JXB Advance Access originally published online on December 10, 2008
Journal of Experimental Botany 2009 60(2):377-390; doi:10.1093/jxb/ern277
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REVIEW-ARTICLE |
Class III peroxidases in plant defence reactions
1Department of Plant Biology, Faculty of Biology, University of Murcia, Campus de Espinardo, E-30100 Murcia, Spain
2Departamento de Agroquimica y Bioquimica, Universidad de Alicante, Campus de San Vicente del Raspeig, E-03080 Alicante, Spain
To whom correspondence should be addressed: E-mail: mpedreno{at}um.es
Received 12 August 2008; Revised 8 October 2008 Accepted 14 October 2008
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Abstract |
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 Top Abstract IntroductionClass III plant peroxidases:...Prxs and the reinforcement...Prxs and the metabolism...Prxs and the production...Signalling pathways in the...References |
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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 plant peroxidases (EC 1.11.1.7 [EC] ; 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
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Introduction |
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TopAbstractIntroductionClass III plant peroxidases:...Prxs and the reinforcement...Prxs and the metabolism...Prxs and the production...Signalling pathways in the...References |
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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 compounds which prevent colonization of the tissue. The active or induced defence responses include the hypersensitive response (HR), the production of phytoalexins and pathogenesis-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 be genetically controlled by plant resistance genes which confer resistance to pathogens with a matching avirulent (Avr) gene by specific recognition events (Zhao et al., 2005). However, triggering resistance is not always due to specific Avr products, which activate defence responses in cultivars possessing the matching resistance genes but, instead, proceeds 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 in molecules 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 (Nürnberger 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 transcriptional and metabolic changes (Zhao et al., 2005). Studies with different plant–pathogen systems have shown that plants can activate different defence pathways involving different regulators, 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 frequently responsive 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.
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Class III plant peroxidases: an overview |
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TopAbstractIntroductionClass III plant peroxidases:...Prxs and the reinforcement...Prxs and the metabolism...Prxs and the production...Signalling pathways in the...References |
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Among the proteins induced during plant defence and playing a key role in several metabolic responses, class III plant peroxidases (EC 1.11.1.7 [EC] ) 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 in a 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.
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Plant Prxs are haem-containing enzymes which catalyse the single one-electron oxidation of several substrates at the expense of H2O2:
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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 classes have been defined (Welinder, 1992). Class I, to which 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 Barceló, 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 ascorbic acid (Jiménez 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 position is free, thus determining a high spin state for the iron (Banci, 1997). Crystallographic analysis and modelling studies (Ros Barceló et al., 2007) reveal that class III plant Prxs usually contain 10–12 conserved 
-helices embedding the prosthetic group, 2 short β-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 (Scherer et 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 classified into 17 subfamilies based on their biochemical and molecular 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 are differentially regulated by plant growth hormones, including 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; Díaz-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).
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Prxs and the reinforcement of the cell walls |
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TopAbstractIntroductionClass III plant peroxidases:...Prxs and the reinforcement...Prxs and the metabolism...Prxs and the production...Signalling pathways in the...References |
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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 wounding and pathogen interactions and thus, cell wall rigidification 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 development of any host plant cell, while lignification and suberization are terminal processes of determinate and highly differentiated plant cells capable of forming secondary cell walls. In the case of lignification, this process is restricted to water-conducting vascular cells and their neighbouring fibres (Ros Barceló, 1997), while suberization is restricted to the cell wall of epidermal tissues of underground 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 or lignified 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 monomers 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, 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 that covalent 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 terminal arabinose (Ara) and galactose residues of pectic polysaccharides 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) forms a cross-link between the polysaccharides to which it is esterified.
In addition to the first-discovered dimer, 5,5'-dehydrodiferulate, 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 polysaccharide chains could potentially be cross-linked by a tetramer of ferulic acid, which suggests that these Prx-mediated oxidatively generated oligomers of ferulate may play an important role in determining cell wall assembly and cell wall susceptibility 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, coniferyl, and sinapyl alcohols, in a H2O2-dependent reaction mediated by Prxs, enzymes which generate the corresponding free radicals from the three monolignols (Ros Barceló, 1997). The regio- and stereospecificity of the cross-coupling reaction of monolignol radicals produces a hydrophobic heteropolymer 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 this process (Ros Barceló 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 (Bernards et 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 Barceló et al., 2004), substrate accommodation in the catalytic centre of the enzyme determines the real role played by each Prx isoenzyme in lignin biosynthesis (Kobayashi et al., 2005; Ros Barceló et al., 2007).
Lignification is an H2O2-dependent Prx-mediated process (Czaninski et al., 1993; Olson and Varner, 1993; Ros Barceló, 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; Ros Barceló, 1998b, 1999; Karlsson et al., 2005), which generates 
. This 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 (,
-dioic acids and -hydroxyalkanoic 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 radical coupling process (Bernards et al., 2004), analogous to the process of lignin formation from monolignols, but this enzyme shows a marked substrate preference for p-hydroxycinnamates (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; Bernards et al., 2004), similar to that occurring during lignification (Ros Barceló, 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 |
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TopAbstractIntroductionClass III plant peroxidases:...Prxs and the reinforcement...Prxs and the metabolism...Prxs and the production...Signalling pathways in the...References |
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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 (
, H2O2, and OH•), predominantly and H2O2, are toxic intermediates 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 , which later dismutates to H2O2. The Prx-mediated 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 Barceló, 1998b; Ros Barceló 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 quantitative 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 cell death (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 elucidate 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 induced by H2O2 during the HR in Arabidopsis (Desikan et al., 1998) and soybean (Solomon et al., 1999) requires transcription and translation, and several studies have demonstrated 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 /H2O2 through two mechanisms. The first mechanism is restricted to the /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)- complex and yields the FeIII form of the enzyme and , 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 /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 no net /H2O2 production (Fig. 2B).
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The second mechanism involves the oxidation through a Prx cycle of a suitable reductor (i.e., a thiol [RSH]) to its corresponding radical ([RSSR]•–) (Fig. 3), which further reacts with O2 through a reaction of mediation redox, to give
(Burner and Obinger, 1997). However, caution should be exercised when considering Prx as a possible enzyme responsible for /H2O2 production since the overall balance of these oxidase/Prx reactions in a closed system is non-net /H2O2 production (Fig. 3).
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The overall balance of the reactions depicted in Fig. 3, however, does not exclude the possibility that, in these enzymatic reactions, (i) both
and H2O2 can be transitorily formed while [RSSR]•– is not totally consumed, (ii) 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, which may 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 /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 (OH•), and it is probable that microbial polysaccharides are also targets of OH•, and so the OH• produced by host plant cells may provoke microbial cell wall polysaccharide scission as a fine defence mechanism against pathogens. OH• can be generated from H2O2 in the host plant cell wall by Prxs (Liszkay et al., 2003) from and H2O2 through a Haber–Weiss-type reaction:
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Although OH• is exceedingly reactive, if its production is controlled, for example, by the correct siting of Prx relative to microbial polysaccharide molecules, OH• could be very precisely targeted to cause microbial polysaccharide scission. How this might be achieved has yet to be determined. Evidence for OH•-induced polysaccharide splitting in plant cell walls has been obtained by finding the predicted products of OH• 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, , and OH• in plant defence reactions, is apparently far from being completely understood (Passardi et al., 2004b).
RNS in plant defence responses
NO• is a relatively stable paramagnetic free-radical molecule 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• 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 NO• 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 NO• and, in general, most of the RNS (NO•, NO+, NO–, 
, 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. Two landmark publications have demonstrated the role of NO• 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 (García-Brugger et al., 2006). At the transcriptional level, microarray and cDNA-AFLP data obtained from NO• donor-treated Arabidopsis cells indicate that NO• modulates the expression of several 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 of these 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 intermediate. It is then possible that NO•, a free radical itself, may react with to form the highly reactive peroxynitrite anion, ONOO–, and subsequent cellular effects may then be induced by ONOO–. In this context, it is noteworthy that NO• 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 NO• is required for the activation of plasma membrane NADPH oxidases (Vandelle et al., 2006). There are also some controversial reports on NO• cross-talk with ROS in host plant defence responses: for example, it appears that RNS works collaboratively with ROS in many cases (Delledonne et al., 1998), while in other cases RNS acts antagonistically (Neill et al., 2002).
Prxs may participate in the metabolism of RNS
It has long been known that NO• 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 NO• 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 NO• 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 and β-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 1.9x105 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):
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NO• 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 7.0x105 M–1 s–1 yielding the nitrosyl species, NO+. NO• also reacts with CII with a rate constant (k3) of 1.3x106 M–1 s–1 to lead probably to the nitrite anion, 
. Interestingly, the reaction of CII with NO• 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• may enhance Prx activity by promoting the formation of the native enzyme, FeIII, from CII. Thus, both activating and inhibitory effects of NO• on Prx could be observed, depending on the environment in which the enzyme is located.
The product of NO• oxidation by CII of Prx is apparently , which can be further oxidized by plant Prxs to lead to the most likely form, (Shibata et al., 1995; van der Vliet et al., 1997). Plant Prxs are also capable of oxidizing the Tyr contained in proteins to Tyr radicals (Tyr•), which combine with another Tyr• to form dityrosine (Michon et al., 1997). When the oxidation of Tyr by plant Prxs is carried out in the presence of , a mixture of Tyr• and 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 protein damage 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 NO• and production. Therefore, it is likely that in diseased tissues both NO and will react to lead to ONOO–:
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ONOO– is formed at a near difusion controlled rate (k=6.7x109 M–1 s–1), and it has been postulated that it plays a major role in cytotoxicity (Gabaldón 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 (k=3x106 M–1 s–1) with the resting form of the enzyme to lead to CII (Floris et al., 1993):
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. CII is catalytically inactive towards ONOO–, and the decay of CII to the native enzyme, Fe(III), only takes place in the presence of an external electron donor, such as a phenol. In such a scenario, a role in the scavenging of ONOO– has been proposed 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 NO•. In this reaction, N-hydroxy-L-arginine, an N-hydroxyguanidine, acts as key intermediate. N-hydroxyguanidines, including N-hydroxy-L-arginine, may be oxidized by plant Prxs to release NO•, yielding the same products as those obtained with NOS (Xian et al., 2001; Cai et al., 2002). The ability of plant Prxs to synthesize NO• 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 NO• as a collateral product of the reaction.
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Prxs and the production of anti-microbial metabolites |
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TopAbstractIntroductionClass III plant peroxidases:...Prxs and the reinforcement...Prxs and the metabolism...Prxs and the production...Signalling pathways in the...References |
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Plant Prxs are able to catalyse the synthesis of bioactive plant products (Ros Barceló and Pomar, 2002), and therefore 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 reactions, and their significance in vivo has been addressed several times (Langcake and Pryce, 1977a, b;Langcake, 1981; Waffo-Teguo et al., 2001; Ros Barceló and Pomar, 2002).
The list of bioactive (anti-fungal and anti-bacterial) products resulting from Prx-mediated reactions is continuously 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 Barceló 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 activity (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 -3',4'-anhydrovinblastine (Costa et al., 2008), the major alkaloid present in C. roseus leaves, and the precursor of the natural antitumoral products, vinblastine and vincristine.
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Signalling pathways in the regulation of Prxs |
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TopAbstractIntroductionClass III plant peroxidases:...Prxs and the reinforcement...Prxs and the metabolism...Prxs and the production...Signalling pathways in the...References |
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SA-mediated defences
SA has long been known to play a central role in plant defence reactions. SA levels increase in plant tissue following 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 is required 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; Martínez et al., 2000; Fernandes et al., 2006), but this behaviour is not universal since some Prxs are not responsive to SA (Ward et al., 1991; Hiraga et al., 2000). This SA-sensitivity probably marks the frontier line between Prxs involved 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 and inhibits catalase as well as Prxs (Chen et al., 1993; Rüffer 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 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 during the Prx catalytic cycle, in which SA could act as e– donor for Prx, generating SA radicals (SA•). SA• could thus generate by means of a reaction of mediation redox, such as that described in Fig. 3 for [RSSR]•–. Evidence supporting the production of SA• 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 SA action 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; Kumari et 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 development 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 as it 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 isoenzymes (Abeles et al., 1989; Morgens et al., 1990; Ishige et 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 defence responses. 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 signalling 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 these Prxs are really integrated within the complex network of defence responses of any host plant cell, will be the cornerstone of future research.
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Acknowledgements |
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L Almagro and S Belchí-Navarro hold grants from the Fundación Séneca. We thank Estefanía Pedreño for revising the English manuscript. This work has been partially supported by the MEC and FEDER (BIO2005-00332, BFU2006-11577) and by the Consejería de Educación, Ciencia e Investigación de la Región de Murcia (BIO BVA 07 01 0003).
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Footnotes |
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* These authors contributed equally to this review.
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Abbreviations |
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Ara, arabinose; Avr, avirulent; CI, compound I; CII, compound II; CIII, compound III; DPI, diphenylene iodonium; EPR, electron paramagnetic resonance; 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.
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