive oxygen species

(ROS) and reactive nitrogen species (RNS). Among the proteins induced during the host plant defence, class III plantperoxidases (EC 1.11.1.7; hydrogen donor: H2O2 oxidoreductase, Prxs) are well known. They belong to a large

multigene family, and participate in a broad range of physiological processes, such as lignin and suberin formation,

cross-linking of cell wall components, and synthesis of phytoalexins, or participate in the metabolism of ROS and

RNS, both switching on the hypersensitive response (HR), a form of programmed host cell death at the infection site

associated with limited pathogen development. The present review focuses on these plant defence reactions in

which Prxs are directly or indirectly involved, and ends with the signalling pathways, which regulate Prx gene

expression during plant defence. How they are integrated within the complex network of defence responses of any

host plant cell will be the cornerstone of future research.

Key words: Ethylene, jasmonic acid, lignification, peroxidases, phytoalexin, reactive nitrogen species, reactive oxygen species,

salicylic acid.

Introduction

When plants are attacked by pathogens, they defend

themselves against such invasion with an arsenal of defence

mechanisms, both passive and active. The passive or pre-

existing defence mechanisms involve structural barriers or

strategically positioned reservoirs of antimicrobial com-

pounds which prevent colonization of the tissue. The active

or induced defence responses include the hypersensitiveresponse (HR), the production of phytoalexins and patho-

genesis-related (PR) proteins, ion fluxes across the plasma

membrane, the production of reactive oxygen species (ROS)

and reactive nitrogen species (RNS) (oxidative bursts),

lignification, and the reinforcement of the cell wall through

both the cross-linking of cell wall structural proteins and

the deposition of callose. The efficacy of these defence

responses often determines whether plants are susceptible or

resistant to pathogenic infection. In many plants, resistance

to diseases or to avirulence determinants is known to begenetically controlled by plant resistance genes which confer

resistance to pathogens with a matching avirulent (Avr)

gene by specific recognition events (Zhao et al., 2005).

* These authors contributed equally to this review.y To whom correspondence should be addressed: E-mail: [email protected]: Ara, arabinose; Avr, avirulent; CI, compound I; CII, compound II; CIII, compound III; DPI, diphenylene iodonium; EPR, electron paramagneticresonance; ESR, electron spin resonance; ET, ethylene; HR, hypersensitive response; HRGPs, hydroxyl-proline (Hyp)-rich; JA, jasmonic acid; MeJA,methyljasmonate; NOS, NO synthase; PCD, programmed cell death; PPD, poly(phenolic) domain; PR, pathogenesis-related; Prx, class III plant peroxidase; RNS,reactive nitrogen species; ROS, reactive oxygen species; SA, salicylic acid; SAR, systemic acquired resistance.ª The Author [2008]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.For Permissions, please e-mail: [email protected]

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However, triggering resistance is not always due to specific

Avr products, which activate defence responses in cultivars

possessing the matching resistance genes but, instead, pro-

ceeds from the action of general elicitors able to activate

defences in different cultivars of one or many species

(Garcia-Brugger et al., 2006).

Early signal transduction pathway studies with elicitors

revealed striking similarities between plants and animals inmolecules which are used to perceive and transmit signals

associated with invaders. These observations highlight the

conservation of a defence-related signalling system in the

different living kingdoms throughout evolution (Nurnberger

et al., 2004). Early events also mobilize or generate, directly

or indirectly, diverse signalling molecules and regulate many

processes, interconnecting branch pathways that amplify and

specify the physiological response through transcriptionaland metabolic changes (Zhao et al., 2005). Studies with

different plant–pathogen systems have shown that plants can

activate different defence pathways involving different regu-

lators, depending on the types of infection (Ton et al., 2002).

The ethylene (ET)- and jasmonic acid (JA)-dependent

defence responses seem to be activated by necrotrophic

pathogens (Lecourieux-Ouaked et al., 2000), whereas the

SA-dependent response is triggered by biotrophic pathogens(Thomma et al., 2001). Some studies indicate that ET or JA

and salicylic acid (SA) responses inhibit each other,

suggesting that cross-talk exists between the pathways,

enabling the plant to adapt the response depending on the

type of pathogen (Spoel et al., 2003). Genetic studies in

Arabidopsis have made it possible to identify numerous

genes involved in both pathways and how they may be

interconnected (Lorrain et al., 2003). Prxs are frequentlyresponsive to SA, JA or ET (El-Sayed and Verpoorte,

2004), and it is widely known that Prxs play a central role in

host plant defences against necrotrophic or biotrophic

pathogens (van Loon et al., 2006). The present review

focuses on the orchestrated plant defence reactions in which

Prxs are directly or indirectly involved, and ends with the

signalling pathways, which regulate Prx gene expression

during host plant defence.

Class III plant peroxidases: an overview

Among the proteins induced during plant defence and playinga key role in several metabolic responses, class III plant

peroxidases (EC 1.11.1.7) are well known. In the literature,

various abbreviations are used for class III plant peroxidases

(POD, POX, Prx, Px, and PER) but, in accordance with gene

annotations, the use of Prxs appears to be the most common

choice. They are members of a large multigenic family, with

138 members in rice (Passardi et al., 2004a) and 73 members

in Arabidopsis (Welinder et al., 2002). Prxs are involved ina broad range of physiological processes throughout the

plant life cycle (Fig. 1), probably due to the high number of

enzymatic isoforms (isoenzymes) and to the versatility of

their enzyme-catalysed reactions (Passardi et al., 2005). Thus,

plant Prxs are involved in auxin metabolism, lignin and

suberin formation, cross-linking of cell wall components,

phytoalexin synthesis, and the metabolism of ROS and RNS.

Plant Prxs are haem-containing enzymes which catalysethe single one-electron oxidation of several substrates at the

expense of H2O2:

2RHþ H2O2/2Rdþ2H2O

They are widely distributed in the plant kingdom, andhave been reported in Chlorophyta, Euglenophyta,Rhodophyta, Byophyta, Pteridophyta, and all the Sper-matophyta studied so far (Passardi et al., 2007).Among the haem-containing Prxs present in eukaryotes

and prokaryotes, class III plant Prxs are grouped in

a superfamily along with fungal and bacterial Prxs, while

animal Prxs constitute a structurally unrelated superfamily

(Welinder, 1992). Within the superfamily of plant, fungal,

and bacterial Prxs, three distantly related structural classeshave been defined (Welinder, 1992). Class I, to which

Fig. 1. Overview of the specific roles of plant Prxs in defence reactions.

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chloroplast and cytosol ascorbate Prxs from higher plants

and bacterial Prx also belong is composed of mitochondrial

yeast cytochrome c Prx. Within class II are grouped all

secretory fungal (manganese) Prxs, while class III contains

all the secretory plant Prxs which show distinctive features

from other plant Prxs, such as ascorbate Prxs.

Prxs (class III) are of a glycoprotein nature, and are

located in vacuoles and cell walls (Passardi et al., 2005).They show a broad range in their substrate requirements

with a moderate but noticeable substrate specificity for

phenols, especially for coniferyl alcohol (Morales and Ros

Barcelo, 1997), and an unusual degree of thermal stability;

all of which distinguishes them from plant ascorbate Prxs

(class I), which are not glycoproteins, and are located in

chloroplasts, mitochondria, peroxysomes, and the cytosol,

where they show moderate substrate specificity for ascorbicacid (Jimenez et al., 1998).

Secretory plant Prxs usually show a molecular mass in the

30–45 kDa range, and contain protohaemin IX (haem b) as

the prosthetic group, as well as two structural Ca2+ ions. In

their resting state (FeIII), an iron ion is present in the

oxidation state of +3. The iron is five co-ordinated to the

four pyrrole nitrogens of the haem and to nitrogen from an

axial (proximal) histidine. The sixth co-ordination positionis free, thus determining a high spin state for the iron

(Banci, 1997). Crystallographic analysis and modelling

studies (Ros Barcelo et al., 2007) reveal that class III plant

Prxs usually contain 10–12 conserved a-helices embedding

the prosthetic group, 2 short b-strands, and four conserved

disulphide bridges.

Prxs as pathogenesis-related (PR) proteins

PR proteins are coded by host plants as a response to

pathological or related situations, and normally accumulate

not only locally in the place of infection, but are also

formed systemically following any kind of infection (Schereret al., 2005). The term PRs is a collective term for all

microbe-induced proteins and their homologues to the

extent that enzymes such as phenylalanine ammonia-lyase,

Prxs, and polyphenoloxidase, which are generally present

constitutively and only increase during most infections, are

often also referred to as PRs (van Loon et al., 2006).

The PR protein family includes all pathogen-induced

proteins and their homologues, and are routinely classifiedinto 17 subfamilies based on their biochemical and molec-

ular biological properties (van Loon et al., 2006). Most of

the PR proteins are induced through the action of several

endogenous growth hormones, including SA, JA, and ET,

whose levels are also increased in infected tissues (Durrant

and Dong, 2004). In Arabidopsis, it has been shown that SA

and JA activate distinct sets of PR genes in an antagonistic

pattern (Thomma et al., 1998). In addition, PR genes aredifferentially regulated by plant growth hormones, includ-

ing SA, ABA, JA, ET, and brassinosteroids, and by diverse

abiotic stresses, supporting the contention that the PR

proteins play a role in plant developmental processes other

than disease resistance responses (Seo et al., 2008).

Prxs are a well-known class of PR proteins, and so they

are induced in host plant tissues by pathogen infection.

They belong to the PR-protein 9 subfamily (van Loon et al.,

2006), and are expressed to limit cellular spreading of the

infection through the establishment of structural barriers or

the generation of highly toxic environments by massively

producing ROS and RNS (Passardi et al., 2005). Prxs

activity or Prxs gene expression in higher plants is, indeed,induced by fungi (Sasaki et al., 2004), bacteria (Young

et al., 1995; Lavania et al., 2006), viruses (Lagrimini and

Rothstein, 1987; Hiraga et al., 2000; Dıaz-Vivancos et al.,

2006), and viroids (Vera et al., 1993). The biotic or abiotic

stress-induced expression of Prxs is conferred by the nature

of the 5’ flanking regions of the genes that contain many

kinds of potential stress-responsive cis-elements (Sasaki

et al., 2007).

Prxs and the reinforcement of the cell walls

Prxs can create a physical barrier to limit pathogen invasion

in host tissues by catalysing the cross-linking of cell wall

components in response to different stimuli such as wound-

ing and pathogen interactions and thus, cell wall rigid-

ification is, in most cases, the result of the Prxs-mediated

H2O2-dependent cross-linking of cell wall components.The irreversible process of cell wall stiffening may either

be dependent or independent of the cell type. Thus, extensin

and ferulic acid cross-linking may constitute temporal and

transitory events within the general programme of de-

velopment of any host plant cell, while lignification and

suberization are terminal processes of determinate and

highly differentiated plant cells capable of forming second-

ary cell walls. In the case of lignification, this process isrestricted to water-conducting vascular cells and their

neighbouring fibres (Ros Barcelo, 1997), while suberization

is restricted to the cell wall of epidermal tissues of un-

derground plant parts (roots, stolons, and tubers), the

endodermis, and the cells of bark tissues (cork and

periderm) (Bernards et al., 2004). In either case, lignification

and suberization have the hallmark of being highly tissue/

cell specific. Indeed, cells that finally become suberized orlignified either derive from specific progenitor cells in

meristems or arise from the vascular cambium, respectively.

Extensin cross-linking

Extensins are the most studied family of hydroxy-proline

(Hyp)-rich proteins (HRGPs). The polypeptide backbone of

extensins contains many repeats of the structural Ser(Hyp)4–

6 motif. These structural motifs are often flanked by short

sequences rich in Tyr, Lys, Val, and His, the Val-Tyr-Lys

motifs being the sites for extensin cross-linking (Fry, 2004b).

Extensins are secreted into the apoplast as soluble mono-mers where the positively charged Lys and the protonated

His residues interact ionically with the negatively charged

uronic acids of pectins. The formation of the insoluble

extensin network is a well-characterized Prxs-mediated and

H2O2-dependent process, which, it has been proposed (Fry,

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2004b), involves the coupling of extensin Tyr residues to

form isodityrosine linkages and larger Tyr oligomers such

as di-isodityrosine or pulcherosine. The interaction of Prxs

with extensins also has a defence function since it makes the

cell wall harder to penetrate. The common relationship

between extensins and Prxs could be the pectin layer.

Indeed, some Prxs can bind to calcium–pectate complexes

(Shah et al., 2004), and there is growing evidence thatcovalent bonds exist between pectins and extensins. Pectins

would act as an anchor for Prxs, which would then cross-

link extensins to create a dense and solid network in the

host plant cell wall, with the aim of limiting pathogen

colonization (Passardi et al., 2004b).

Ferulic acid cross-linking

Ferulic acid is ester-bonded to cell wall polysaccharides

(Ralph et al., 2004a). In dicots, non-reducing terminalarabinose (Ara) and galactose residues of pectic polysac-

charides are feruloylated, while in monocots feruloylation is

mainly restricted to the O-5 position of some Ara residues

of arabinoxylans (Fry, 2004a). Feruloyl residues can form

covalent bonds with each other by oxidative coupling. This

process only occurs in the presence of Prx and H2O2 and it

has been speculated (Ralph et al., 2004a) that the resulting

dehydrodiferuloyl residue (5,5#-dehydrodiferulate) formsa cross-link between the polysaccharides to which it is

esterified.

In addition to the first-discovered dimer, 5,5#-dehydrodi-ferulate, several of its isomers have been obtained by alkaline

hydrolysis of plant cell wall polysaccharides; and several

specific trimers and tetramers have now been characterized

(Ralph et al., 2004a). Depending on the linkage formed

(intra- or inter-polysaccharide), up to four polysaccharidechains could potentially be cross-linked by a tetramer of

ferulic acid, which suggests that these Prx-mediated oxida-

tively generated oligomers of ferulate may play an important

role in determining cell wall assembly and cell wall suscepti-

bility to digestion (Grabber et al., 1998).

Lignification

Lignins are three-dimensional, amorphous, heteropolymers

which result from the oxidative coupling of three p-

hydroxycinnamyl alcohols (monolignols): p-coumaryl, con-

iferyl, and sinapyl alcohols, in a H2O2-dependent reactionmediated by Prxs, enzymes which generate the corresponding

free radicals from the three monolignols (Ros Barcelo, 1997).

The regio- and stereospecificity of the cross-coupling reaction

of monolignol radicals produces a hydrophobic heteropoly-

mer composed of p-hydroxyphenyl, guaiacyl, and syringyl

units, respectively. Both the chemistry and biochemistry of

the lignification have recently been revised (Ralph et al.,

2004b), as well as the nature of the Prx responsible for thisprocess (Ros Barcelo et al., 2007). Although lignification is

a structural barrier restricted to vascular tissues, xylem cell

wall lignification may be especially important during the

defence of plants against soil-borne pathogens which cause

vascular wilts (Pomar et al., 2004).

The cross-linking of the phenolic monomers in the

oxidative coupling of lignin subunits has been associated

with Prxs using H2O2 as the oxidant. Acidic and basic Prxs

are capable of oxidizing p-coumaryl and coniferyl alcohol.

However, this situation is not so clear in the case of sinapyl

alcohol, which possesses a syringyl moiety; for this reason

typical acidic Prxs, with some exceptions (Christensen et al.,

1998), are generally regarded as poor catalysts (Bernardset al., 1999). This observation constitutes a central key for

the unravelling specificity of lignin assembly since sinapyl

alcohol is more prone to oxidation than either coniferyl

alcohol or p-coumaryl alcohol (Kobayashi et al., 2005), and

suggests that, although Prx-catalysed reactions are driven

by redox thermodynamic forces (Ros Barcelo et al., 2004),

substrate accommodation in the catalytic centre of the

enzyme determines the real role played by each Prxisoenzyme in lignin biosynthesis (Kobayashi et al., 2005;

Ros Barcelo et al., 2007).

Lignification is an H2O2-dependent Prx-mediated process

(Czaninski et al., 1993; Olson and Varner, 1993; Ros

Barcelo, 1998a; Weir et al., 2005), in which the H2O2

necessary for the peroxidative oxidation of monolignols

comes from a diphenylene iodonium (DPI)-sensitive

NADPH oxidase-like enzyme (Ogawa et al., 1997; RosBarcelo, 1998b, 1999; Karlsson et al., 2005), which gener-

ates Od

2 . This Od

2 then dismutates to H2O2 by a tissue-

specific CuZn-SOD (Ogawa et al., 1997; Karlsson et al.,

2005; Srivastava et al., 2007) or, alternatively, by an Mn-

SOD (Corpas et al., 2006).

Suberization

Both lignification and suberization involve the formation of

a three-dimensional poly(phenolic) matrix initially within

the carbohydrate matrix of the primary cell wall (Keren-

Keiserman et al., 2004). In addition to this phenolic

component, suberized cells develop a distinct poly(aliphatic)layer described (Bernards et al., 2004) as a polyester

connected through primary ester bonds between the major

aliphatic components (a,x-dioic acids and x-hydroxyalka-noic acids), in close association with p-hydroxycinnamic

acids, such as p-coumaric, caffeic, and ferulic acids, which

constitute the cell wall-bound poly(phenolic) domain

(PPD). The macromolecular assembly of potato PPD

occurs via a H2O2-dependent Prx-mediated free radicalcoupling process (Bernards et al., 2004), analogous to the

process of lignin formation from monolignols, but this

enzyme shows a marked substrate preference for p-hydroxy-

cinnamates (i.e. ferulic acid and derivatives).

Suberization is an H2O2-dependent Prx-mediated process,

in which the H2O2 necessary for the peroxidative oxidation

of phenolics also comes from a DPI-sensitive NADPH

oxidase-like enzyme (Razem and Bernards, 2003; Bernardset al., 2004), similar to that occurring during lignification

(Ros Barcelo, 1998b). In fact, a potato NADPH-oxidase

homologue (StrbohA) has recently been implicated

(Kumar et al., 2007) in the generation of H2O2 during

suberization.



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Prxs and the metabolism of ROS and RNS

ROS in plant defence responses

One significant event in plant defence reactions is the

oxidative burst, a common early response of host plant cells

to pathogen attack and elicitor treatment. ROS (Od

2 , H2O2,

and OHd

), predominantly Od

2 and H2O2, are toxic intermedi-

ates resulting from the successive one-step reduction of O2 to

H2O. Four possible mechanisms have been proposed to

explain how ROS are produced in host plant cells: one is

located at the level of the external face of the plasma

membrane, and is mediated by NADPH oxidases (Desikan

et al., 1996), and three are located at the level of the cell wall

matrix, and which would involve the action of Prxs (Bolwell

et al., 2002; Kawano, 2003; Choi et al., 2007), poly(di)amine

oxidases (Angelini and Federico, 1989) and oxalate oxidases

(Lane, 1994). Unlike poly(di)amine oxidases and oxalate

oxidases, which directly generate H2O2, both NADPH

oxidases and Prxs catalyse the initial formation of Od

2 , which

later dismutates to H2O2. The Prx-mediated Od

2 production

may be distinguished from that catalysed by NADPH-

oxidase by the different Km values for O2 and the different

sensitivities of the two enzymes to inhibitors such as cyanide,

azide, and DPI (Bolwell et al., 1998). However, caution

should be exercised in the use of these inhibitors (Frahry

and Schopfer, 1998; Ros Barcelo, 1998b; Ros Barcelo and

Ferrer, 1999).

Recent studies have identified plant respiratory burst

oxidase homologues (rboh) as the main source of ROS

during the apoplastic oxidative burst (Overmyer et al.,

2003), although a role for Prxs has been also proposed

(Bolwell et al., 2002). The relative importance of both

systems can be clearly seen from the following example.

Tobacco cells that had been transformed with an antisense

construct of NtrbohD no longer produced ROS (Simon-Plas

et al., 2002) after treatment with cryptogein, an elicitor of

defence responses. Likewise, Ntrboh-silenced tobacco plants

had a reduced oxidative burst and a reduced disease

resistance to Phytophthora infestans (Yoshioka et al., 2003).

Whatever the source of ROS, H2O2 acts as a signal

molecule to induce an array of molecular, biochemical, and

physiological responses in plant cells (Neill et al., 2002).

Certainly, H2O2 is able to initiate the octadecanoid pathway

leading to the biosynthesis of JA, JA-related compounds,

and other oxylipins which have been reported to function as

inducers of plant secondary metabolites biosynthesis

(Thomma et al., 2001). Given that H2O2 is produced in

response to a wide variety of abiotic and biotic stimuli, it is

likely that H2O2 mediates the cross-talk between signalling

pathways and is a signalling molecule contributing to cross-

tolerance; that is, the exposure of plants to one stress

confers protection towards others (Bowler and Fluhr, 2000).

Moreover, it may be that cellular responses to H2O2 differ

according to their site of synthesis or perception (Neill

et al., 2002). Kacperska (2004) has suggested that the role of

ROS and H2O2 in the mediation of stress responses may

depend on the severity of the stressor.

This implies that, rather than sensor type, the quantita-

tive effects of the sensor-initiated modifications in the

oxidant-antioxidant activities in different cell compartments

may be responsible for the different effects of a particular

stressor. This suggestion is in line with observations that

small increases of H2O2 allow the general enhancement of

stress tolerance; whereas large increases in H2O2 trigger

local responses that unavoidably lead to programmed celldeath (PCD). In fact, H2O2 has been shown to be

a diffusible signal mediating localized PCD during HR

(Levine et al., 1996), as well as being involved in a systemic

signalling network (Alvarez et al., 1998). Mittler et al.

(1999) using transgenic catalase/Prx-deficient tobacco plants

showed that these were hyper-responsive to pathogen

challenge, thus providing direct evidence for a role for

H2O2 in HR cell death. Within this context, Neill et al.

(2002), using Arabidopsis suspension cell cultures to eluci-

date the role of H2O2 as a signalling molecule, showed that

H2O2 is generated following elicitor and pathogen challenge

and that this H2O2 acts as a signal to induce PCD and

defence gene expression (Desikan et al., 2000). PCD in-

duced by H2O2 during the HR in Arabidopsis (Desikan

et al., 1998) and soybean (Solomon et al., 1999) requires

transcription and translation, and several studies havedemonstrated that H2O2 modulates gene expression during

defence responses (Levine et al., 1994; Desikan et al., 1998).

Prxs may transitorily deliver ROS

Although the key function of plant Prxs is to oxidize

phenolic substrates at the expense of H2O2, Prxs may,

paradoxically and transitorily, generate Od

2 /H2O2 through

two mechanisms. The first mechanism is restricted to the

Od

2 /H2O2 generating step of plant Prxs during their

catalytic cycle, which is represented by the decay of

Compound III (CIII) into FeIII (Fig. 2A). This reaction

most likely involves the dissociation of a (FeIII)- Od

2

complex and yields the FeIII form of the enzyme and Od

2 ,

which may further dismutate to H2O2, either chemically

or enzymatically. However, the kdecay of CIII into FeIII is

very slow, and it is unlikely to be responsible for noticeable

Od

2 /H2O2 production such as that observed during the

oxidative burst. Thus, early kinetic studies (Yamazaki and

Yokota, 1973) suggested even that the main way for CIII

decay is its auto-decomposition and that this elapses with nonet Od

2 /H2O2 production (Fig. 2B).

The second mechanism involves the oxidation through

a Prx cycle of a suitable reductor (i.e., a thiol [RSH]) to its

corresponding radical ([RSSR]d�) (Fig. 3), which further

reacts with O2 through a reaction of mediation redox, to

give Od

2 (Burner and Obinger, 1997). However, caution

should be exercised when considering Prx as a possible

enzyme responsible for Od

2 /H2O2 production since theoverall balance of these oxidase/Prx reactions in a closed

system is non-net Od

2 /H2O2 production (Fig. 3).

The overall balance of the reactions depicted in Fig. 3,

however, does not exclude the possibility that, in these

enzymatic reactions, (i) both Od

2 and H2O2 can be



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transitorily formed while [RSSR]d�

is not totally consumed,

(ii) Od

2 and H2O2 can be detected by fast trapping agents,

and (iii) the overall reaction is inhibited by both superoxide

dismutase and catalase.

Furthermore, due to the fact that compound I (CI) and

compound II (CII) are continuously generated and broken

during these oxidase/Prx cycles (Figs 2, 3), the introduction

in the bulk of the reactions of a phenolic compound, whichmay act as substrate for CI and CII, would result in the

oxidation of the phenolic to its corresponding radical,

which would then undergo polymerization reactions. This

is what occurs when either a lignin precursor (e.g. coniferyl

alcohol) (Ferrer et al., 1990), or soluble cell wall proteins

(Wojtaszek et al., 1997), are introduced in the bulk of the

oxidase/Prx reaction. All these contraints mean that Prxs

are mainly considered to be merely ROS-detoxifying

enzymes (Zhao et al., 2005).

However, not all Prx-mediated ROS-production reactions

deliver Od

2 /H2O2. It has been proposed (Fry, 1998) that

plant cell wall polysaccharides may be subjected in vivo to

non-enzymatic scission mediated by hydroxyl radicals

(OHd

), and it is probable that microbial polysaccharides arealso targets of OH

d

, and so the OHd

produced by host plant

cells may provoke microbial cell wall polysaccharide

scission as a fine defence mechanism against pathogens.

OHd

can be generated from H2O2 in the host plant cell wall

by Prxs (Liszkay et al., 2003) from Od

2 and H2O2 through

a Haber–Weiss-type reaction:

Od

2 þ FeIII/O2þFeII

2Od

2 þ2Hþ/H2O2þO2

FeIIþ H2O2/FeIIIþ OHdþOH�

Although OHd

is exceedingly reactive, if its production is

controlled, for example, by the correct siting of Prx relative

to microbial polysaccharide molecules, OHd

could be very

precisely targeted to cause microbial polysaccharide scission.

How this might be achieved has yet to be determined.

Evidence for OHd

-induced polysaccharide splitting in plant

cell walls has been obtained by finding the predicted productsof OH

d

action on polysaccharides (Fry, 1998); however,

evidence for such products has not been found from either

plant cell walls or microbial cell walls.

All these results suggest that host plant cells, by means of

Prxs, may generate ROS. However, the dichotomy of the

Prx-mediated ROS production, especially as regards the fate

of H2O2, Od

2 , and OHd

in plant defence reactions, is

apparently far from being completely understood (Passardiet al., 2004b).

RNS in plant defence responses

NOd

is a relatively stable paramagnetic free-radical mole-

cule involved in many physiological processes in plants,

where it serves as a synchronizing chemical messenger

involved in cytotoxicity and PCD (Van Camp et al., 1998;

Durner and Klessig, 1999; Neill et al., 2003). In animal cells,most of the biological regulatory properties of NO

d

have

been explained on the basis of its capacity to act as an iron

ligand in haemproteins (Tsai, 1994). Dual (activating or

inhibitory) effects of NOd

on haemproteins have been

described (Tsai, 1994), and the nature of the effect seems to

depend to a great extent on the resting state (oxidation

state) of the haemprotein, which conditions the ligand

properties and the electronic configuration of the haem iron(Tsai, 1994).

It is now clear that NOd

and, in general, most of the RNS

(NOd

, NO+, NO–, NOd

2, and ONOO–), are major signalling

molecules in plants (Durner and Klessig, 1999) which can be

synthesized during stress responses at the same time as H2O2.

Fig. 3. Catalytic cycle of Prxs in the presence of thiols, showing

the inter-conversion between the resting state (FeIII), and the

activated forms, compound I (CoI) and compound II (CoII). Kinetic

constants are taken from Yokota and Yamazaki (1973) and Burner

and Obinger (1997). The balance of the reaction is put in a frame.

Fig. 2. Pathways of compound III (CIII) formation (A) and CIII auto-

decomposition (B) of Prxs, showing the resting state of the enzyme

(FeIII), its reduced form (FeII), and the activated forms, compound I

(CI) and compound II (CII). Kinetic constants are taken from Yokota

and Yamazaki (1973). The balance of the reaction is put in a frame.



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Two landmark publications have demonstrated the role of

NOd

during the HR to infection by bacteria and viruses

(Delledonne et al., 1998; Durner et al., 1998), NO being part

of the intracellular signalling cascade is activated in plant

cells in response to pathogens or elicitors (Garcıa-Brugger

et al., 2006). At the transcriptional level, microarray and

cDNA-AFLP data obtained from NOd

donor-treated Arabi-

dopsis cells indicate that NOd

modulates the expression ofseveral defence genes, including genes encoding PR proteins

and proteins related to secondary metabolism (Polverari

et al., 2003; Parani et al., 2004).

RNS, generated together with H2O2 in response to pathogen

attack, was found to mediate defence responses similar to

those seen following H2O2 generation. Thus, stress responses

may reflect responses to both H2O2 and RNS. In fact,

bacteria-induced PCD has been reported to involve both ofthese signals in soybean (Delledonne et al., 1998) and in

Arabidopsis (Clarke et al., 2000), although the effects of RNS

and H2O2 were synergistic in the former, while in the latter,

they were additive. As discussed above, H2O2 formation may

transit via an Od

2 intermediate. It is then possible that NOd

,

a free radical itself, may react with Od

2 to form the highly

reactive peroxynitrite anion, ONOO–, and subsequent cellular

effects may then be induced by ONOO–. In this context, it isnoteworthy that NO

d

and H2O2 might control each other’s

synthesis. Thus, exogenously applied H2O2 has been found to

trigger NO production in mung bean through a Ca2+ influx-

dependent process (Lum et al., 2002), and it has recently been

reported that NOd

is required for the activation of plasma

membrane NADPH oxidases (Vandelle et al., 2006). There are

also some controversial reports on NOd

cross-talk with ROS

in host plant defence responses: for example, it appears thatRNS works collaboratively with ROS in many cases (Delle-

donne et al., 1998), while in other cases RNS acts antagonis-

tically (Neill et al., 2002).

Prxs may participate in the metabolism of RNS

It has long been known that NOd

reversibly binds to the haem

prosthetic group of plant Prxs (Yonetani et al., 1972; Ascenzi

et al., 1989). Optical and electron paramagnetic resonance(EPR) studies suggest that, once the complex is formed,

a one electron transfer between NOd

and the protoporphyrin

IX prosthetic group of Prxs takes place, which results in the

formation of spin-paired complexes (Yonetani et al., 1972).

The binding of NOd

to plant Prxs results in spectrally distinct

complexes (Yonetani et al., 1972), in which the Soret peak at

405 nm shifted to 419 nm, and the a and b-absorption bands

at 495 nm and 636 nm shifted to 533 nm and 568 nm,respectively. The shapes and positions of these bands are

typical of low spin ferrous [Fe(II)] Prxs. Kinetic analyses

using flash photolysis and stopped-flow methods (Kobayashi

et al., 1982) have revealed a reaction constant (k) of 1.93105

M�1 s�1. The formation of these ferrous nitrosyl complexes

[Fe(II)NO+] removes enzyme turnover intermediates such as

the resting form, Fe(III):

FeðIIIÞ þ NOd/FeðIIIÞNO4FeðIIÞNOþ

so that NOd is capable of inhibiting Prx-catalysedreactions with Ki in the lM range (Ischiropoulos et al.,1996; Ferrer and Ros Barcelo, 1999), especially when Prxis working with physiological substrates, such as con-iferyl alcohol.

NOd

may also be regarded as a Prx substrate (Glover et al.,

1999), and therefore Prx could play any role in NO

detoxification in plant tissues. In fact, NO reacts with CI

with a rate constant (k2) of 7.03105 M�1 s�1 yielding thenitrosyl species, NO+. NO

d

also reacts with CII with a rate

constant (k3) of 1.33106 M�1 s�1 to lead probably to the

nitrite anion, NO2. Interestingly, the reaction of CII with

NOd

is unusually high relative to that of CI, which is usually

the faster reaction. This means that, in the presence of poor

electron donors of CII, such as catechols (Nappi and Vass,

2001) or guaiacol (Uchida et al., 2002; Hung et al., 2002),

which show k3 values ;102 M�1 s�1 and ;105 M�1 s�1,respectively (Yamazaki and Yokota, 1973), NO

d

may

enhance Prx activity by promoting the formation of the

native enzyme, FeIII, from CII. Thus, both activating and

inhibitory effects of NOd

on Prx could be observed, depend-

ing on the environment in which the enzyme is located.

The product of NOd

oxidation by CII of Prx is apparently

NO2, which can be further oxidized by plant Prxs to lead to

the most likely form, NOd

2 (Shibata et al., 1995; van derVliet et al., 1997). Plant Prxs are also capable of oxidizing

the Tyr contained in proteins to Tyr radicals (Tyrd

), which

combine with another Tyrd

to form dityrosine (Michon

et al., 1997). When the oxidation of Tyr by plant Prxs is

carried out in the presence of NO2, a mixture of Tyrd

and

NOd

2 is formed in the reaction medium, species that couple

to yield 3-nitro-tyrosine (van der Vliet et al., 1997). 3-Nitro-

tyrosine is a well-established marker of oxidative proteindamage in mammals (van der Vliet et al., 1997), and

evidence for this has recently been reported in plant tissues

(Romero-Puertas et al., 2007).

As discussed above, during pathogen attack, host plant

tissues are capable of sustaining both NOd

and Od

2 pro-

duction. Therefore, it is likely that in diseased tissues both

NO and Od

2 will react to lead to ONOO–:

NOd þ Od

2 /ONOO

ONOO– is formed at a near difusion controlled rate

(k¼6.73109 M�1 s�1), and it has been postulated that it

plays a major role in cytotoxicity (Gabaldon et al., 2005),

including PCD (Delledonne et al., 2001; Wendehenne et al.,2001), although its real role in living cells remains unclear

(Fukuto and Ignarro, 1997). Independently of their real role

in plant cells, which remains to be clearly established,

ONOO– may be regarded as a substrate of plant Prxs (Floris

et al., 1993; Gebicka and Gebicki, 2000). In fact, ONOO–

reacts (k¼33106 M�1 s�1) with the resting form of the

enzyme to lead to CII (Floris et al., 1993):

FeðIIIÞ þ ONOO /CIIþ NOd

2

yielding the nitrosylating species, NOd

2. CII is catalyticallyinactive towards ONOO–, and the decay of CII to the



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native enzyme, Fe(III), only takes place in the presence ofan external electron donor, such as a phenol. In sucha scenario, a role in the scavenging of ONOO– has beenproposed for the chlorogenic acid/Prx system (Grace et al.,1998), which may be functional with any other phenol.

Prx is not only involved in the detoxification of NO

species and relatives, but it may also participate in bio-mimetic NO-synthesizing pathways. One of the possible

enzymes involved in NO synthesis in plant cells is NO

synthase (NOS) (Wendehenne et al., 2001). NOS catalyses

the conversion of L-arginine in L-citrulline yielding NOd

.

In this reaction, N-hydroxy-L-arginine, an N-hydroxy-

guanidine, acts as key intermediate. N-hydroxyguanidines,

including N-hydroxy-L-arginine, may be oxidized by plant

Prxs to release NOd

, yielding the same products as thoseobtained with NOS (Xian et al., 2001; Cai et al., 2002). The

ability of plant Prxs to synthesize NOd

is not restricted to

the course of the oxidation of N-hydroxyguanidines, since

the oxidation of N-hydroxy-N-nitrosamines (Alston et al.,

1985), such as cupferron, a xenobiotic, or alanosine (a

natural antineoplastic drug closely related to aspartic acid),

also yields NOd

as a collateral product of the reaction.

Prxs and the production of anti-microbialmetabolites

Plant Prxs are able to catalyse the synthesis of bioactive

plant products (Ros Barcelo and Pomar, 2002), andtherefore a role in plant defence through their involvement

in the synthesis of phytoalexins has been proposed for these

enzymes. Thus, viniferins (stilbene phytoalexins in Vitis

spp.), hordatines (dimers of p-coumaryl-agmatine and p-

coumaryl-hydroxy-agmatine in Hordeum spp.), and certain

lignans/neo-lignans (dimers and oligomers of monolignols

and p-hydroxy-cinnamic acids) are well known bioactive

(anti-fungal) products resulting from Prx-mediated reac-tions, and their significance in vivo has been addressed

several times (Langcake and Pryce, 1977a, b;Langcake,

1981; Waffo-Teguo et al., 2001; Ros Barcelo and Pomar,

2002).

The list of bioactive (anti-fungal and anti-bacterial)

products resulting from Prx-mediated reactions is continu-

ously growing, as is illustrated by the following examples.

After infection with pathogenic fungi, oat (Avena sativa)leaves produce the phenolic phytoalexins, avenanthramides,

which are a series of p-hydroxycinnamic amides of

p-hydroxyanthranilates. Okazaki et al. (2004), investigating

the biosynthesis of avenanthramides, identified a dimeric

compound of avenanthramide B in elicited oat leaves. In

a recent study, Okazaki et al. (2007) reported the structure

of five novel dimers, named bisavenanthramides B1–B6,

which exclusively result from Prx-mediated reactions.The involvement of Prx in the metabolism of other

phytoalexins has also been inferred through accumulated

evidence. In Medicago truncatula cell suspension cultures,

the isoflavonoid-derived daidzein dimer was found to

accumulate extracellularly exclusively in response to a yeast

elicitor (Farag et al., 2008), and it is well-known that

isoflavonoid dimers lacking o-catechol substructures may

only arise from Prx-catalysed oxidations (Ros Barcelo and

Pomar, 2002). In white lupin (Lupinus albus), lupinalbisone

A and B, two biflavonoids derived from 2#-hydroxygenistein,are well-known products of the Prx-catalysed oxidation of

2#-hydroxygenistein, which show increased antifungal activ-

ity (Sakasai et al., 2000).Prxs are also involved in the biosynthesis of secondary

metabolites with not well-understood functions in plants,

but instead have recognized medicinal properties. This is the

case of the terpenoid indole alkaloids of Catharanthus

roseus (Sottomayor et al., 2004). In this plant, a basic Prx

was shown to be responsible for the dimerization reaction

between catharantine and vindoline to produce a-3#,4#-anhydrovinblastine (Costa et al., 2008), the major alkaloidpresent in C. roseus leaves, and the precursor of the natural

antitumoral products, vinblastine and vincristine.

Signalling pathways in the regulation of Prxs

SA-mediated defences

SA has long been known to play a central role in plant

defence reactions. SA levels increase in plant tissue follow-

ing pathogen infection, and exogenous application of SA

results in enhanced resistance to a broad range of pathogens

(Ryals et al., 1996). Genetic studies have shown that SA isrequired for the rapid activation of defence responses that

are mediated by several resistance genes, for the induction

of local defences that contain the growth of virulent

pathogens, and for the establishment of systemic acquired

resistance (SAR) (Chen et al., 1993; Rao et al., 1997). SAR

is a state of heightened defence that is activated throughout

the plant following primary infection by pathogens that

elicit tissue damage at the site of infection (Ryals et al.,1996). Several PR genes whose expression is SA-dependent

are commonly used as reporters of SA-dependent defences.

In this context, a great number of class III plant Prxs are

generally induced by SA (Rasmussen et al., 1995; Rao et al.,

1997; Martınez et al., 2000; Fernandes et al., 2006), but this

behaviour is not universal since some Prxs are not re-

sponsive to SA (Ward et al., 1991; Hiraga et al., 2000). This

SA-sensitivity probably marks the frontier line between Prxsinvolved in plant defence reactions and Prxs involved in

other aspects of the plant cell metabolism.

The interaction between SA and Prxs not only covers

those aspects related to gene regulation, but SA may

also interfere positively or negatively in Prx-mediated

metabolic pathways. It has been proposed that the SA

signal transduction pathway leading to SAR may be

mediated by increased ROS levels, since SA binds andinhibits catalase as well as Prxs (Chen et al., 1993; Ruffer

et al., 1995). The inhibition of Prxs by SA is probably due

to the fact that SA may act as a kinetic inhibitor of the

enzyme since, on the one hand, SA is a substrate, although

a weak one, of CII (Kawano et al., 2002a) and, on the other



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hand, SA favours the irreversible inactivation of the enzyme

(Kawano et al., 2002b), blocking all those Prx-mediated

reactions which consume H2O2. The mechanism of SA

action on Prxs, however, is apparently more complex.

Kawano et al. (2004) have suggested a series of reactions

for the generation of Od

2 during the Prx catalytic cycle, in

which SA could act as e– donor for Prx, generating SA

radicals (SAd

). SAd

could thus generate Od

2 by means ofa reaction of mediation redox, such as that described in Fig.

3 for [RSSR]d�. Evidence supporting the production of SA

d

by Prxs has been obtained by electron spin resonance (ESR)

studies (Kawano and Muto, 2000). In such a scenario, it has

been proposed that the mechanism for the SA-dependent

early ROS production solely depends on the interaction of

SA with Prx (Kawano and Muto, 2000), whereas the

involvement of NADPH oxidase in the later stages of SAaction acquires a major role since this requires the SA-

induced NADPH oxidase gene expression (Yoshioka et al.,

2001, 2003).

JA-dependent and ET-dependent defences

JA, and its more permeable derivative, methyljasmonate

(MeJA), have been proposed as key compounds of the

signal transduction pathway involved in the elicitation of

plant defence reactions (Farmer et al., 2003). Consistent

with the notion of Prxs participating in plant defence

responses, JA and MeJA positively regulate Prx gene

expression (Repka et al., 2004; Ali et al., 2006; Kumariet al., 2006), but cross-talks between JA and SA in the

regulation of Prxs have not been established.

Unlike SA and JA, ET is a phytohormone that regulates

a wide range of plant processes from growth and de-

velopment to defence responses. ET production can be

induced by various stresses such as wounding, microbial

pathogen and insect attack, as well as small elicitors.

However, the role of ET in plant defence is controversial asit contributes to resistance in some interactions (Norman-

Setterblad et al., 2000; Thomma et al., 1999), but promotes

disease in others (Bent et al., 1992; Lund et al., 1998;

Hoffman et al., 1999). The behaviour of Prx in these

systems has not been studied. However, in others, ET

promotes Prx activity and Prx gene expression, with the de

novo expression, although not always of novel Prx iso-

enzymes (Abeles et al., 1989; Morgens et al., 1990; Ishigeet al., 1993).

The interaction of JA and ET signalling pathways is one

of the most significant interactions known, and it influences

many aspects of plant development and defence responses.

JA signalling can lead to ET production in host plants,

while ET apparently stimulates JA production (Xu et al.,

1994; Mirjalili and Linden, 1996; Zhao et al., 2004). In

many cases, JA and ET co-operatively regulate defenceresponses. Evidence that JA and ET co-ordinately regulate

defence-related genes has been obtained in A. thaliana from

microarray experiments that monitored gene expression in

response to various defence-related stimuli (Schenk et al.,

2000). These authors reported that nearly half of the genes

that were induced by ET were also induced by JA

treatment. Consistent with this notion, Prxs that apparently

participate in plant defence responses are activated by both

JA and ET (Buzi et al., 2004; Bailey et al., 2005).

The above-described results point to the possible signal-

ling pathways that regulate Prx gene expression during

plant defence. How certain Prxs have suffered the natural

selection to be responsive to biotic factors, and how thesePrxs are really integrated within the complex network of

defence responses of any host plant cell, will be the

cornerstone of future research.

Acknowledgements

L Almagro and S Belchı-Navarro hold grants from the

Fundacion Seneca. We thank Estefanıa Pedreno for revising

the English manuscript. This work has been partially

supported by the MEC and FEDER (BIO2005-00332,BFU2006-11577) and by the Consejerıa de Educacion,

Ciencia e Investigacion de la Region de Murcia (BIO BVA

07 01 0003).

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