Nitric oxide: A new player in plant signalling and defence responses

Current Opinion in Plant Biology

Volumn 7, Issue 4, 2004, Pages 449-455

  Wendehenne, David ^a   Durner, Jörg ^b   Klessig, Daniel F ^c  

^a UNIVERSITÉ DE BOURGOGNE   (France)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c Boyce Thompson Institute for Plant Research   (United States)

Author keywords

ABA; abscisic acid; cADPR; cyclic ADP ribose; GC; GDC; glycine decarboxylase complex; guanylate cyclase; HR; hypersensitive response; iNOS; JA; jasmonic acid; nitrate reductase; nitric oxide; nitric oxide synthase(s); NO; NOS; NR; PAL; pathogen inducible NOS

Indexed keywords

NITRIC OXIDE;

BIOLOGICAL MODEL; CELL DEATH; DRUG EFFECT; METABOLISM; PLANT; REVIEW; SIGNAL TRANSDUCTION;

CELL DEATH; MODELS, BIOLOGICAL; NITRIC OXIDE; PLANTS; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 3042806779     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2004.04.002     Document Type: Review

References (41)

1. Stamler J.S., Lamas S., Fang F.C. Nitrosylation: the prototypic redox-based signaling mechanism. Cell. 106:2001;675-683
2. Mayer B., Hemmens B. Biosynthesis and action of nitric oxide in mammalian cells. Trends Biochem Sci. 22:1997;477-481
3. Delledonne M., Xia Y., Dixon R.A., Lamb C. Nitric oxide functions as a signal in plant disease resistance. Nature. 394:1998;585-588
4. Durner J., Wendehenne D., Klessig D.F. Defense gene induction in tobacco by nitric oxide, cyclic GMP and cyclic ADP-ribose. Proc Natl Acad Sci USA. 95:1998;10328-10333
5. 2+-calmodulin/NADPH-dependent NOS activity and shows similarities to a group of bacterial proteins that contain putative GTP-binding or GTPase domains.
6. Pagnussat G.C., Lanteri M.L., Lamattina L. Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiol. 132:2003;1241-1248
7. Neill S., Desikan R., Clarke A., Hancock J.T. Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiol. 128:2002;13-16 The authors of this paper and of [22] make the important discovery that NO is a prerequisite for the ABA signal transduction pathway in guard cells. Neill, et al. report that ABA induces significant NO production that can be visualised in guard cells using a NO-sensitive fluorophore. NO scavengers suppress ABA-induced stomatal closure whereas stomatal closure is promoted by NO donors in the absence of the hormone, arguing that NO is a mediator of ABA signalling. Pharmacological analyses support a role for cGMP and cADPR in mediating NO effects that lead to stomatal closure.
8. Wendehenne D., Pugin A., Klessig D., Durner J. Nitric oxide: comparative synthesis and signaling in animal and plant cells. Trends Plant Sci. 6:2001;177-183
9. Butt Y.K-C., Lum J.H-K., Lo S.C-L. Proteomic identification of plant proteins probed by mammalian nitric oxide synthase antibodies. Planta. 216:2003;762-771
10. ••] define new classes of NOS.
11. Lamotte O, Gould K, Lecourieux D, Sequeira-Legrand A, Lebun-Garcia A, Durner J, Pugin A, Wendehenne D: Analysis of nitric oxide signaling functions in tobacco cells challenged by the elicitor cryptogein. Plant Physiol 2004, in press.
12. Chandok M, Ekengren S, Martin GB, Klessig DF: Suppression of pathogen-inducible nitric oxide synthase (iNOS) activity in tomato increases susceptibility to Pseudomonas syringae. Proc Natl Acad Sci USA, in press.
13. Yamasaki H. Nitrite-dependent nitric oxide production pathway: implications for involvement of active nitrogen species in photoinhibition in vivo. Philos Trans R Soc Lond B Biol Sci. 355:2000;1477-1488
14. Rockel P., Strube F., Rockel A., Wildt J., Kaiser W.M. Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J Exp Bot. 53:2002;103-110
15. 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. Proc Natl Acad Sci USA. 99:2002;16314-16318 The authors make an outstanding contribution to the field by providing genetic, pharmacological and physiological evidence of the role of NR as a source of NO in ABA signalling in A. thaliana guard cells. The generation of NO after the treatment of guard cells with either ABA or nitrite, a substrate for NR, correlated with stomatal closure. Both ABA and nitrite failed to induce stomatal closure in epidermal peels of the NR double mutant nia1 nia2, arguing that NR is required to generate NO that subsequently mediates ABA-induced stomatal closure.
16. Yamamoto A., Katou S., Yoshioka H., Doke N., Kawakita H. Nitrate reductase, a nitric oxide-producing enzyme: induction by pathogen signals. J Gen Plant Pathol. 69:2003;218-229
17. del Rio L.A., Corpas F.J., Sandalio L.M., Palma J.M., Barroso J.B. Plant peroxisomes, reactive oxygen metabolism and nitric oxide. IUBMB Life. 55:2003;71-81
18. Bethke P.C., Badger M.R., Jones R.L. Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell. 16:2004;332-341 This work provides the first evidence that NO is produced non-enzymatically in the apoplast. The authors show that NO is rapidly synthesised by the chemical reduction of nitrite in the apoplast of barley aleurone layers. Nitrite-dependent, non-enzymatic NO synthesis required an acidic pH and was observed to occur in response to gibberellin and ABA, two hormones that rapidly acidified the apoplastic medium. Furthermore, the chemical production of NO was accelerated by reducing agents, including phenolic compounds.
19. Klessig D., Durner J., Noad R., Navarre D.A., Wendehenne D., Kumar D., Zhou J.M., Shah J., Zhang S., Kachroo P., et al. Nitric oxide and salicylic acid signaling in plant defense. Proc Natl Acad Sci USA. 97:2000;8849-8855
20. - channels at the plasma membrane, two key events in ABA-induced stomatal closure.
21. Gould K., Lamotte O., Klinguer A., Pugin A., Wendehenne D. Nitric oxide production in tobacco leaf cells: a generalised stress response? Plant Cell Environ. 26:2003;1851-1862
22. Garcia-Mata C., Lamattina L. Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol. 126:2001;1196-1204
23. Huang X., Stettmaier K., Michel C., Hutzler P., Mueller M.J., Durner J. Nitric oxide is induced by wounding and influences jasmonic acid signaling in Arabidopsis thaliana. Planta. 218:2004;938-946
24. Song F., Goodman R.M. Activity of nitric oxide is dependent on, but is partially required for function of, salicylic acid in the signaling pathway in tobacco systemic acquired resistance. Mol Plant Microbe Interact. 12:2001;1458-1462
25. Orozco-Cardenas M.L., Ryan C.A. Nitric oxide negatively modulates wound signaling in tomato plants. Plant Physiol. 130:2002;487-493
26. Jih P-J., Chen Y-C., Jen S-T. Involvement of hydrogen peroxide and nitric oxide in expression of the ipomoelin gene from sweet potato. Plant Physiol. 132:2003;381-389
27. Saviani E.E., Orsi C.H., Oliveira J.F.P., Pinto-Maglio C.A.F., Salgado I. Participation of the mitochondrial permeability transition pore in nitric oxide-induced plant cell death. FEBS Lett. 510:2002;136-140
28. Seregélyes C., Barna B., Hennig J., Konopka D., Pasternak T.P., Lukacs N., Fehér A., Horvath G.V., Dudits D. Phytoglobins can interfere with nitric oxide functions during plant growth and pathogenic responses: a transgenic approach. Plant Sci. 165:2003;541-550
29. Dordas C., Hasinoff B.B., Igamberdiev A.U., Manac'h N., Rivoal J., Hill R.D. Expression of a stress-induced haemoglobin affects NO levels produced by alfalfa root cultures under hypoxic stress. Plant J. 35:2003;763-770
30. Delledonne M., Zeier J., Marocco A., Lamb C. Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci USA. 98:2001;13454-13459
31. de Pinto M., Tommasi F., De Gara L. Changes in the antioxidant systems as part of the signaling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in tobacco bright-yellow 2 cells. Plant Physiol. 130:2002;698-708
32. Zhang C., Czymmek K.J., Shapiro A.D. Nitric oxide does not trigger early programmed cell death events but may contribute to cell-to-cell signaling governing progression of the Arabidopsis hypersensitive response. Mol Plant Microbe Interact. 16:2003;962-972
33. Beligni M.V., Fath A., Bethke P.C., Lamattina L., Jones R.L. Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers. Plant Physiol. 129:2002;1642-1650
34. •], this paper describes a highlight of recent work on NO signalling in plants. The authors studied the transcriptional changes mediated by artificially generated NO in A. thaliana suspension cells by using a cDNA microarray that included about 200 defence-related genes and 50 genes that are associated with primary metabolism. About 5% of the transcripts showed transient changes in expression. Amongst the NO-sensitive genes, NO strongly induces a gene that encodes alternative oxidase, a protein that might act to counteract NO-induced inhibition of cytochrome c-dependent respiration.
35. Polverari A., Molesini B., Pezzotti M., Buonaurio R., Marte M., Delledonne M. Nitric oxide-mediated transcriptional changes in Arabidopsis thaliana. Mol Plant Microbe Interact. 16:2003;1094-1105 cDNA-amplification fragment length polymorphism (AFLP) analysis identified transcripts whose expression was rapidly altered following infiltration of A. thaliana leaves with a NO donor. Of approximately 2500 cDNAs analysed, 120 differentially regulated cDNAs were detected. In addition to the expected activation of genes that are related to defence responses and oxidative stress, a large number of genes that are associated with metabolism and signalling were also expressed in response to NO treatment.
36. Navarre D.A., Wendehenne D., Durner J., Noad R., Klessig D.F. Nitric oxide modulates the activity of tobacco aconitase. Plant Physiol. 122:2000;573-582
37. Ignarro L.J., Buga G.M., Wood K.S., Byrns R.E., Chaudhuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci USA. 84:1987;9265-9269
38. Palmer R.M.J., Ferrige A.G., Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature. 327:1987;524-526
39. Stöhr C., Strube F., Marx G., Ullrich W.R., Rockel P. A plasma membrane-bound enzyme of tobacco roots catalyses the formation of nitric oxide from nitrite. Planta. 212:2001;835-841
40. Belenghi B., Acconcia F., Trovato M., Perazzolli M., Bocedi A., Polticelli F., Ascenzi P., Delledonne M. AtCYS1, a cystatin from Arabidopsis thaliana, suppresses hypersensitive cell death. Eur J Biochem. 270:2003;2593-2604
41. Murgia I., Delledonne M., Soave C. Nitric oxide mediates iron-induced ferritin accumulation in Arabidopsis. Plant J. 30:2002;521-528