JXB Advance Access originally published online on November 1, 2007
Journal of Experimental Botany 2008 59(1):25-35; doi:10.1093/jxb/erm218
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SPECIAL ISSUE REVIEW PAPER |
Nitric oxide evolution and perception
1Centre for Research in Plant Science, Faculty of Applied Sciences, University of the West of England, Bristol, Bristol BS16 1Q, UK
2Division of Biology, Imperial College London, London SW7 2AZ, UK
* To whom correspondence should be addressed. E-mail: Steven.Neill{at}uwe.ac.uk
Received 14 June 2007; Revised 24 July 2007 Accepted 1 August 2007
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Abstract |
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 Top Abstract IntroductionNO generation and removal...NO perceptionNO movementNO evolution from plantsConclusionsReferences |
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Various experimental data indicate signalling roles for nitric oxide (NO) in processes such as xylogenesis, programmed cell death, pathogen defence, flowering, stomatal closure, and gravitropism. However, it still remains unclear how NO is synthesized. Nitric oxide synthase-like activity has been measured in various plant extracts, NO can be generated from nitrite via nitrate reductase and other mechanisms of NO generation are also likely to exist. NO removal mechanisms, for example, by reaction with haemoglobins, have also been identified. NO is a gas emitted by plants, with the rate of evolution increasing under conditions such as pathogen challenge or hypoxia. However, exactly how NO evolution relates to its bioactivity in planta remains to be established. NO has both aqueous and lipid solubility, but is relatively reactive and easily oxidized to other nitrogen oxides. It reacts with superoxide to form peroxynitrite, with other cellular components such as transition metals and haem-containing proteins and with thiol groups to form S-nitrosothiols. Thus, diffusion of NO within the plant may be relatively restricted and there might exist ‘NO hot-spots’ depending on the sites of NO generation and the local biochemical micro-environment. Alternatively, it is possible that NO is transported as chemical precursors such as nitrite or as nitrosothiols that might function as NO reservoirs. Cellular perception of NO may occur through its reaction with biologically active molecules that could function as ‘NO-sensors’. These might include either haem-containing proteins such as guanylyl cyclase which generates the second messenger cGMP or other proteins containing exposed reactive thiol groups. Protein S-nitrosylation alters protein conformation, is reversible and thus, is likely to be of biological significance.
Key words: Arginine, cyclic GMP, GSNO, haem, nitric oxide, nitrite, perception, peroxynitrite, S-nitrosylation, S-nitrosothiol, superoxide, transport, tyrosine nitration
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Introduction |
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TopAbstractIntroductionNO generation and removal...NO perceptionNO movementNO evolution from plantsConclusionsReferences |
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In recent years nitric oxide (NO) has emerged as an important endogenous signalling molecule in plants that mediates many developmental and physiological processes including xylogenesis, programmed cell death, pathogen defence, flowering, stomatal closure, and gravitropism (Lamattina et al., 2003; Neill et al., 2003; Delledonne, 2005; Lamotte et al., 2005). Experimental evidence in support of such signalling roles for NO has typically been obtained via the application of either NO or NO donors (NO itself is a reactive gas with a short half-life in air), via the measurement of endogenous NO and through the manipulation of endogenous NO content by chemical and genetic means. There are potential complications with using NO donors (Floryszak-Wieczorek et al., 2006) and undoubtedly technical problems associated with assaying the NO content of and release from plants (Planchet and Kaiser, 2006a, b). Moreover, in some situations, NO can be released in far higher amounts than would probably be required to effect biological responses which raises the question of how it can actually function as a biological signal. NO also has paradoxical effects. For example, it is growth promoting at low concentrations, but quite inhibitory or toxic at high concentrations (Beligni and Lamattina, 1999) and being reactive, is perhaps unlikely to travel far between or even within cells. It may be that in the rush of enthusiasm to ascribe biological roles to NO some problems have been overlooked and with hindsight some of the experimental data may require re-evaluation.
This short review, part of a series on ‘Transport of plant growth regulators’, focuses on NO evolution and perception by plants and inevitably, perhaps, raises more questions than answers.
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NO generation and removal in plants |
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TopAbstractIntroductionNO generation and removal...NO perceptionNO movementNO evolution from plantsConclusionsReferences |
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NO biosynthesis
It is clearly important to elucidate the mechanisms by which NO is biosynthesized in plant cells. However, despite all the research effort over the last 10 years or so, there is still much uncertainty. Most work has focused on two potential enzymatic sources of NO in plants, nitric oxide synthase (NOS) and nitrate reductase (NR), but recent research has also alluded to other potential sources of NO in different compartments of plant cells (Fig. 1A).
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Prior to the complete sequencing of the Arabidopsis genome, early work on NO signalling in plants used pharmacological inhibitors of NO-generating enzymes to indicate the potential source of NO. In addition to non-specific inhibitors of NR, these inhibitors included compounds such as NG-nitro-L-arginine methyl ester (L-NAME) and NG-monomethyl-L-arginine acetate (L-NMMA), analogues of arginine expected to function as competitive inhibitors of NOS. Tungstate, that probably replaces molybdenum in the NR enzyme, has also been used as a potential NR inhibitor. The inhibition of physiological responses such as programmed cell death, stomatal closure or root growth by these compounds suggested that either NOS or NR were likely to be sources of endogenous NO (Neill et al., 2003). Early work by del Rio and colleagues (del Rio et al., 2002) used immunogold labelling to indicate that NOS-like enzymes were present in pea peroxisomes, but the cloning of a pea homologue of NOS was not reported. In furthering this work, the peroxisomal NOS activity was biochemically characterized and arginine-dependent NO accumulation measured by chemiluminescence and electron paramagnetic resonance (EPR) spectroscopy (Corpas et al., 2004a). In addition, constitutive NOS activity, which appeared to be developmentally regulated, was detected in the leaves, stems, and roots of pea seedlings (Corpas et al., 2006). More recently, arginine-dependent, salinity-induced increases in NOS activity have also been demonstrated in olive (Valderrama et al., 2007). What still remains to be achieved, however, is the identification of genes encoding the enzymes responsible for these activities.
The first genetic evidence for a NOS-like enzyme in plants came from the work of Crawford and colleagues who identified an Arabidopsis orthologue of mammalian NOS, named AtNOS1 (Guo et al., 2003). The encoded protein, AtNOS1, had similarity to one from a snail that was possibly involved in NO synthesis. Importantly, AtNOS1 was shown to possess the biochemical characteristics of NOS in that it reduced arginine to citrulline when assayed with a commercial NOS-assay kit. More importantly still, a T-DNA insertion mutant, Atnos1, was identified that produced much reduced levels of NO in guard cells and roots in response to ABA. Collectively, these data strongly suggested that AtNOS1 was truly a source of NO in Arabidopsis. Indeed, other studies also confirmed that the mutant, Atnos1, was deficient in NO synthesis and action (He et al., 2004; Zeidler et al., 2004; Bright et al., 2006).
However, the function of AtNOS1 as a NOS has now been seriously questioned, with three parallel reports in 2006 discussing the problems associated with this concept. It now appears that AtNOS1 may not actually be a NOS at all. Certainly, it has been difficult reproducibly to demonstrate typical NOS activity. Various researchers have been unable to reproduce the results of the earlier work and detect citrulline when using the arginine-to-citrulline conversion kit and working with either AtNOS1 or related enzymes from other species (Zemojtel et al., 2006). Other tests to detect NO arising from the activity of this enzyme have also failed (Crawford et al., 2006). The current view is that, although AtNOS1 may not be a NOS per se, it is somehow involved in NO synthesis or accumulation. Hence, a name change to Arabidopsis thaliana Nitric Oxide Associated 1 (AtNOA1) has been suggested (Crawford et al., 2006). AtNOS1, or as we shall now call it, AtNOA1, has a conserved GTPase domain and because it is probably targeted to the mitochondria (Guo and Crawford, 2005), it has been speculated that it may be a GTPase involved in mitochondrial ribosome biogenesis. Presumably impaired AtNOA1 activity would then be expected to result in impaired mitochondrial function and thus, altered NO levels (Zemojtel et al., 2006). However, GTPase activity is yet to be shown for AtNOA1. Moreover, Guo (2006) argues that the lack of detection of NOS activity from AtNOA1 and its homologues could be due to the fact that their NAD(P)H-dependent activity may be very low compared with that of their mammalian counterparts. It was also suggested that AtNOA1 may use the stable NO synthesis intermediate, N-w-hydroxyarginine (NOHA), rather than arginine to produce NO. Such an intermediate would not be detectable by the traditional NOS assay. In addition, it has been suggested that there may be other co-factors yet to be identified in plants which could be required to regulate ATNOA1 activity (Guo, 2006).
Realistically, these recent developments lead us back to square one: no plant NOS gene has yet been identified. They also highlight a major caveat in the field of NO research in that the traditional NOS assay kits that have been used for mammalian enzymes may not be appropriate for plants. Additional methods such as EPR spectroscopy and chemiluminesence to detect arginine-dependent NOS activity would be suitable alternatives (Corpas et al., 2004a). Nevertheless, the substantial pharmacological data resulting from the use of NOS inhibitors to inhibit biological responses and NO production do indicate that there must be enzymes in plants that are thus affected. By definition, these enzymes are NOS enzymes, but how they use arginine to make NO remains to be seen. It is not unlikely that a plant NOS will have little sequence similarity with its mammalian counterpart, but will still contain domains which allow its redox functions to occur. Such domains could even be located on different polypeptides which could be brought together following a signalling event. If such a scenario were to be correct, the identification of the NO-producing enzyme in plants could be more difficult than previously thought, but one may assume that the enzyme would have a redox function and contain binding sites for redox prosthetic groups such as flavin or haem.
Another enzymatic source of NO is NR. The primary function of the NR family of enzymes in plants is one of nitrogen assimilation by converting nitrate to nitrite. However, NR can also convert nitrite to NO via a NAD(P)H-dependent reaction. This was shown originally in vivo using mutant NR soybean plants (Dean and Harper, 1986), but has also been shown in vitro using purified NR and plant extracts (Rockel et al., 2002; Neill et al., 2003). The first genetic evidence of a physiological role for the generation of NO by NR was in ABA-induced stomatal closure in Arabidopsis (Desikan et al., 2002). NR uses nitrite as a substrate to generate NO and we have been able to show this for Arabidopsis NR in vitro and in vivo (Bright et al., 2006). The inhibition of NR activity with tungstate inhibited both ABA and nitrite-induced stomatal closure and prevented NO generation (Desikan et al., 2002; Bright et al., 2006), thus implying that a NR-like enzyme did play a role in generating the NO normally required to produce these responses. Importantly, it has also been possible to show the inhibition of purified NR activity in vitro using tungstate (Bright et al., 2006). Arabidopsis contains two NR genes, NIA1 and NIA2, which have a high degree of coding sequence similarity and result in two isoforms which are 83.5% identical at the amino acid level, but which show some localized areas of sequence divergence in the first 90 N-terminal amino acids and in various other regions within the two proteins. Use of the Arabidopsis nia1nia2 NR double mutant confirmed a role for one or both of the encoded enzymes in guard cell responses to ABA (Desikan et al., 2002). The observation that nitrite did not induce NO generation in nia1nia2 guard cells suggests that this requirement for NR reflected its in vivo capacity to produce NO from nitrite. However, as pointed out by Crawford (2006), a lack of NR may have several effects on plant N metabolism and indeed Modolo et al. (2006) have reported that the arginine content of nia1nia2 leaves is substantially reduced. Our recent work using single NR mutants indicates that NIA1, which is usually present at a much lower abundance than NIA2, is the source of NO during ABA signalling (Bright et al., 2006). These data also suggest that the aberrant NO biology in nia1nia2 is due specifically to the lack of NIA1 as opposed to generally aberrant N metabolism. Interestingly, Yu et al. (1998) similarly concluded that NIA1 and NIA2 have distinct signal transduction and nitrogen assimilatory roles. Key questions must then relate to the differential expression of their encoding genes, their subcellular localization and interacting protein partners, their activation characteristics and the functional significance of their partial sequence divergence. NO generation by NR is stimulated by hypoxic conditions and in spinach and maize NR-mediated NO generation can be modulated by the phosphorylation status of the NR (Rockel et al., 2002). Thus, a potential regulatory mechanism may exist in vivo. Increasing endogenous nitrite concentrations, either by dark treatment or by antisense-inhibition of endogenous nitrite reductase activity (Morot-Gaudry et al., 2002; Rockel et al., 2002), increases NO emission. NR-mediated NO generation has also been demonstrated in roots with a potential physiological role, that of mediating aerenchyma formation, having been suggested (Dordas et al., 2003).
As shown in tobacco, mitochondrial reduction of nitrite to NO can also be a major source of NO with tissue nitrite concentrations being a major limiting factor and NR function obligatory (Planchet et al., 2005). However, it is not clear whether or not this occurs in both leaves and roots (Gupta et al., 2005; Modolo et al., 2005). In addition, soybean chloroplasts have recently been identified as a source of NO via arginine or nitrite (Jasid et al., 2006). However, in this latter case, the enzymes regulating both arginine and nitrite-dependent NO formation are not yet known. Apoplastic, non-enzymatic conversion of nitrite to NO at low pH has also been demonstrated in the barley aleurone layer (Bethke et al., 2004).
A plasma membrane-bound, root-specific enzyme, nitrite-NO oxidoreductase (Ni-NOR), may also function as a further source of NO. This enzyme was identified biochemically via its NO-generating activity. However, unlike NR, it does not use NAD(P)H as a cofactor, but uses cytochrome c as an electron donor in vitro and has a comparatively reduced pH optimum. However, neither its physiological role nor its genetic identity is yet known (Stohr and Stremlau, 2006).
Other enzymes may also be involved in NO production (Corpas et al., 2004b). For example, in animals, xanthine oxidoreductase (XOR), under hypoxic conditions, can produce NO in preference to H2O2 (Millar et al., 1998). However, Planchet and Kaiser (2006b) were unable to observe any NO production from recombinant xanthine oxidase. Interestingly, Arnaud et al. (2006) demonstrated a plastid-located, iron-induced NO burst in Arabidopsis that, although susceptible to inhibition by L-NAME, required neither AtNOS1 nor NR. Such novel NO sources await characterization.
Removal of nitric oxide
It is likely that biologically active molecules such as NO are rapidly removed or metabolized following initial signalling events. It is also possible that increased rates of NO accumulation or emission actually reflect reduced rates of removal rather than increased generation. Thus, the importance of determining how NO levels are controlled is of obvious importance (Fig. 1B). Simple chemical reactions are often responsible for the removal of NO from solution. Nitric oxide is inherently unstable and will readily react with oxygen to form nitrite and nitrate. As described above, nitrite can act as a precursor to NO and may have some biological activity per se (Gladwin et al., 2005).
The free radical nature of NO means that it will readily react with other radicals that might also be present. In both animals and plants, NO is often produced at the same time and in the same place as Reactive Oxygen Species (ROS) such as superoxide anions. Superoxide and NO will react in a stoichiometric manner to produce peroxynitrite (ONOO–). Although it has been noted that plant cells, unlike animal cells, appear resistant to peroxynitrite (Delledonne et al., 2001), it may have intrinsic signalling properties. Whether or not this turns out to be the case, the level of NO can be instrumental in controlling ROS levels in cells and vice versa. It has been noted that the basal rates of NO production in leaves are often under-estimated because the NO reacts rapidly with superoxide anions (Vanin et al., 2004).
NO reacts readily and reversibly with either thiol groups in the cysteine residues of proteins or with the tripeptide glutathione (GSH) and protein S-nitrosylation may be a key facet of NO signalling (see below). Glutathione concentrations are typically 2–3 mM in plant cells (Ball et al., 2004) and thus, formation of S-nitrosylated glutathione (GSNO) could have a large impact on the concentration of free NO. GSNO is metabolized by the enzyme GSNO reductase (Diaz et al., 2003; Fig. 1B) and this enzyme may be instrumental in controlling the bioavailability of NO and the formation of protein S-NO groups, thereby regulating such NO-regulated processes as, for example, plant pathogen defence responses (Feechan et al., 2005).
As well as reacting with thiol groups, NO can also interact with transition metals, particularly with iron which is often associated with haem as in guanylyl cyclase (see below) and it has long been recognized that NO can react with haemoglobins. Non-symbiotic haemoglobins (nsHbs) from barley, alfalfa, and Arabidopsis are known to react with NO resulting in its removal from solution. Nitrate is formed in a NAD(P)H-dependent reaction with the oxidized haem intermediate being re-reduced by either the NAD(P)H or FADH or, as in the case of the barley haemoglobin, by methaemoglobin reductase (reviewed by Perazzolli et al., 2006). Arabidopsis AHb1 is also S-nitrosylated (Perazzolli et al., 2004). Interestingly, nsHbs are induced by certain treatments where NO generation might be enhanced, for example, by low partial pressures of O2 (Trevaskis et al., 1997) or by nitrate or nitrite and by NO itself (Wang et al., 2000; Ohwaki et al., 2005; Shimoda et al., 2005; Sasakura et al., 2006). Transgenic manipulation of AHb1 affects NO evolution, which, correlated with the ability to survive hypoxic stress (Perazzolli et al., 2004), indicates a physiological role for AHb1 in modulating NO levels. Further evidence for the endogenous NO-detoxifying action of Hb comes from work involving plant–microbe interactions. Boccara et al. (2005) showed that HmpX, an Erwinia chrysanthemi flavohaemoglobin and virulence determinant, removed NO. Infection with a HmpX-deficient mutant of E. chrysanthemi triggered high levels of NO coupled to the hypersensitive response in the host plant. Sasakura et al. (2006) showed that a nsHb in the actinorhizal plant Alnus firma is highly expressed in nodules and may serve to detoxify NO.
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NO perception |
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TopAbstractIntroductionNO generation and removal...NO perceptionNO movementNO evolution from plantsConclusionsReferences |
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Although there is no doubt that plants perceive and respond to NO, the mechanisms by which such perception occurs still require clarification. There is now considerable research interest concerning this question, but as no specific plant NO receptor has been identified, work in this area has taken its lead from mammalian research. The reactive nature of NO and its ability to interact with and modify many proteins suggests that there may turn out to be many ‘NO perceptors’ (Fig. 2). In animal cells, soluble guanylyl cyclase (sGC) has a key role in NO signalling. NO activates sGC by binding to its haem domain stimulating a transient rise in cGMP levels which, in turn, activates a number of targets. In plants, pharmacological studies using inhibitors of NO sensitive guanylyl cyclase have implicated cGMP downstream of NO and ABA signalling in guard cells (Neill et al., 2003). NO induces an increase in cGMP (Durner et al., 1998) and work in our laboratory has shown that application of ABA or the NO donor SNP to guard cell-enriched preparations from Arabidopsis induces a small and transient increase in cGMP that can be prevented by the application of the GC inhibitor 1H-[1,2,4] oxadiazolo[4,3-a]quinoxalin-1-one (ODQ) or the NO scavenger PTIO (J Harrison et al., unpublished data). Thus, a similar mechanism of NO stimulated cGMP synthesis may also operate in plants. A key signalling molecule downstream of cGMP is cyclic ADP-ribose (cADPR) (Wendehenne et al., 2001). In animal cells cADPR stimulates Ca2+ release via intracellular ryanodine receptor calcium channels (RYR) and it is possible that a similar signalling mechanism operates in plants. In tobacco, cADPR elevates the expression of the genes encoding phenylalanine ammonia lysase (PAL) and the pathogenesis-related protein 1 (PR-1) in a manner that is sensitive to RYR inhibitors (Durner et al., 1998). These genes are also NO-regulated and cADPR antagonists reduce the expression of PR-1 (Klessig et al., 2000). NO is known to cause increases in the level of free Ca2+ (Durner et al., 1998; Garcia-Mata et al., 2003). Thus, NO may signal through cGMP, cADPR, and Ca2+ to promote its effects. NO, cGMP, and cADPR have all also been shown to mediate ABA-induced stomatal closure (Neill et al., 2003; Garcia-Mata and Lamattina, 2002). The cPTIO inhibition during this process of the ABA-induced inactivation of the Ca2+-dependent inward rectifying K+ channel and activation of the outward rectifying Cl– channel (Garcia-Mata et al., 2003) strongly implicates NO and Ca2+ in the signalling cascade that may operate.
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Mammals, vertebrates, insects, and many lower eukaryotes possess sGCs with a haem domain capable of binding NO. Bacterial sGCs contain a similar NO binding domain termed the H-NOX domain (Karow et al., 2004; Boon et al., 2006). However, plant homologues of the animal NO sensitive sGC have yet to be identified. The Arabidopsis guanylyl cyclase, AtGC1, is apparently not activated by NO (Ludidi and Gehring, 2003). Thus, the question remains as to how and by what signalling process NO induces a rise in the level of cGMP in plants and it may be that plant enzymes that generate cGMP in response to this gas are quite different from their mammalian counterparts. Indeed, a recent report has demonstrated that the Arabidopsis brassinosteroid receptor BRI1 contains a domain with guanylyl cyclase activity (Kwezi et al., 2007) indicating that there may well be more novel plant guanylyl cyclases awaiting discovery.
The redox chemistry of NO facilitates its reaction with iron–sulphur and haem groups which are present in a number of different proteins. In addition, NO may also signal its presence through other mechanisms such as either direct S-nitrosylation or indirect trans-nitrosylation of either protein cysteine residues or low molecular weight compounds such as glutathione or via peroxynitrite nitration of tyrosine residues (Fig. 2; see Mur et al., 2006, for an excellent discussion of NO chemistry). In animals, S-nitrosylation has been shown to regulate a number of signalling processes, stuctural proteins, and metabolic pathways and has become established as the prototype redox-based, post-translational protein modification in the animal kingdom (Wang et al., 2006). In plants, evidence is now beginning to emerge that S-nitrosylation may also play an important role in NO signalling. A number of proteins appeared to become S-nitrosylated when extracts of Arabidopsis cell cultures were treated with GSNO and SNO-containing proteins isolated by the biotin switch method (Lindermayr et al., 2005). The proteins identified were involved in a wide range of cellular processes. However, their in vivo S-nitrosylation and its biological significance remain to be seen. The in vitro activity of one of three recombinant methionine adenosyl transferase isoforms has been shown to be altered by S-nitrosylation in a manner dependent on the presence or absence of Cys-114 (Lindermayr et al., 2006). Similarly, the activity of an Arabidopsis metacaspase appears to be dependent on the nitrosylation of a critical cysteine residue (Belenghi et al., 2007). Under lowered partial pressures of O2 the mammalian RyR1 calcium channel also becomes S-nitrosylated on a specific Cys residue at physiologically relevant NO levels and in a manner dependent on the presence of calmodulin (Eu et al., 2000). Should this occur in plants, it would have obvious relevance in terms of NO signalling and responses and there is some work suggesting that this may be the case in stomatal guard cells (Sokolovski and Blatt, 2004).
As protein S-nitrosylation can be mediated by GSNO, formed by the S-nitrosylation of GSH (Wang et al., 2006), the degree of protein S-nitrosylation and thus, ‘NO activity’, will be reflected in the availability of reactive GSNO. An Arabidopsis GSNO reductase, AtGSNOR1, has now been identified and its biological importance highlighted (Sakamoto et al., 2002; Diaz et al., 2003; Feechan et al., 2005). Loss-of-function mutations of this gene increased S-nitrosylation levels and disabled R (Resistance)-gene related defence responses against microbial pathogens (Feechan et al., 2005). Conversely, gain-of-function mutants were enhanced in their defensive ability. It was demonstrated that AtGSNOR1 positively regulated the signalling network controlled by the plant immune system activator, salicylic acid. In pea, both GSNO reductase activity and gene expression are decreased by cadmium stress (Barroso et al., 2006). Thus, there is definitely a case for S-nitrosylation being involved in signalling pathways which may include that for NO. Obviously the study of S-nitrosylation in plants is in its infancy and much work is required to determine on which specific proteins it occurs in vivo during the different physiological processes regulated by NO. Various protein S-nitrosylation motifs have also been suggested, based on the appropriate regions of animal proteins that are known to be affected. Wang et al. (2006) suggested the motif [HKR]-C-[VILMFWC]-x-[DE] as that targeted by NO and the motif [GSTCYNQ]-[KRHDE]-C-[DE] has been suggested as that targeted by GSNO. Scanning the Arabidopsis protein databases with these motifs yields 231 and 241 hits, respectively. While the proteins identified include a number of MAP kinases and other signalling proteins, none of those identified as being S-nitrosylated by Lindermayer et al. (2005) are present in the lists of proteins generated. Thus, there is probably no substitute for laboratory-based investigations in this case. However, a number of potential, bioinformatically-generated targets could be examined in transgenic mutant complementation experiments where the highlighted Cys is either present or absent for nitrosylation in the complementing protein.
It is also possible that NO signals via the nitration of tyrosine residues. Tyrosine nitration is mediated by reactive nitrogen species such as the peroxynitrite anion (ONOO–) and nitrogen dioxide (NO2) which are formed during the metabolism of NO in the presence of oxidants such as superoxide radicals (O
), hydrogen peroxide (H2O2), and transition metal centres (Radi, 2004). Although the peroxynitrite anion can cause tyrosine nitration in vitro, its role in this process has been questioned and alternative mechanisms have come to the fore that depend on the formation of NO2 by the action of haem peroxidases on nitrite (Brennan et al., 2002). A number of recombinant Arabidopsis haemoglobins that exhibit peroxidase-like activity and differentially mediate nitrite-dependent protein nitration in vitro have been identified (Sakamoto et al., 2004). Endogenous protein tyrosine nitration has also been demonstrated, in mutant tobacco plants with greatly increased amounts of NO (Morot-Gaudry et al., 2002) and more recently in olive leaves where the amount of tyrosine nitrated proteins increased under salt stress (Valderrama et al., 2007). Thus, the extent and biological significance of protein nitration and whether or not what appears to be a non-reversible reaction can act as a signalling process, presumably in tandem with protein turnover, remains to be determined.
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NO movement |
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TopAbstractIntroductionNO generation and removal...NO perceptionNO movementNO evolution from plantsConclusionsReferences |
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It is possible that NO can diffuse within a cell from a specific site of generation, say in the mitochondria, to other regions of the cell where it might induce an effect by interaction with specific target proteins. It is also possible that NO can diffuse out of the cell across the plasma membrane into adjacent cells and thereby create a small region of cells responding to NO. However, whether or not NO does diffuse within and between cells and if it does how far it moves remains unknown. Given that cells clearly contain many proteins and other molecules that react with NO, it might be that such diffusion is limited. This could of course be the case unless the NO concentration were to be sufficiently high, not necessarily across the whole cell, but perhaps in a microlocale within the cell, so as to saturate, transiently at least, such ‘NO-binding molecules’ in its immediate vicinity. This would leave non-reacted NO free to diffuse across and out of cells. It is likely that cellular regions do have higher local NO concentrations either because they contain the biochemical machinery required for NO synthesis or because NO accumulates preferentially in such regions. For example, NO is more soluble in lipid than water and so may accumulate preferentially in membranes where its rates of reaction with any interacting molecules may be consequently higher (Liu et al., 1998). Different stimuli may activate NO synthesis either by different mechanisms and/or in different subcellular compartments and there may also be a directional focus. For example, a bacterium or fungal hypha may abut only one region of a plant cell and the resultant signalling might activate NO generation in only a proximal and discrete region of the cell. If NO-response proteins such as ion channels or second messenger-generating enzymes are also co-located then one could envisage local ‘NO hot-spots’ and NO signalling micro-domains (Fig. 3). Although it may well be technically difficult to monitor NO transport, it may be informative to apply NO via a point source to the exterior or interior of a tissue and then to monitor real-time NO movement by, for instance, fluorescent imaging using a NO-sensing dye such as DAF-2DA.
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An alternative, but not exclusive scenario for NO transport might be that its generation is elevated in discrete regions owing to localized stimulation resulting from the long-distance transport and site-specific accumulation of compounds such as the hormones ABA or IAA that can stimulate its production. Directional transport of IAA is well-known, particularly with respect to its role in mediating tropic responses to gravity and light. NO has been implicated in gravity signalling with localized NO accumulation being induced either by gravistimulation or asymmetric IAA application and prevented by the inhibition of IAA transport (Hu et al., 2005). The systemic transport of ‘defence-signals’ is activated by pathogen challenge and it may be that these signals also stimulate NO generation at sites distant from those of the initial pathogen perception.
Another possibility awaiting clarification is that NO precursors or ‘NO storage compounds’ may be transported with either NO generation or release occurring at distant sites in a manner analogous to the transport of the ethylene precursor ACC. GSNO has been suggested as one transportable form of NO and although it has not yet been unequivocally identified in plants, a recent report demonstrated cross-reactivity with an anti-GSNO antibody in pea collenchyma cells and immunofluorescence microscopy indicated that the GSNO content decreased dramatically under cadmium stress (Barroso et al., 2006). GSNO has recently been demonstrated in leaf vascular tissue and shown to increase under salt stress using confocal laser microscopy (Valderrama et al., 2007). Glutathione is also present at high (e.g. millimolar levels in wheat) concentrations in phloem cells (Bourgis et al., 1999). Arginine and nitrite could also serve as transported NO precursors. Nitrite concentrations in the phloem and xylem are unknown. However, whole tissue nitrite concentrations, which are typically 10–20 µM, can be transiently raised above this level (Rockel et al., 2002) which may be indicative of the movement of NO precursors. Arginine concentrations can be quite high [e.g. 250 µM in Arabidopsis leaves (Modolo et al., 2006) and 300–800 µM in melon phloem] and, interestingly, can be increased by ABA treatment (Mitchell and Madore, 1992).
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NO evolution from plants |
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TopAbstractIntroductionNO generation and removal...NO perceptionNO movementNO evolution from plantsConclusionsReferences |
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There can be no doubt that NO is evolved from plants. Such evolution, measured as NOx (a mixture of NO and NO2), was first reported in the 1980s and shown to be increased by treatment with salicylic acid and various other compounds (Harper, 1981; Dean and Harper, 1986; Klepper,1990). Wildt et al. (1997) measured NO emissions from several species and several other reports have demonstrated that NO evolution from plants can increase or decrease in response to treatments such as pathogen challenge, water stress, exposure to UV-B, the application of fungicides, and anoxic conditions (Lesham and Haramaty, 1996; Clarke et al., 2000; Magalhaes et al., 2000; Rockel et al., 2002; Hari et al., 2003; Conrath et al., 2004; Perazzolli et al., 2004; Mur et al., 2005, 2006). However, there are a number of technical and biological uncertainties with these measurements and quite varied rates of NO evolution have been estimated using a variety of different measuring techniques. Of course, it is also difficult to gauge the biological significance of the NO evolved. Typically, the rates of evolution are in the nmol g–1 h–1 range (Table 1). A key question is whether or not this NO evolution reflects increased concentrations of biologically active NO in planta. In some cases, this seems likely to be the case. For example, during responses to pathogen challenge there are good correlations between NO evolution and the biological responses that occur. Such correlations have been shown using either NO scavengers and NO synthesis inhibitors or virulent and avirulent pathogens. However, as pointed out by Planchet and Kaiser (2006a, b), estimates of intracellular NO content and rates of NO evolution do not always agree. For example, during anoxia NO is generated at a much higher level than is probably required for its cell signalling function. Such paradoxes remain to be resolved, but the concept of localized NO generation and action (Fig. 3) may partly explain them.
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It is not known if NO released from one part of a plant can induce effects on either other parts of the same plant or on adjacent plants. Agricultural soils can also release substantial amounts of NO (Davidson and Kingerlee, 1997). Certainly, NO gas does have effects on plant biology. Indeed, the early work on NO concerned its effects as an air pollutant (Mansfield, 2002). NO is still an air pollutant today and plants in urban areas or close to traffic are likely to receive higher chronic and more acute exposures than those in rural areas (rural locations 7–70 nl l–1, urban 20–900 nl l–1; Environment Agency, 2006). The early work showed that NO at 50–500 nl l–1 (urban smog [NO]
5000 nl l–1) could retard growth and inhibit photosynthesis (Mansfield, 2002) and other studies have shown that trace amounts of NO in smoke can stimulate seed germination (Keely and Fotheringham, 1997). This latter work has recently been questioned (Baldwin et al., 2005), but physiological concentrations of NO gas do appear to stimulate seed germination (Bethke et al., 2006) and very short exposures to high concentrations of NO gas have substantial effects on the transcriptome (Huang et al., 2004). Thus, there is much fertile ground for further research. For instance, does NO released by plants contribute to the global N economy? Under waterlogged conditions plant NO evolution may be substantial. Does NO, after reaction with other atmospheric gases such as ozone, contribute to the ‘Greenhouse Effect’ and what effects does atmospheric NO have on plants? |
Conclusions |
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TopAbstractIntroductionNO generation and removal...NO perceptionNO movementNO evolution from plantsConclusionsReferences |
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Clearly there is still much to be discovered about NO synthesis, evolution, and perception in plants. NO is undoubtedly made by plant cells and has a range of biological activities. Therefore, it would seem likely that the processes by which NO is made and removed are subject to regulation. Even though the details remain to be resolved, it is clear that various stimuli can increase the rate of NO production and that altering NO turnover in cells, either by modulating its production or removal, does have biological effects. NO is evolved from plants and the rate of evolution can be dramatically increased in response to various stimuli, but the physiological significance of such evolution is not clear. Increased NO evolution probably reflects increased cellular NO generation, but whether NO derived from different intracellular sources is evolved at different rates or from different cells is not known. NO appears to be generated locally in response to mobile signals, but again it remains to be seen if either NO per se acts as a mobile, diffusible signal or if NO reservoirs or precursors are transported and importantly, whether or not such transport is regulated. NO reacts with many other molecules inside and outside of cells. This includes reactions with oxygen to form nitrogen oxides, with GSH and proteins during the S-nitrosylation of thiol residues and with superoxide to form peroxynitrite during the nitration of tyrosine residues within proteins. Thus, NO perception may well involve several mechanisms and it could be that NO is unlikely to travel far even within a single cell and, consequently, not far between cells. It is possible that local pathogen or hormone induced ‘NO-hotspots’ exist within cells and tissues and that the extent and duration of the accumulation of NO at these sites is a balance between synthesis and removal. There is clearly much we do not know.
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Acknowledgements |
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Work in the authors’ laboratory was supported by BBSRC, the Leverhulme Trust, and the Wellcome Trust.
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