JXB Advance Access originally published online on November 26, 2007
Journal of Experimental Botany 2008 59(2):147-154; doi:10.1093/jxb/erm244
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FOCUS PAPER |
Nitric oxide function and signalling in plant disease resistance
1Institute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, King's Buildings, Edinburgh EH9 3JR, UK
2Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Daturn Road, Andingmenwai 100101, Beijing, China
* To whom correspondence should be addressed: gloake{at}ed.ac.uk
Received 19 June 2007; Revised 9 August 2007 Accepted 14 September 2007
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Abstract |
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 Top Abstract IntroductionNO: chemical properties and...NO productionNO function in hypersensitive...NO function in plant...S-nitrosylation: a key regulator...ConclusionsReferences |
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Nitric oxide (NO) is one of only a handful of gaseous signalling molecules. Its discovery as the endothelium-derived relaxing factor (EDRF) by Ignarro revolutionized how NO and cognate reactive nitrogen intermediates, which were previously considered to be toxic molecules, are viewed. NO is now emerging as a key signalling molecule in plants, where it orchestrates a plethora of cellular activities associated with growth, development, and environmental interactions. Prominent among these is its function in plant hypersensitive cell death and disease resistance. While a number of sources for NO biosynthesis have been proposed, robust and biologically relevant routes for NO production largely remain to be defined. To elaborate cell death during an incompatible plant–pathogen interaction NO functions in combination with reactive oxygen intermediates. Furthermore, NO has been shown to regulate the activity of metacaspases, evolutionary conserved proteases that may be intimately associated with pathogen-triggered cell death. NO is also thought to function in multiple modes of plant disease resistance by regulating, through S-nitrosylation, multiple nodes of the salicylic acid (SA) signalling pathway. These findings underscore the key role of NO in plant–pathogen interactions.
Key words: Hypersensitive response, nitric oxide, plant disease resistance, S-nitrosylation, S-nitrosothiols
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Introduction |
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TopAbstractIntroductionNO: chemical properties and...NO productionNO function in hypersensitive...NO function in plant...S-nitrosylation: a key regulator...ConclusionsReferences |
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In animals, the identification of NO as the endothelium-derived relaxing factor combined with the discovery of NO generation by nitric oxide synthases primed an explosion of research in this area in the 1990s (Palmer et al., 1987; Ignarro, 1990; Moncada et al., 1991). Despite the report of NO generation by plants in 1979 (Klepper 1979), developments in NO research lagged significantly behind the advances made utilizing animal systems. However, progress in uncovering NO function in plants is now starting to move forward with increased impetus. An increasing number of roles for NO in plant growth, development, and especially disease resistance, are now emerging. While a model for NO function in plants at the molecular level remains to be formulated, the first targets for NO are now starting to emerge. This holds the promise of potentially new paradigms in NO function because plants do not possess an NO-regulated guanylate cyclase-dependent signalling pathway, which underpins a plethora of NO-mediated responses in animals. Here, recent findings in NO biology related to the field of plant disease resistance are reviewed.
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NO: chemical properties and signalling |
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TopAbstractIntroductionNO: chemical properties and...NO productionNO function in hypersensitive...NO function in plant...S-nitrosylation: a key regulator...ConclusionsReferences |
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Nitric oxide (NO) possesses a number of key features that collectively make this molecule ideally suited to its cellular signalling functions. NO is a lipophilic diatomic gas under atmospheric conditions. It has a relatively small Stoke's radius and this, in combination with its neutral charge, facilitates rapid membrane diffusion (Goretski and Hollocher, 1988). The presence of an unpaired electron in NO supports its high reactivity with oxygen (O2), superoxide (O2), transition metals, and thiols, which largely shape its cellular functions within the cell. The removal of the unpaired electron in NO generates the nitrosonium cation NO+, while the addition of an electron forms the nitroxyl anion (NO–). These different forms of NO exhibit distinct chemical reactivities (Stamler et al., 1992).
NO reacts with O2 to produce a variety of distinct nitrogen oxides which each possess unique reactivity profiles (Henry et al., 1997). In the presence of O2, NO reacts with this reactive oxygen intermediate (ROI) to form peroxynitrite (ONOO–), a particularly destructive molecule within biological systems (Bonfoco et al., 1995). NO is also reported to bind a variety of haemoproteins forming a nitrosyl–iron complex. For example, in animals, guanylate cyclase (GC), which generates cyclic GMP (cGMP), is a key NO target (Lucas et al., 2000). When NO binds to the haem group within the regulatory domain it forms an iron–nitrosyl–haem complex, which is required for GC activation and cognate cGMP formation. Subsequently, the function of this enzyme activates a cGMP-dependent protein kinase, which regulates a plethora of cellular activities (Hofmann et al., 2000). In plants, pharmacological inhibitors of GC activity have been reported to diminish plant defence gene expression (Durner et al., 1998). While orthologues of animal GCs have not been found, a new class of these enzymes has been uncovered in Arabidopsis (Ludidi and Gehring, 2003). This plant-specific GC does not possess a haem-binding motif that is characteristically required for NO binding to animal GCs. Furthermore, the activity of this enzyme was not NO-dependent in vitro. Collectively, these data suggest that this GC is not regulated directly by NO. Despite the apparent absence of a prototypic GC target, plants contain a multitude of proteins with metal-bound domains whose activities could potentially be modulated by NO. Furthermore, over the last decade research in the animal field has led to an appreciation that a large slew of NO signalling does not in fact operate through the classical GC-dependent pathway. Many key regulatory proteins contain thiols at active sites or points of allosteric regulation. The reaction of NO with these critical thiols to form S-nitrosothiols (SNOs), a process coined S-nitrosylation, represents a control mechanism that is being uncovered for an increasing number of proteins (Wang et al., 2006b).
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NO production |
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TopAbstractIntroductionNO: chemical properties and...NO productionNO function in hypersensitive...NO function in plant...S-nitrosylation: a key regulator...ConclusionsReferences |
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In animals, the route for NO synthesis is well established: NO is generated during the conversion of L-arginine to citrulline by a family of nitric oxide synthase (NOS) enzymes (Palmer et al., 1993). The active form of these enzymes is a homodimer. However, as two monomers of calmodulin (CaM) are required for activity, the holoenzyme is a homotetramer. Animal NOS enzymes also possess a number of key co-factors such as haem, FAD, FMN, and tetrahydrobiopterin. Mammals possess three extensively characterized NOS enzymes which exhibit distinct tissue specificities and Ca2+ requirements (Nathan and Xie, 1994). Thus, while the constitutive neuronal (n)NOS and endothelial (e)NOS isoforms are Ca2+-dependent, the inducible (i)NOS enzyme is Ca2+-independent. NOS has also been identified in the model arthropod Drosophila melanogaster (Regulski and Tully, 1995) and in Neurospora crassa (Ninnemann and Maier, 1996).
A key feature of the plant defence response is the generation of a burst of NO following pathogen recognition (Delledonne et al., 1998; Durner et al., 1998). This was first reported during resistance (R) gene-mediated protection in soybean suspension cultures against Pseudomonas syringae pv. glycinea expressing the AvrA avirulence gene (Delledonne et al., 1998) and N-mediated recognition of toabacco mosaic virus (TMV) in Nicotiana tabacum (Durner et al., 1998). Kinetic studies during these plant–pathogen interactions suggested maximal NO accumulation occurred within 4–6 h following R gene recognition. Furthermore, the deployment of animal NOS inhibitors effectively abrogated this pathogen-triggered NO production (Delledonne et al., 1998; Durner et al., 1998). Thus suggesting an animal-inducible (i)NOS-like enzyme may function in plant disease resistance. However, extensive in silico searches have revealed no candidate orthologues of animal NOS genes.
To date, numerous enzymatic sources of NO synthesis have been suggested in plants, together with a number of non-enzymatic mechanisms (Lamattina et al., 2003). It has been well established that nitrate reductase (NR) can catalyse the synthesis of NO and N2O from nitrite (Harper, 1981). Furthermore, an Arabidopsis line containing mutations in each of two NR genes has been reported to be compromised in abscisic acid (ABA)-induced stomatal closure (Desikan et al., 2002). However, significant NO production from NR is dependent upon high levels of nitrite and anoxia (Vaucheret et al., 1992) or the absence of photosynthetic activity (Botrel et al., 1996). Thus, during aerobic conditions the level of NO synthesis is low. Also, plants may not always have access to an abundant pool of nitrite, under which conditions NO production would be compromised. Nevertheless, recent data suggest NR may contribute towards to the NO burst in Arabidopsis in response to an avirulent strain of P. syringae pv. maculicola (Modolo et al., 2005). While a NOS-like activity and a mitochondrial-dependent nitrite-reducing activity were also proposed to play a significant role. Collectively, these data suggest that NR is unlikely to be the major generator of NO synthesized during the pathogen-triggered nitrosative burst.
Recently, a plant gene, AtNOS1, has been identified that exhibited significant sequence similarity to a snail gene which encoded a NOS-like activity (Guo et al., 2003). Although AtNOS1 does not share any features with archetypal mammalian NOS enzymes, this protein was reported to show NOS activity (Guo et al., 2003). More recent data, however, seem to suggest that recombinant AtNOS1 protein does not exhibit NOS activity (Crawford et al., 2006; Zemojtel et al., 2006). Nevertheless, loss of AtNOS1 function reduced in vivo NO levels in response to abscisic acid (ABA) (Guo et al., 2003). The absence of AtNOS1 activity also compromised the nitrosative burst induced in response to bacterial lipopolysaccharide (LPS) (Zeidler et al., 2004). Taken together, these findings suggest that, while AtNOS1 is unlikely to encode a NOS-like activity this gene product may well be required for NO production. Thus, AtNOS1 may operate directly or indirectly to regulate NO synthesis. In this context, AtNOS1 has sequence similarity to GTP-binding proteins (Zemojtel et al., 2006). In the light of these observations, AtNOS1 has therefore been renamed Arabidopsis thaliana nitric oxide associated 1 (AtNOA1) (Crawford et al., 2006).
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NO function in hypersensitive cell death |
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TopAbstractIntroductionNO: chemical properties and...NO productionNO function in hypersensitive...NO function in plant...S-nitrosylation: a key regulator...ConclusionsReferences |
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An almost ubiquitous feature of R gene-mediated resistance is the cellular execution of the directly challenged cell and sometimes additional surrounding cells, termed the hypersensitive response (HR) (Greenberg and Yao, 2004). This phenomenon is thought to deny nutrients to invading biotrophic pathogens, which can only parasitize living plant cells. Despite the potential importance of this defence strategy to the host plant, the molecular mechanisms underpinning HR development remain largely unknown. The emerging evidence suggests that NO plays a central role in plant protection, probably functioning in combination with reactive oxygen intermediates (ROIs) (Delledonne et al., 1998, 2001). One of the most rapid responses of plants to potential pathogens is the congruent production of both NO and ROIs. Genetic evidence suggests that ROIs are predominantly generated from enzymes similar to those responsible for the respiratory ROI burst in mammalian phagocytes (Cross and Segal, 2004; Torres et al., 2002).
Cell death during the HR is thought to be dependent upon the balanced production of NO and ROIs (Delledonne et al., 2001). In animals, NO co-operates with ROIs by reacting with O2 in a diffusion-limiting reaction to form ONOO–, a pervasive mediator of cellular injury (Bonfoco et al., 1995). Plants, however, are thought to be relatively resistant to this molecule (Delledonne et al., 2001). In this case, cell death has been proposed to develop through the action of NO with H2O2, rather than O2, supported by the acceleration of O2 dismutation to H2O2 by superoxide dismutase (SOD) during the HR (Delledonne et al., 2001). Thus, a substantial increase in SOD activity during the plant defence response would be expected because most of the basal NO produced rapidly reacts with O2 to produce ONOO– (Vanin et al., 2004). In this context, genes encoding specific SOD isoforms are powerfully induced following pathogen recognition (Montalbini and Buonaurio, 1986). The reaction of NO with O2 to produce ONOO– is so pervasive that it resulted in a 94% underestimation of the levels of basal NO synthesis (Vanin et al., 2004). Thus, in the absence of attempted pathogen infection, plants are exposed to an environment rich in ONOO–, an inevitable consequence of producing NO in a photosynthetic organism. This could explain why plant cells have been reported to exhibit a surprising level of resistance against ONOO– (Delledonne et al., 2001). Exposure of animal cells to concentrations of ONOO– from 1–1000 µM resulted in concentration-dependent killing (Lin et al., 1995), however, soybean suspension cells were found to be resistant to 1 mM ONOO– (Delledonne et al., 2001). In another study, 0.1 mM ONOO– produced conspicuous necrotic lesions when infiltrated into Arabidopsis leaves (Alamillo and Garcia-Olmedo, 2001), possibly reflecting differences between cellular environments. Perhaps informatively, an increasing number of novel ONOO– scavengers are now being uncovered from plant sources (Yokozawa et al., 2002; Rose et al., 2003), probably reflecting the exposure of plant cells to high levels of this molecule. A requirement for NO and H2O2 in plant cell death has also been provided by experiments using transgenic tobacco lines with reduced catalase activity. Under moderate light intensities these transgenics accumulate H2O2 and exhibit significantly increased levels of cell death compared with wild-type lines when infiltrated with NO (Zago et al., 2006). Transgenic plants containing a bacterial nitric oxide dioxygenase transgene, which turns over NO, accumulated significantly less of this molecule (Zeier et al., 2004). Furthermore, these lines showed increased levels of H2O2, possibly because NO produced during the nitrosative burst functions both to blunt the activity of antioxidant enzymes and remove O2, by forming ONOO–, thereby collectively promoting H2O2 accumulation.
The molecular mechanisms triggering hypersensitive cell death in response to NO and H2O2 remain to be uncovered. In animals, the most well understood mode of regulated cell death involves the co-ordinated demolition of cellular structures by members of the caspase family of cysteine proteases (Martin and Green, 1995). Caspases are present as inactive enzymes in healthy cells and become activated during conditions of cellular stress or infection that result in the release of cytochrome c from mitochonria (Goldstein et al., 2000). Plants do not contain structural homologues of caspases, but encode several related proteins. Metacaspases have been proposed to be the ancestors of metazoan caspases (Uren et al., 2000), although it remains to be established if they have a function in the HR. By contrast, a plant vacuolar cysteine protease (VPE) has been implicated in pathogen-triggered plant cell death (Hatsugai et al., 2004). Furthermore, overexpression of a cystatin, a cysteine protease inhibitor, diminished cell death (Belenghi et al., 2003), suggesting an important role for cysteine proteases in this process. A subtilisin-like serine protease is also thought to be required for cell death in response to the pathogen-derived toxin, victorin (Coffeen and Wolpert, 2004). Moreover, recent data also suggests an important role for plant homologues of animal cathepsin B proteases (Gilroy et al., 2007).
An important recent study demonstrated that the Arabidopsis thaliana metacaspase 9 (AtMC9) zymogen was S-nitrosylated at its active site cysteine in vivo (Belenghi et al., 2007). This post-translational modification suppressed both AtMC9 autoprocessing and proteolytic activity. The mature processed form of this protease, however, is not a target for S-nitrosylation due to the presence of a second S-nitrosylation-insensitive cysteine that can replace the S-nitrosylated cysteine residue within the catalytic centre of processed AtMC9 (Belenghi et al., 2007). Therefore, S-nitrosylation of AtMC9 and perhaps also other metacaspases could help maintain theses proteases in their inactive state by preventing autocleavage and cognate activation. Furthermore, because dithiothreitol, which reverses S-nitrosylation, activated AtMC9 autoprocessing, in addition to the enzymatic activity of the S-nitrosylated zymogenic form, de-nitrosylation may therefore have an important role in the activation of these enzymes. Although no mechanism has yet been ascribed for this process, it could be mediated by redox enzymes such as glutaredoxin or thioredoxin (Mitchell and Marletta, 2005). These data parallel those from mammals, where caspase-3 activity is inactivated by S-nitrosylation of a catalytic cysteine (Melino et al., 1997). Conversely, Fas-induced de-nitrosylation, via an unknown mechanism, leads to caspase-3 activation (Mannick et al., 1999).
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NO function in plant disease resistance |
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TopAbstractIntroductionNO: chemical properties and...NO productionNO function in hypersensitive...NO function in plant...S-nitrosylation: a key regulator...ConclusionsReferences |
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Plants have evolved a variety of defence mechanisms to protect themselves against microbial colonization. Non-host resistance (NHR) functions as the first bulwark, conveying protection against whole species of parasites (Yun et al., 2003). In response to microbes that avoid, tolerate or suppress NHR, plants have evolved a phalanx of R proteins, which, upon pathogen recognition, trigger a battery of inducible defence responses (Dangl and Jones, 2001). In the absence of R gene recognition, plants rely on basal resistance to restrict the growth of virulent parasites.
NO is not only thought to function during the development of hypersensitive cell death but also in the establishment of plant disease resistance. Administration of NO donors to tobacco plants or cell suspension cultures induced the expression of the defence-related genes encoding phenylalanine ammonia lyase (PAL) and pathogenesis-related protein 1 (PR1), markers for phenylpropanoid biosynthesis and salicylic acid (SA)-mediated signalling, respectively. Both of these genes play important roles in the development of plant disease resistance (Delledonne et al., 1998; Durner et al., 1998). Subsequently, more wide-ranging studies demonstrated that NO could modulate the expression of genes encoding a range of plant effector and regulatory proteins (Polverari et al., 2003; Huang et al., 2004; Parani et al., 2004; Zago et al., 2006). Moreover, a recent study in catalase-deficient tobacco plants, uncovered a small number of genes specifically regulated by either NO or H2O2 (Zago et al., 2006). Although, somewhat surprisingly, most of the genes identified were modulated by both NO and H2O2, revealing a significant overlap in gene targets for these two distinct redox signalling molecules.
The first direct link between NO and disease resistance was provided by the finding that infiltration of the NOS inhibitors L-NNA and PBITU supported increased growth of the incompatible bacterial pathogen P. syringae pv. tomato (Pst) DC3000 expressing the avrRpm1 avirulence gene (Delledonne et al., 1998). Thus, suggesting a role for NO in R gene-mediated resistance against bacterial pathogens. NO has also been proposed to function in basal disease resistance triggered following recognition of lipopolysaccharide (LPS), a pathogen-associated molecular pattern (PAMP) (Zeidler et al., 2004). Loss of AtNOA function diminished NO accumulation in response to LPS, reduced defence-related transcript accumulation, and most significant, compromised basal disease resistance against PstDC3000 (Zeidler et al., 2004). Collectively, these data argue that NO has an important signalling function in basal disease resistance, at least against bacterial pathogens.
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S-nitrosylation: a key regulator of disease resistance |
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TopAbstractIntroductionNO: chemical properties and...NO productionNO function in hypersensitive...NO function in plant...S-nitrosylation: a key regulator...ConclusionsReferences |
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In animals, S-nitrosylation is emerging as a prototypic redox-based post-translational modification, which underpins NO signal function during many cellular responses (Stamler et al., 2001; Wang et al., 2006b). S-nitrosylated proteins are in dynamic equilibrium with de-nitrosylated proteins largely due to the action of glutathione (Liu et al., 2001). This antioxidant tripeptide reacts with SNOs to form S-nitrosoglutathione (GSNO) reconstituting the protein thiol (SH) as a consequence. Recently, an enzyme activity was purified, initially from Escherichia coli, which effectively turned over GSNO (Liu et al., 2001). A homologue of the gene encoding this activity has now been identified in plants (Diaz et al., 2003; Sakamoto et al., 2002). Loss-of-function mutations in Arabidopsis thaliana GSNO reductase 1 (AtGSNOR1) resulted in increased cellular levels of SNOs, while a gain-of-function mutation, which resulted in increased AtGSNOR1 gene expression and elevated GSNO turnover, decreased endogenous SNO levels (Feechan et al., 2005). Importantly, loss of AtGSNOR1 activity compromised NHR against the wheat powdery mildew pathogen, Blumeria graminis f.sp tritici (Feechan et al., 2005). Furthermore, the absence of AtGSNOR function also compromised protection mediated by distinct R gene sub-classes and basal resistance towards bacterial and oomycete pathogens (Feechan et al., 2005). Conversely, over-expression of AtGSNOR1 resulted in strikingly enhanced basal resistance, suggesting AtGSNOR1 may be of significantly agricultural utility. When taken together these important findings suggest that AtGSNOR1 is required for multiple modes of plant disease resistance.
What is the mechanism of AtGSNOR1 function during the establishment of disease resistance? Loss-of-function mutations in AtGSNOR1 were found to reduce and delay SA-dependent gene expression in response to either pathogen infection or exogenous SA application and also to diminish SA accumulation (Feechan et al., 2005). By contrast, increased AtGSNOR1 activity accelerated SA-dependent gene expression. Thus, this enzyme regulates both SA biosynthesis and SA signalling. These data suggest that at least two nodes of the SA signalling network may be controlled by S-nitrosylation. A scheme outlining the potential role of NO and SNOs in disease resistance is shown in Fig. 1.
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Surprisingly, reducing the level of AtGSNOR1 transcripts by expressing antisense RNA has been reported to increase basal resistance (Rusterucci et al., 2007), the opposite result to that obtained by Feechan et al. (2005). However, the level of AtGSNOR1 transcripts was only reduced by 40% in this study, whereas the atgsnor1-3 mutation reported by Feechan et al. (2005) is thought to be a null. Furthermore, while SA levels were strikingly decreased in atgsnor1-3 (Feechan et al., 2005) they remained similar to that of wild-type plants in the antisense AtGSNOR1 line (Rusterucci et al., 2007). Also, Feechan et al. (2005) analysed multiple gain and loss-of-function alleles of AtGSNOR1, which exhibited complementary phenotypes to a series of diverse pathogens. By contrast, Rusterucci et al. (2007) only analysed one antisense AtGSNOR1 line, which showed a change in response to a single pathogen, a virulent isolate of Hyaloperonospora parasitica (Rusterucci et al., 2007). One possible explanation for these conflicting data is that different cellular SNO concentrations might either repress or activate signalling pathways depending on the SNO levels required to drive the S-nitrosylation of key regulatory cysteines. In this context, while there is a striking change in SNO levels between the atgsnor1 mutants (Feechan et al., 2005) only a minor change in SNO level is reported in the plants investigated by Rusterucci et al. (2007).
One potential target for S-nitrosylation is NON-EXPRESSOR OF PR1 (NPR1) (Cao et al., 1994). This protein is routinely present in the cytoplasm, but shuttles to the nucleus in response to changes in cellular redox tone during the establishment of disease resistance (Mou et al., 2003), where it orchestrates the expression of a plethora of SA-dependent genes (Wang et al., 2006a). This cytoplasm-to-nucleus shuttling is controlled by the presence of a number of redox responsive cysteines, which could potentially be targets for S-ntrosylation. In an unbiased biochemical screen for proteins that become specifically S-nitrosylated during the plant defence response, Loake and co-workers have demonstrated that SA-binding protein 3 is S-nitrosylated on a specific reactive cysteine (Y Wang et al., unpublished results). S-nitrosylation of SABP3 has been shown to modulate SA-binding and also the cognate carbonic anhydrase activity of this protein.
Recently, a number of Arabidopsis proteins have been shown to be S-nitrosylated following exogenous NO application (Lindermayr et al., 2005). One of these S-nitrosylated proteins, methionine adenosyltransferase (MAT), catalyses the synthesis of the ethylene precursor, S-adenosylmethionine (Lindermayr et al., 2006). Delledonne and co-workers have also recently identified a peroxiredoxin type II E that becomes specifically S-nitrosylated during an incompatible plant–pathogen interaction (MC Romero-Puertas et al., unpublished results). Interestingly, S-nitrosylation of this protein is thought to diminish its ability to turnover ONOO–, leading to increased accumulation of this reactive nitrogen intermediate, which promotes tyrosine nitration. This process has long been thought only to mark cellular damage due to nitrosative stress (Radi, 2004), however, recent studies suggest that it may serve significant signalling functions (Klotz et al., 2002). In a similar fashion to S-nitrosylation, nitration on tyrosine residues may alter protein conformation thus potentially impacting upon catalytic activity, location or protein–protein interactions. Interestingly, the plant non-symbiotic haemoglobin, AHb1, scavenges NO through the production of S-nitrosohaemoglobin (Perazzolli et al., 2004). However, this mechanism of NO depletion does not operate during the development of hypersensitive cell death triggered by avirulent pathogens.
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Conclusions |
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TopAbstractIntroductionNO: chemical properties and...NO productionNO function in hypersensitive...NO function in plant...S-nitrosylation: a key regulator...ConclusionsReferences |
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The accumulating data highlight a key role for NO in plant cell death and disease resistance. It will now be important to identify the elusive NOS that produces NO during an incompatible interaction. The mechanisms by which NO, often in conjunction with ROIs, orchestrate a plethora of cellular activities during the defence response also remain largely obscure. However, with the identification of the first S-nitrosylated proteins progress should now accelerate in this area. In addition, recent data have also provided the first insights into the machinery regulating cellular levels of S-nitrosylation. Consequently, significant advances can now be expected in the mechanisms controlling NO/SNO turnover. In other reference systems detailed prototypic examples exist to explain how NO controls gene expression networks by directly modulating the function of target transcription factors. In this context, plant paradigms are yet to emerge. In the longer term, it may be anticipated that advances in NO/SNO biology may provide novel opportunities for breeding and rational crop design to improve plant disease resistance.
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Acknowledgements |
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We are grateful to those colleagues who provided unpublished data for this review. JKH was supported by a Korea Research Foundation Grant funded by the Korean Government (MOEHRD) (KRF-2005-214-C00231). YW received a Fellowship from the Chinese Academy of Sciences and, subsequently, an International Fellowship from the Royal Society of London. MU was the recipient of a HEC Scholarship from the Governmen of Pakistan. BWY is a BBSRC postdoctoral fellow, while KS received a BBSRC studentship. JGK is funded by a Torrance Scholarship. Work on S-nitrosylation in the Loake lab is funded by BBSRC grant BB/D0118091/1.
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