JXB Advance Access originally published online on January 22, 2008
Journal of Experimental Botany 2008 59(2):155-163; doi:10.1093/jxb/erm197
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
FOCUS PAPER |
Nitric oxide signalling in plants: interplays with Ca2+ and protein kinases
1Unité Mixte de Recherche INRA 1088/CNRS 5184/Université de Bourgogne, Plante-Microbe-Environnement, 17 rue Sully, BP 86510, F-21065 Dijon cedex, France
2Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland
To whom correspondence should be addressed. E-mail: wendehen{at}dijon.inra.fr
Received 14 June 2007; Revised 23 July 2007 Accepted 26 July 2007
 |
Abstract |
|---|
 Top Abstract IntroductionInterplay of NO and...Protein kinases as targets...ConclusionReferences |
|---|
Much attention has been paid to nitric oxide (NO) research since its discovery as a physiological mediator of plant defence responses. In recent years, newer roles have been attributed to NO, ranging from root development to stomatal closure. The molecular mechanisms underlying NO action in plants are just begun to emerge. The currently available data illustrate that NO can directly influence the activity of target proteins through nitrosylation and has the capacity to act as a Ca2+-mobilizing intracellular messenger. The interplay between NO and Ca2+ has important functional implications, expanding and enriching the possibilities for modulating transduction processes. Furthermore, protein kinases regulated through NO-dependent mechanisms are being discovered, offering fresh perspective on processes such as stress tolerance.
Key words: Ca2+, cADPR, nitric oxide, protein kinases, signalling, SnRK2
|
Introduction |
|---|
|
TopAbstractIntroductionInterplay of NO and...Protein kinases as targets...ConclusionReferences |
|---|
If one lists the number of cellular processes under the control of NO in animals, the physiological importance of NO becomes immediately apparent. NO was reported to play pivotal roles in synaptic transmission, vasodilatation, erection, egg fertilization, defence against pathogenic micro-organisms, and apoptosis (Schmidt and Walter, 1994). Exactly how NO exerts such diversity of functions is the subject of intense study. An increasing body of evidence indicates that NO, and derived species such as peroxynitrite (ONOO–), exert part of their biological activities by chemical modification of protein targets (Bogdan, 2001). These include the nitrosylation, nitrosation, nitration, and oxidation of proteins (Bogdan et al., 2000). In particular, nitrosylation, that is the direct binding of an NO group to a transition metal or cysteine residues (Mannick and Schonhoff, 2002), is emerging as an important post-translational modification of proteins. More than 100 proteins have been found to undergo reversible regulation by nitrosylation in vitro and/or in vivo (Hanafy et al., 2001; Stamler et al., 2001). Remarkably, the broad spectrum of functions ascribed to proteins found to be nitrosylated affects essentially all major cellular activities, highlighting the multifunctional roles of NO (Stamler et al., 2001). Furthermore, nitrosylation is one of the molecular strategies used for signalling (Hess et al., 2005). Accordingly, through nitrosylation, NO was shown to regulate key signalling-related proteins including the soluble guanylate cyclase (sGC), the small GTP-binding protein p21ras, and a number of Ca2+-permeable channels (Mannick and Schonhoff, 2002). Furthermore, NO-dependent regulation of protein kinase activities occurs by nitrosylation of the kinases themselves or by modulation of interacting/upstream factors such as cGMP, Ca2+, p21ras or protein phosphatases (Beck et al., 1999). It is worth realizing that the analysis of the cross-talk operating between NO, protein kinases, and the second messengers Ca2+ and cGMP provided a framework for understanding the molecular bases of major physiological processes, such as egg fertilization or modulation of neuronal excitability (Willmott et al., 1996; Ahern et al., 2002).
The past few years have seen an increasing number of studies dedicated to NO functions in plants. NO appears to be involved in plant developmental processes and participates in a number of physiological processes such as stomatal closure, flowering, response to environmental stresses, and cell death (for reviews see Lamattina et al., 2003; Wendehenne et al., 2004; Delledonne, 2005; Lamotte et al., 2005). Understanding of the mechanisms by which NO contributes to these processes is still in its infancy, but promising results are being obtained. Notably, the identification of NO target proteins and genes whose expression is regulated by NO has already borne fruit, indicating that NO can directly influence the activity of plant proteins as well as the signalling cascade leading to gene expression (Lindermayr et al., 2005, 2006; Grun et al., 2006; Belenghi et al., 2007). These observations also paved the way for research into NO involvement in plant signalling. This article focuses on advances in the characterization of NO signalling activities in plants with respect to its cross-talk with Ca2+ and protein kinases.
|
Interplay of NO and Ca2+ |
|---|
|
TopAbstractIntroductionInterplay of NO and...Protein kinases as targets...ConclusionReferences |
|---|
Ca2+ is well established as a universal intracellular second messenger (Sanders et al., 2002; Petersen et al., 2005). Notably, increases in cytosolic free Ca2+ concentration ([Ca2+]cyt) have been detected in response to a wide range of environmental, developmental, and growth stimuli (Lecourieux et al., 2006). According to the ‘Ca2+ signature hypothesis’, each stimulus induces Ca2+ transients which have unique temporal and spatial arrangements determining the specificity of the physiological response (Scrase-Field and Knight, 2003). The changes in [Ca2+]cyt are decoded and relayed through Ca2+ sensors such as calmodulins (CaMs), CDPKs (Ca2+-Dependent Protein Kinases) or annexins (Berridge et al., 2003). Interestingly, recent progress on animal cells have highlighted that, similarly to Ca2+ signalling, NO signalling might display spatial and temporal organization (Stamler et al., 2001). Accordingly, several NO-signalling components such as Ca2+-permeable channels, p21ras, sGC, and MAPKs (Mitogen-Activated Protein Kinases) are organized into macromolecular complexes in which NO signalling functions within highly localized environments (Kone et al., 2003). The complementary aspect of NO and Ca2+ signalling is reinforced by the occurrence of transduction networks in which Ca2+ acts both as a promoter and a sensor of NO signalling (Clementi, 1998). In plants, concomitant changes in [Ca2+]cyt and NO levels are apparent during the transduction of biotic and abiotic signals (Garcia-Mata et al., 2003; Gould et al., 2003; Lamotte et al., 2004; Vandelle et al., 2006). As reported in animal cells, growing evidence suggest that these two messengers may interact in subtle ways.
Ca2+-dependence of NO synthesis
Current reports show that there are at least two main enzymatic routes for NO synthesis in plants: a nitrite-dependent pathway and a L-arginine-dependent pathway. The nitrite pathway mainly involves nitrate reductase (NR) which catalyses the NAD(P)H reduction of nitrite to NO (Yamasaki et al., 1999), and a root-specific plasma membrane-bound nitrite reductase not identified yet (Stöhr et al., 2001). NR is the only enzyme whose NO-producing activity has been rigorously confirmed both in vivo and in vitro. A question that still arises is whether the NR-derived NO can act as a signal or whether it is just the product of an enzyme side reaction (Desikan et al., 2002; Meyer et al., 2005; Bright et al., 2006; Crawford, 2006; Modolo et al., 2006). Whatever scenario, no functional link between Ca2+ and NR-mediated NO synthesis has been reported so far. The L-arginine-dependent pathway is based principally on the assumption that plants do possess nitric oxide synthase (NOS)-like enzyme(s). In animals, NOSs catalyse the conversion of L-arginine to L-citrulline and NO. Activities of the constitutive isoforms of mammalian NOSs (cNOSs) are strictly CaM/Ca2+-dependent (Bogdan, 2001). During the past decade, there has been an increasing number of reports showing the presence of NOS activity in plants and a candidate catalysing a L-arginine-dependent NO synthesis has been identified (Guo et al., 2003). However, its ability to catalyse NO synthesis has been questioned and a mechanism for L-arginine-dependent NO synthesis in plants is still unknown (Crawford et al., 2006; Zemojtel et al., 2006). Interestingly, plant NOS activity measured in several plant species and various tissues requires Ca2+ and CaM as cofactors, suggesting that Ca2+ or Ca2+-bound CaM might directly interact with the plant NOS-like enzyme (Delledonne et al., 1998; Modolo et al., 2002; Corpas et al., 2004, 2006; del Rio et al., 2004). The importance of Ca2+ in L-arginine-dependent NO synthesis is further supported by experiments showing that elicitor-induced NO synthesis in tobacco and grapevine cells was suppressed by pharmacological agents that inhibit mammalian NOS activities and increases in [Ca2+]cyt (Lamotte et al., 2004; Vandelle et al., 2006). In agreement with these findings, in a recent study by Ali et al. (2007) genetic evidence has been provided that lipopolysaccharide-induced NO synthesis, which was found to be suppressed by mammalian NOS inhibitors, is controlled by an upstream Ca2+ influx mediated by the plasma membrane Ca2+-permeable channel cyclic-nucleotide-gated channel (CNGC)2. In addition, NO synthesis catalysed by NOS-like-enzyme(s) was shown to be up-regulated by H2O2-, SA- (salicylic acid), and aldehyde-induced elevations of [Ca2+]cyt in various plant species and phytoplankton populations (Lum et al., 2002; Allen et al., 2006; Zottini et al., 2007). While these studies did not ascertain a direct interacting role for Ca2+ with plant NOS-like enzyme, they provided physiological evidence that changes of [Ca2+]cyt might be involved intimately in mediating NO synthesis in plant cells and that NO appears as a step in the signalling cascade initiated by the cation.
NO as a Ca2+-mobilizing agent
In animals, NO regulates Ca2+ channel activities through different mechanisms: direct S-nitrosylation or indirect modulation via cGMP-dependent cascades (Fig. 1). S-nitrosylated Ca2+ channels include voltage-gated Ca2+ channels (P/Q- and L-type), CNGC, ryanodine receptors (RyR), and the N-methyl D-aspartate receptor (Clementi, 1998; Ahern et al., 2002). For example, NO was reported to enhance the activity of type 1 RYR by S-nitrosylation of a single cysteine (Sun et al., 2001). The NO-cGMP cascade modulates the activity of L-, T-, and N-type voltage-gated Ca2+ channels, CNGC, inositol (1,4,5)-triphosphate receptor, and RyR (Clementi, 1998; Ahern et al., 2002). Cyclic GMP targets Ca2+ channels by virtue of their cyclic nucleotide binding sites (particularly in the case of CNGC) or mediates its effects through serine/threonine cGMP-dependent protein kinases (PKGs). It is especially noteworthy that protein sequences from practically every type of ion channel contain PKG consensus phosphorylation sites (Ahern et al., 2002). To add further to the complexity of this picture, in various cell types PKGs trigger the activation of RYR by promoting the synthesis of the nicotinamide adenine dinucleotide (NAD+) metabolite cyclic ADP ribose (Fig. 1). Furthermore, NO also decreases [Ca2+]cyt by activating plasma membrane and endomembrane Ca2+ transporters (Clementi, 1998; Fig. 1). The detailed mechanism of this action is still unclear and might involve both nitrosylation and cGMP-dependent processes (see, for instance, Yao and Huang, 2003). Because cNOSs activity is strictly Ca2+-dependent, the finding discussed above also indicates that NO exerts a positive or a negative feedback control of its own production by promoting activation or inhibition of Ca2+-channels and Ca2+ transporters, respectively.
|
The first arguments that Ca2+ might participate downstream of NO in plant signal transduction pathways were provided by Durner et al. (1998) and Klessig et al. (2000). These authors showed that the cADPR antagonist 8-bromo-cADPR reduces and delays NO-induced accumulation of PR (Pathogenesis-Related)-1 transcripts in tobacco leaves. Accordingly, cADPR itself caused substantial PR-1 expression through a mechanism sensitive to RyR inhibitors. This set of observations provided evidence that the dynamic regulation of plant gene expression by NO could take place via a NO-cADPR-Ca2+ cascade. Subsequent studies have partly reinforced this conclusion. First, artificially generated NO has been reported to raise [Ca2+]cyt of Vicia faba guard cells by promoting Ca2+ release from intracellular stores (Garcia-Mata et al., 2003). The rise in [Ca2+]cyt was blocked by sGC and RYR inhibitors, establishing cGMP as a putative mediator for NO-induced activation of cADPR-dependent endomembrane Ca2+ channels. A similar situation was found by analysing the effects of the non-thiol NO donor DEA-NONOate in tobacco cell suspensions expressing the Ca2+ reporter apoaequorin in the cytosol (Lamotte et al., 2004, 2006). Here too, NO markedly enhanced the [Ca2+]cyt through a process sensitive to 8-bromo-cADPR, indicating that NO-induced Ca2+ mobilization operates predominantly via a cADPR-mediated Ca2+-release mechanism. Interestingly, these latter studies also pointed to a role for NO in modulating plasma membrane Ca2+-permeable channels. Indeed, NO released by DEA-NONOate was found to trigger a fast and transient influx of extracellular Ca2+ in tobacco cells. Because the NO-evoked Ca2+ influx occurred concomitantly with a Ca2+-independent plasma membrane depolarization, it was assumed that NO may promote the opening of voltage-gated Ca2+ channels subsequent to membrane depolarization (Lamotte et al., 2006). At present, however, the exact mechanisms of NO-induced plasma membrane depolarization remain to be elucidated. Recent work has suggested that NO might modulate plasma membrane Ca2+-permeable channels by showing that NO negatively regulates Ca2+ entry in grapevine cells challenged by the elicitor endopolygalacturonase 1 (Vandelle et al., 2006). This finding is of particular interest because it expands the role of NO in plant signalling as a more general regulator of Ca2+ homeostasis, promoting both activation and/or inhibition of Ca2+ fluxes. As reported in endothelial cells or neurons, a negative feedback could serve to protect cells from the detrimental effects of excessive NO and Ca2+ (see, for instance, Yao and Huang, 2003). Finally, it should be mentioned that artificially generated NO did not evoke rises in nuclear free Ca2+ concentration in tobacco cell suspensions expressing apoaequorin in the nucleus (Lecourieux et al., 2005). Therefore, NO action on Ca2+ homeostasis might be restricted to specific cellular compartments.
Although these studies support a possible link between NO, cADPR, cGMP, and Ca2+, a note of caution is required. First of all, it remains to be seen whether the level of cADPR changes in response to NO-dependent processes. Second, while the ability of NO to induce cGMP synthesis in plant cells is well established (Durner et al., 1998; Hu et al., 2005), the plant NO-sensitive sGC-like enzyme is unknown. Finally, although several investigators have reported the requirement of phosphorylation-dependent events in the mediation of NO-induced Ca2+ mobilization (Sokolovski et al., 2005; Lamotte et al., 2006), plant PKGs have not yet been identified. Therefore, at this stage of knowledge, the conclusion that the NO signalling pathway leading to Ca2+ mobilization in plants is similar to that defined in animals remains speculative.
Several studies supportive of a potential role for NO as an endogenous regulator of Ca2+ mobilization in physiological contexts have been reported. Notably, it has been shown that NO contributes to [Ca2+]cyt increases in plant cells exposed to biotic and abiotic stresses including hyper-osmotic stresses and elicitors of defence responses (Gould et al., 2003; Lamotte et al., 2004, 2006; Vandelle et al., 2006). For example, a specific role for NO in activating intracellular Ca2+ channels was assumed through pharmacological and biochemical approaches in tobacco and grapevine cells exposed to the elicitors cryptogein and endopolygalacturonase 1, respectively (Lamotte et al., 2004; Vandelle et al., 2006). Furthermore, pharmacological experiments suggested that NO is active upstream of [Ca2+]cyt transients during the processes of ABA-induced stomatal closure and auxin–induced adventitious root formation (Desikan et al., 2002; Lanteri et al., 2006).
These studies also raise the question of how the NO-mediated Ca2+ fluxes are propagated downstream into cellular responses. Clearly, this aspect has been poorly investigated. However, it is likely that protein kinases might represent an important pathway by which NO-dependent Ca2+ signals are decoded. Recently, a 50 kDa CDPK, the activity of which was induced by NO through a Ca2+-dependent process, was characterized in cucumber explants (Lanteri et al., 2006). The 50 kDa CDPK might contribute to NO-induced adventious root formation. Likewise, in our laboratory, evidence was obtained that the activation of the tobacco MAPK SIPK (Salicylic acid-Induced Protein Kinase) by NO donors (Klessig et al., 2000) requires a transient influx of extracellular Ca2+ in tobacco cells (C Courtois and D Wendehenne, unpublished data).
Another puzzling aspect to discuss here is the cellular impact of the NO/Ca2+ pathway. Here too, the first hypotheses have only just begun to emerge. First, a rise in [Ca2+]cyt may serve to initiate but also to amplify and/or maintain NO production. Accordingly, Lamotte et al. (2004) showed that addition of inhibitors of plasma membrane Ca2+-permeable channels in the mid-course of cryptogein-induced NO synthesis in tobacco cell suspensions suppressed NO production within minutes. Second, by elevating [Ca2+]cyt, NO might influence indirectly the activity of proteins including protein kinases (see above) and Ca2+-sensitive K+ and Cl– channels as described in guard cells (Garcia-Mata et al., 2003). Third, based on animal studies (see, for instance, Peunova and Enikolopov, 1993) and the data discussed above, it is reasonable to speculate that NO/Ca2+ pathways, as well as the combined action of NO and Ca2+, might modulate the transcriptional regulation of specific set of genes involved, for instance, in disease resistance or developmental processes. Finally, it seems plausible that interplays of NO and Ca2+ might be implicated in cell death. This idea is supported by the fact that both NO and Ca2+ are triggers and modulators of cell death (Lam, 2004; Delledonne, 2005). This hypothesis is further reinforced by the finding that H2O2, which acts in concert with NO in triggering cell death (Delledonne et al., 2001; Zago et al., 2006), also contributes to stimulus-induced [Ca2+]cyt changes (Garcia-Brugger et al., 2006; Lecourieux et al., 2006). Mechanistically, Ca2+ might represent a signalling carrier of NO and/or H2O2-triggered cell death pathways or, as described in animal cells, cell death could also be related to the cellular Ca2+ overload or perturbation of intracellular compartmentalization resulting from NO- and/or H2O2-induced Ca2+ fluxes (Orrenius et al., 2003). Therefore, understanding of the mechanisms underlying cell death should also include experiments designed to delineate the cross-talk between Ca2+, NO, and H2O2 in further detail.
|
Protein kinases as targets for NO action |
|---|
|
TopAbstractIntroductionInterplay of NO and...Protein kinases as targets...ConclusionReferences |
|---|
In animal cells, NO modulates the activity of distinct classes of protein kinases that play a key role in signal transduction, including MAPK cascades, protein kinase C, and Janus kinases (Beck et al., 1999). Furthermore, kinases related to primary metabolism such as pyruvate kinase were reported to be activated or inhibited by S-nitrosylation (Gao et al., 2005). In plants, the possibility that NO might influence protein kinase activities has been poorly explored and most of the available data come from studies based on artificially generated NO. NO-dependent activation of protein kinases exhibiting, for instance, MAPK or CDPK properties were reported in A. thaliana suspension cell cultures and roots (Clarke et al., 2000; Capone et al., 2004), cucumber explants (Pagnussat et al., 2004; Lanteri et al., 2006) and tobacco leaves and suspension cell cultures (Klessig et al., 2000; Yamamoto et al., 2004). With the exception of SIPK (Klessig et al., 2000), none of these protein kinases has been identified. Furthermore, the NO donor SNP was shown to increase the amount and histone H1 phosphorylating activity of the p34cdc2 cyclin-dependent kinase in auxin-treated alfalfa protoplasts (Ötvös et al., 2005). The NO-induced activation of these kinases has been thought to be part of processes related to defence responses and/or cell death (Clarke et al., 2000; Klessig et al., 2000; Yamamoto et al., 2004) and to auxin-mediated adventitious root formation and cell division (Pagnussat et al., 2004; Ötvös et al., 2005; Lanteri et al., 2006). Finally, it should be mentioned that several kinases including phosphoglycerate kinase, nucleoside diphosphate kinase, and adenosine kinase have been shown to be S-nitrosylated in vitro (Lindermayr et al., 2005). The biological relevance of the S-nitrosylation of these kinases has not yet been defined.
The first evidence that NO modulates the activation of a member of the plant SNF1-related protein kinase 2 (SnRK2) subfamily has been reported recently (Lamotte et al., 2006). Plant SnRKs are classified into three subfamilies: SnRK1, SnRK2, and SnRK3, the SnRK2 and SnRK3 subfamilies being specific to plants (Harmon, 2003). Members of the SnRK2 subfamily function in abiotic stress signalling and include the tobacco 42 kDa protein kinase NtOSAK (Nicotiana tabacum Osmotic Stress-Activated Protein Kinase; Mikolajczyk et al., 2000). NtOSAK is activated very rapidly in response to osmotic stress through phosphorylation of two serine residues (154 and 158) located within the enzyme activation loop (Burza et al., 2006). In our laboratory, it has been demonstrated that the NO donor DEA/NONOate induced a fast and transient activation of NtOSAK in tobacco suspension cell cultures (Lamotte et al., 2006). Furthermore, evidence has been provided that NO might be a key component of the hyperosmotic stress-induced signalling cascade leading to NtOSAK activation. An attempt was also made to clarify the NO-dependent upstream pathway of NtOSAK activation. Initial data established that neither NO-mediated Ca2+ influx nor Ca2+ release from internal stores were required for NtOSAK activation (Lamotte et al., 2006). Among the other possibilities, NtOSAK activity might be up-regulated through phosphorylation by an upstream NO-dependent protein kinase, by auto-phosphorylation, and/or through direct S-nitrosylation or nitration by NO-derived species. Preliminary experiments are not in favour of the last possibility.
The question that further comes to mind is the incidence of the NO/NtOSAK pathway on the cell response. Protein kinases of the SnRK2 subfamily are activated by osmolytes and some of them by ABA as well, highlighting a role for these enzymes in a general response to osmotic stress (Boudsocq et al., 2004; Kobayashi et al., 2004). The SnRK2 kinases present in guard cells, AAPK (ABA-Activated Protein Kinase) from Vicia faba and its Arabidopsis orthologue SnRK2.6/OST1/SRK2E play an important role in ABA signalling in response to drought and regulate stomata closure under low humidity stress (Li et al., 2000; Mustilli et al., 2002; Yoshida et al., 2002). It has been shown that the other Arabidopsis ABA-dependent SnRK2 kinase, SRK2C/SnRK2.8, improves plant drought tolerance, probably by promoting the up-regulation of stress-responsive genes expression, including DREB1A/CBF3 encoding a transcription factor that broadly regulates stress-responsive genes (Umezawa et al., 2004). Several lines of evidence indicate that SnRK2 kinases can also phosphorylate and, in this way, activate transcription activators AREB1 and TRAB1 in Arabidopsis and rice, respectively (Kobayashi et al., 2005; Furihata et al., 2006). These data strongly suggest that SnRK2 protein kinases are involved in the regulation of expression of ABA-responsive genes. Based on these studies, it is plausible that plant cells challenged by osmotic stress might use NO as an early signalling compound acting upstream of SnRK2-induced pathways. This could be true for other plant responses in which both changes in osmotic pressure and NO production are observed, such as responses to pathogens or elicitors of defence responses (Lamotte et al., 2004; Gauthier et al., 2007). Regarding this aspect, it has recently been shown that Arabidopis OST1 kinase and NO production are required in the plant innate immunity against bacterial invasion (Melotto et al., 2006). However, the involvement of NO in OST1 activation was not investigated. Here again, future work will have to clarify this possibility, but the findings so far are certainly promising.
|
Conclusion |
|---|
|
TopAbstractIntroductionInterplay of NO and...Protein kinases as targets...ConclusionReferences |
|---|
The field of nitric oxide in plant biology was born almost ten years ago, when it was first revealed that this free radical gas is involved in defence responses (Delledonne et al., 1998; Durner et al., 1998). Since that time, NO has been shown to function as an ubiquitous molecule with diverse physiological roles. Although much has been learnt about NO, several issues concerning its action remain outstanding. As discussed above, mechanisms through which it might affect transduction processes imply the regulation of key signalling proteins such as protein kinases and Ca2+-permeable channels as well as the mobilization of second messengers including Ca2+, cGMP, and cADPR (Fig. 2). However, little is known at the molecular level concerning these signalling proteins and important goals are to identify them and to investigate how NO modulates their activities. Furthermore, it is necessary to define the physiological relevance of these modulations and to understand how interplays between NO and Ca2+ guide the cell toward a specific response. Such tasks will require functional analysis of the molecular mechanisms that relay NO-dependent Ca2+ signals. Finally, it should be kept in mind that pharmacological evidence for cADPR involvement in mediating NO-induced Ca2+ mobilization has been obtained, but the direct measurement of cellular cADPR levels is urgently required. Although in its infancy, research into the signalling functions of NO in plants is advancing rapidly and there should soon be a much better understanding of this most unusual signalling agent.
|
|
Acknowledgements |
|---|
Studies by the authors were supported by the Conseil Régional de Bourgogne, the Ministère de l'Education Nationale, de la Recherche et de la Technologie, the Institut National de la Recherche Agronomique, the Ministère des Affaires Etrangères (EGIDE Polonium, grant 11545WG), and the Polish Ministry of Education and Science (grant PBZ-KBN-110/PO4/2004).
|
Footnotes |
|---|
* Joint first author.
|
References |
|---|
|
TopAbstractIntroductionInterplay of NO and...Protein kinases as targets...ConclusionReferences |
|---|
Ahern GP, Klyachko VA, Jackson MB. cGMP and S-nitrosylation: two routes for modulation of neuronal excitability by NO. Trends in Neuroscience (2002) 25:510–517.[CrossRef][Web of Science][Medline]
Ali R, Ma W, Lemtiri-Chlieh F, Tsaltas D, Leng Q, von Bodman S, Berkowitz GA. Death don't have no mercy and neither does calcium: Arabidopsis CYCLIC NUCLEOTIDE GATED CHANNEL2 and innate immunity. The Plant Cell (2007) 19:1081–1095.
Allen AE, Vardi A, Bowler C. An ecological and evolutionary context for integrated nitrogen metabolism and related signalling pathways in marine diatoms. Current Opinion in Plant Biology (2006) 9:264–273.[CrossRef][Web of Science][Medline]
Beck KF, Eberhardt W, Frank S, Huwiler A, Messmer UK, Mühl H, Pfeilschifter J. Inducible NO synthase: role in cellular signalling. Journal of Experimental Biology (1999) 202:645–653.[Abstract]
Belenghi B, Romero-Puertas MC, Vercammen D, Brackenier A, Inzé D, Delledonne M, Van Breusegem F. Metacaspase activity of Arabidopsis thaliana is regulated by S-nitrosylation of a critical cysteine residue. Journal of Biological Chemistry (2007) 282:1352–1358.
Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis and remodelling. Nature Reviews Molecular Cell Biology (2003) 4:517–529.[CrossRef][Web of Science][Medline]
Bogdan C. Nitric oxide and the regulation of gene expression. Trends in Cell Biology (2001) 11:66–75.[CrossRef][Web of Science][Medline]
Bogdan C, Röllinghoff M, Diefenbach A. Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Current Opinion in Immunology (2000) 12:64–76.[CrossRef][Web of Science][Medline]
Boudsocq M, Barbier-Brygoo H, Lauriere C. Identification of nine SNF1-related protein kinase 2 activated by hyperosmotic and saline stresses in Arabidopsis thaliana. Journal of Biological Chemistry (2004) 279:41758–41766.
Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ. ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. The Plant Journal (2006) 45:113–122.[CrossRef][Web of Science][Medline]
Burza AM, Pekala I, Sikora J, Siedlecki P, Malagocki P, Bucholc M, Koper L, Zielenkiewicz P, Dadlez M, Dobrowolska G. Nicotiana tabacum osmotic stress-activated kinase is regulated by phosphorylation on Ser-154 and Ser-158 in the kinase activation loop. The Journal of Biological Chemistry (2006) 281:34299–34311.
Capone R, Tiwari BS, Levine A. Rapid transmission of oxidative and nitrosative stress signals from roots to shoots in Arabidopsis. Plant Physiology and Biochemistry (2004) 42:425–428.[CrossRef][Web of Science][Medline]
Clarke A, Desikan R, Hurst RD, Hancock JT, Neill SJ. NO way back: nitric oxide and programmed cell death in Arabidopsis thaliana suspension cultures. The Plant Journal (2000) 24:667–677.[CrossRef][Web of Science][Medline]
Clementi E. Role of nitric oxide and its intracellular signalling pathways in the control of Ca2+ homeostasis. Biochemical Pharmacology (1998) 55:713–718.[CrossRef][Web of Science][Medline]
Corpas FJ, Barroso JB, Carreras A, et al. Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants. Plant Physiology (2004) 136:2722–2733.
Corpas FJ, Barroso JB, Carreras A, Valderrama R, Palma JM, Leon AM, Sandalio LM, del Rio LA. Constitutive arginine-dependent nitric oxide synthase activity in different organs of pea seedlings during plant development. Planta (2006) 224:246–254.[CrossRef][Medline]
Crawford NM. Mechanisms for nitric oxide synthesis in plants. Journal of Experimental Botany (2006) 57:471–478.
Crawford NM, Galli M, Tischner R, Heimer YM, Okamoto M, Mack A. Response to Zemojtel et al: plant nitric oxide synthase: back to square one. Trends in Plant Science (2006) 11:526–527.[CrossRef][Web of Science]
Delledonne M. NO news is good news for plants. Current Opinion in Plant Biology (2005) 8:390–396.[CrossRef][Web of Science][Medline]
Delledonne M, Xia Y, Dixon RA, Lamb C. Nitric oxide functions as a signal in plant disease resistance. Nature (1998) 394:585–588.[CrossRef][Medline]
Delledonne M, Zeier J, Marocco A, Lamb C. Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proceedings of the National Academy of Sciences, USA (2001) 98:13454–13459.
del Rio LA, Corpas FJ, Barroso JB. Nitric oxide and nitric oxide synthase activity in plants. Phytochemistry (2004) 65:783–792.[CrossRef][Web of Science][Medline]
Desikan R, Griffiths R, Hancock J, Neill S. A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA (2002) 99:16314–16318.
Durner J, Wendehenne D, Klessig DF. Defense genes induction in tobacco by nitric oxide, cyclic GMP and cyclic ADP ribose. Proceedings of the National Academy of Sciences, USA (1998) 95:10328–10333.
Furihata T, Maruyama K, Fujita Y, Umezawa T, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K. Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proceedings of the National Academy of Sciences, USA (2006) 103:1988–1993.
Gao C, Guo H, Wei J, Mi Z, Wai PY, Kuo PC. Identification of S-nitrosylated proteins in endotoxin-stimulated RAW264.7 murine macrophages. Nitric Oxide (2005) 12:121–126.[CrossRef][Web of Science][Medline]
Garcia-Brugger A, Lamotte O, Vandelle E, Bourque S, Lecourieux D, Poinssot B, Wendehenne D, Pugin A. Early signalling events induced by elicitors of plant defenses. Molecular Plant–Microbe Interaction (2006) 19:711–724.[CrossRef]
Garcia-Mata C, Gay R, Sokolovski S, Hills A, Lamattina L, Blatt MR. Nitric oxide regulates K+ and Cl– channels in guard cells through a subset of abscisic acid-evoked signalling pathways. Proceedings of the National Academy of Sciences, USA (2003) 100:11116–11121.
Gauthier A, Lamotte O, Reboutier D, Bouteau F, Pugin A, Wendehenne D. Nitrate efflux is an early prerequisite to morphological and biochemical events participating to cryptogein-induced cell death. Plant Signalling and Behavior (2007) 2:89–98.
Gould KS, Lamotte O, Klinguer A, Pugin A, Wendehenne D. Nitric oxide production in tobacco leaf cells: a generalized stress response? Plant, Cell and Environment (2003) 26:1851–1862.[CrossRef]
Grun S, Lindermayr C, Sell S, Durner J. Nitric oxide and gene regulation in plants. Journal of Experimental Botany (2006) 57:507–516.
Guo FQ, Okamoto M, Crawford NM. Identification of a plant nitric oxide synthase gene involved in hormonal signalling. Science (2003) 302:100–103.
Hanafy KA, Krumenacker JS, Murad F. NO, nitrotyrosine, and cyclic GMP in signal transduction. Medical Science Monitoring (2001) 7:801–819.
Harmon AC. Calcium-regulated protein kinases of plants. Gravitational and Space Biology Bulletin (2003) 16:83–90.[Medline]
Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS. Protein S-nitrosylation: purview and parameters. Nature Reviews Molecular Cell Biology (2005) 6:150–166.[CrossRef][Web of Science][Medline]
Hu X, Neill S, Tang Z, Cai W. Nitric oxide mediates gravitropic bending in soybean roots. Plant Physiology (2005) 137:663–670.
Klessig DF, Durner J, Noad R, et al. Nitric oxide and salicylic acid signalling in plant defense. Proceedings of the National Academy of Sciences, USA (2000) 97:8849–8855.
Kobayashi Y, Yamamoto S, Minami H, Kagaya Y, Hattori T. Differential activation of the rice sucrose nonfermenting 1-related protein kinase2 family by hyperosmotic stress and abscisic acid. The Plant Cell (2004) 16:1163–1177.
Kobayashi Y, Murata M, Minami H, Yamamoto S, Kagaya Y, Hobo T, Yamamoto A, Hattori T. Abscisic acid-activated SNRK2 protein kinases function in the gene regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors. The Plant Journal (2005) 44:939–949.[CrossRef][Web of Science][Medline]
Kone BC, Kuncewicz T, Zhang W, Yu ZY. Protein interactions with nitric oxide synthases: controlling the right time, the right place, and the right amount of nitric oxide. American Journal of Renal Physiology (2003) 285:178–190.
Lam E. Controlled cell death, plant survival and development. Nature Molecular and Cell Biology (2004) 5:305–315.[CrossRef]
Lamattina L, Garcia-Mata C, Graziano M, Pagnussat G. Nitric oxide: the versatility of an extensive signal molecule. Annual Review of Plant Biology (2003) 54:109–136.[CrossRef][Medline]
Lamotte O, Gould K, Lecourieux D, Sequeira-Legrand A, Lebrun-Garcia A, Durner J, Pugin A, Wendehenne D. Analysis of nitric oxide signalling functions in tobacco cells challenged by the elicitor cryptogein. Plant Physiology (2004) 135:516–529.
Lamotte O, Courtois C, Barnavon L, Pugin A, Wendehenne D. Nitric oxide in plants: the biosynthesis and cell signalling properties of a fascinating molecule. Planta (2005) 221:1–4.[CrossRef][Web of Science][Medline]
Lamotte O, Courtois C, Dobrowolska G, Besson A, Pugin A, Wendehenne D. Mechanisms of nitric oxide-induced increase of free cytosolic Ca2+ concentration in Nicotiana plumbaginifolia cells. Free Radical Biology and Medicine (2006) 40:1369–1376.[CrossRef][Web of Science][Medline]
Lanteri M, Pagnussat GC, Lamattina L. Calcium and calcium-dependent protein kinases are involved in nitric oxide- and auxin-induced adventitious root formation in cucumber. Journal of Experimental Botany (2006) 57:1341–1351.
Lecourieux D, Lamotte O, Bourque S, Mazars C, Wendehenne D, Ranjeva R, Pugin A. Elicitors induce specific changes in nuclear free calcium in tobacco cell suspensions. Cell Calcium (2005) 38:527–538.[CrossRef][Web of Science][Medline]
Lecourieux D, Ranjeva R, Pugin A. Calcium in plant defence-signalling pathways. New Phytologist (2006) 171:249–269.[CrossRef][Web of Science][Medline]
Li J, Wang XQ, Watson MB, Assmann SM. Regulation of abscisic acid-induced stomatal closure and anion channels by guard cell AAPK kinase. Science (2000) 287:300–303.
Lindermayr C, Saalbach G, Bahnweg G, Durner J. Differential inhibition of Arabidopsis methionine adenosyltransferase by protein S-nitrosylation. Journal of Biological Chemistry (2006) 281:4285–4291.
Lindermayr C, Saalbach G, Durner J. Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiology (2005) 137:921–930.
Lum HK, Butt YK, Lo SC. Hydrogen peroxide induces a rapid production of nitric oxide in mung bean (Phaseolus aureus). Nitric Oxide (2002) 6:205–213.[CrossRef][Web of Science][Medline]
Mannick JB, Schonhoff CM. Nitrosylation: the next phosphorylation? Archive of Biochemistry and Biophysic (2002) 408:1–6.[CrossRef]
Melotto M, Undrewood W, Koczan J, Nomura K, He SY. Plant stomata function in innate immunity against bacterial invasion. Cell (2006) 126:969–980.[CrossRef][Web of Science][Medline]
Meyer C, Lea US, Provan F, Kaiser WM, Lillo C. Is nitrate reductase a major player in the plant NO (nitric oxide) game? Photosynthesis Research (2005) 83:181–189.[CrossRef][Web of Science][Medline]
Mikolajczyk M, Awotunde OS, Muszynska G, Klessig DF, Dobrowolska G. Osmotic stress induces rapid activation of a salicylic acid-induced protein kinase and a homolog of protein kinase ASK1 in tobacco cells. The Plant Cell (2000) 12:165–178.
Modolo LV, Cunha FQ, Braga MR, Salgado I. Nitric oxide synthase-mediated phytoalexin accumulation in soybean cotyledons in response to the Diaporthe phaseolorum f. sp. meridionalis elicitor. Plant Physiology (2002) 130:1288–1297.
Modolo LV, Augusto O, Almeida IMG, Pinto-Maglio CAF, Oliveira HC, Seligman K, Salgado I. Decreased arginine and nitrite levels in nitrate reductase-deficient Arabidopsis thaliana plants impair nitric oxide synthesis and the hypersensitive response to Pseudomonas syringae. Plant Science (2006) 171:34–40.
Mustilli AC, Merlot S, Vavasseur A, Frenzi F, Giraudat J. Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. The Plant Cell (2002) 14:3089–3099.
Orrenius S, Zhivotovsky B, Nicotera P. Regulation of cell death: the calcium-apoptosis link. Nature Molecular and Cell Biology (2003) 4:552–565.[CrossRef]
Ötvos K, Pasternak TP, Miskolczi P, Domoki M, Dorjgotov D, Szücs A, Bottka S, Dudits D, Fehér A. Nitric oxide is required for, and promotes auxin-mediated activation of, cell division and embryogenic cell formation but does not influence cell cycle progression in alfalfa cell cultures. The Plant Journal (2005) 43:849–860.[CrossRef][Web of Science][Medline]
Pagnussat GC, Lanteri ML, Lombardo MC, Lamattina L. Nitric oxide mediates the indole acetic acid induction activation of a mitogen-activated protein kinase cascade involved in adventitious root development. Plant Physiology (2004) 135:279–286.
Petersen OH, Michalak M, Verkhratsky A. Calcium signalling: past, present and future. Cell Calcium (2005) 38:161–169.[CrossRef][Web of Science][Medline]
Peunova N, Enikolopov G. Amplification of calcium-induced gene transcription by nitric oxide in neuronal cells. Nature (1993) 264:450–453.
Sanders D, Pelloux J, Brownlee C, Harper JF. Calcium at the crossroads of signalling. The Plant Cell (2002) 14:401–417.
Schmidt HHHW, Walter U. NO at work. Cell (1994) 78:919–925.[CrossRef][Web of Science][Medline]
Scrase-Field SA, Knight MR. Calcium: just a chemical switch? Current Opinion in Plant Biology (2003) 6:500–506.[CrossRef][Web of Science][Medline]
Sokolovski S, Hills A, Gay R, Garcia-Mata C, Lamattina L, Blatt MR. Protein phosphorylation is a prerequisite for intracellular Ca2+ release and ion channel control by nitric oxide and abscisic acid in guard cells. The Plant Journal (2005) 43:520–529.[CrossRef][Web of Science][Medline]
Stamler JS, Lamas S, Fang FC. Nitrosylation: the prototypic redox-based signalling mechanism. Cell (2001) 106:675–678.[CrossRef][Web of Science][Medline]
Stöhr C, Strube F, Marx G, Ullrich WR, Rockel P. A plasma membrane-bound enzyme of tobacco roots catalyses the formation of nitric oxide from nitrite. Planta (2001) 212:835–841.[CrossRef][Web of Science][Medline]
Sun J, Xin C, Eu JP, Stamler JS, Meissner G. Cysteine-3635 is responsible for skeletal muscle ryanodine receptor modulation by NO. Proceedings of the National Academy of Sciences, USA (2001) 98:11158–11162.
Umezawa T, Yoshida R, Maruyama K, Yamaguchi-Shinozaki K, Shinozaki K. SRK2C, a SNF1-related protein kinase 2, improves drought tolerance by controlling stress-responsive gene expression in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA (2004) 101:17306–17311.
Vandelle E, Poinssot B, Wendehenne D, Bentejac M, Pugin A. Integrated signalling network involving calcium, nitric oxide, active oxygen species but not mitogen-activated protein kinases in BcPG1-elicited grapevine defenses. Molecular Plant–Microbe Interaction (2006) 19:429–440.[CrossRef]
Wendehenne D, Durner J, Klessig DF. Nitric oxide: a new player in plant signalling and defence responses. Current Opinion in Plant Biology (2004) 7:449–455.[CrossRef][Web of Science][Medline]
Willmott N, Sethi JK, Walseth TF, Lee H, White AM, Galione A. Nitric oxide-induced mobilization of intracellular calcium via the cyclic ADP-ribose signalling pathway. Journal of Biological Chemistry (1996) 271:3699–3705.
Yamamoto A, Katou S, Yoshioka H, Doke N, Kawakita K. Involvement of nitric oxide generation in hypersensitive cell death induced by elicitin in tobacco cell suspension culture. Journal of General Plant Pathology (2004) 70:85–92.[CrossRef]
Yamasaki H, Sakihama Y, Takahashi S. An alternative pathway for nitric oxide production in plants: new features of an old enzyme. Trends in Plant Science (1999) 4:128–129.[CrossRef][Web of Science][Medline]
Yao X, Huang Y. From nitric oxide to endothelial cytosolic Ca2+: a negative feedback control. Trends in Pharmacological Sciences (2003) 24:262–266.
Yoshida R, Hobo T, Ichimura K, Mizoguchi T, Takahashi F, Aronso J, Ecker JR, Shinozaki K. ABA-activated SnRK2 protein kinase is required for dehydratation stress signaling in Arabidopsis. Plant Cell Physiology (2002) 43:1473–1483.
Zago E, Morsa S, Dat JF, Alard P, Ferrarini A, Inzé D, Delledonne M, Van Breusegem F. Nitric oxide- and hydrogen peroxide-responsive gene regulation during cell death induction in tobacco. Plant Physiology (2006) 141:404–411.
Zemojtel T, Frohlich A, Palmieri MC, et al. Plant nitric oxide synthase: a never-ending story? Trends in Plant Science (2006) 11:524–525.[CrossRef][Web of Science][Medline]
Zottini M, Costa A, De Michele R, Ruzzenz M, Carimi F, Lo Schiavo F. Salicylic acid activates nitric oxide synthesis in Arabidopsis. Journal of Experimental Botany (2007) 58:1397–1405.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  H. Zhang, Q. Fang, Z. Zhang, Y. Wang, and X. Zheng The role of respiratory burst oxidase homologues in elicitor-induced stomatal closure and hypersensitive response in Nicotiana benthamiana J. Exp. Bot., July 1, 2009; 60(11): 3109 - 3122. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Besson-Bard, A. Gravot, P. Richaud, P. Auroy, C. Duc, F. Gaymard, L. Taconnat, J.-P. Renou, A. Pugin, and D. Wendehenne Nitric Oxide Contributes to Cadmium Toxicity in Arabidopsis by Promoting Cadmium Accumulation in Roots and by Up-Regulating Genes Related to Iron Uptake Plant Physiology, March 1, 2009; 149(3): 1302 - 1315. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S.-J. Wu and J.-Y. Wu Extracellular ATP-induced NO production and its dependence on membrane Ca2+ flux in Salvia miltiorrhiza hairy roots J. Exp. Bot., October 1, 2008; 59(14): 4007 - 4016. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. Ma, A. Smigel, Y.-C. Tsai, J. Braam, and G. A. Berkowitz Innate Immunity Signaling: Cytosolic Ca2+ Elevation Is Linked to Downstream Nitric Oxide Generation through the Action of Calmodulin or a Calmodulin-Like Protein Plant Physiology, October 1, 2008; 148(2): 818 - 828. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||