Abstract
Recognition of an avirulent pathogen triggers the rapid production of the reactive oxygen intermediates superoxide (O2−) and hydrogen peroxide (H2O2)1. This oxidative burst drives cross-linking of the cell wall2, induces several plant genes involved in cellular protection and defence3,4, and is necessary for the initiation of host cell death in the hypersensitive disease-resistance response1,3. However, this burst is not enough to support a strong disease-resistance response4,5. Here we show that nitric oxide, which acts as a signal in the immune, nervous and vascular systems6, potentiates the induction of hypersensitive cell death in soybean cells by reactive oxygen intermediates and functions independently of such intermediates to induce genes for the synthesis of protective natural products. Moreover, inhibitors of nitric oxide synthesis compromise the hypersensitive disease-resistance response of Arabidopsis leaves to Pseudomonas syringae, promoting disease and bacterial growth. We conclude that nitric oxide plays a key role in disease resistance in plants.
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References
Lamb, C. & Dixon, R. A. The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant. Mol. Biol. 48, 251–275 (1997).
Bradley, D. J., Kjellbom, P. & Lamb, C. J. Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: A novel, rapid defense response. Cell 70, 21–30 (1992).
Levine, A., Tenhaken, R., Dixon, R. A. & Lamb, C. H2O2from the oxidative burst orchestrates the plant hypersensitive response. Cell 79, 583–593 (1994).
Jabs, T., Tschöpe, M., Colling, C., Hahlbrock, K. & Scheel, D. Elicitor-stimulated ion fluxes and O2− from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. Proc. Natl Acad. Sci. USA 94, 4800–4805 (1997).
Glazener, J. A., Orlandi, E. W. & Baker, J. C. The active oxygen response of cell suspensions is not sufficient to cause hypersensitive cell death. Plant Physiol. 110, 759–763 (1996).
Schmidt, H. H. H. W. & Walter, U. NO at work. Cell 78, 919–925 (1994).
Shirasu, K., Nakajima, H., Rajasekhar, V. K., Dixon, R. A. & Lamb, C. Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell 9, 261–270 (1997).
Nathan, C. Natural resistance and nitric oxide. Cell 82, 873–876 (1995).
Chandra, S., Martin, G. B. & Low, P. S. The Pto kinase mediates a signaling pathway leading to the oxidative burst in tomato. Proc. Natl Acad. Sci. USA 93, 13393–13397 (1996).
Guo, Z.-J. & Ohta, Y. Effect of ethylene biosynthesis on the accumulation of 6-methoxymellein induced by elicitors in carrot cells. J. Plant Physiol. 144, 700–704 (1994).
Yahraus, T., Chandra, S., Legendre, L. & Low, P. S. Evidence for a mechanically induced oxidative burst. Plant Physiol. 109, 1259–1266 (1995).
Murphy, M. E. & Noack, E. Nitric oxide assay using hemoglobin method. Meth. Enzymol. 233, 241–250 (1994).
Cueto, M. et al. Presence of nitric oxide synthase activity in roots and nodules of Lupinus albus. FEBS Lett 398, 159–164 (1996).
Ninnemann, H. & Maier, J. Indications for the occurrence of nitric oxide synthases in fungi and plants and the involvement in photoconidiation of Neurospora crassa. Photochem. Photobiol. 64, 393–398 (1996).
Griffith, O. W. & Stuehr, D. J. Nitric oxide synthases: Properties and catalytic mechanism. Annu. Rev. Physiol. 57, 707–736 (1995).
Garvey, E. P. et al. Potent and selective inhibition of human nitric oxide synthases. J. Biol. Chem. 269, 26669–26676 (1994).
Dixon, R. A. & Paiva, N. Stress-induced phenylpropanoid metabolism. Plant Cell 7, 1085–1097 (1995).
Debener, T., Lehnackers, H., Arnold, M. & Dangl, J. L. Identification and molecular mapping of a single Arabidopsis thaliana locus determining resistance to a phytopathogenic Pseudomonas syringae isolate. Plant J. 1, 289–302 (1991).
Bowler, C., Neuhaus, G., Yamagata, H. & Chua, N.-H. Cyclic GMP and calcium mediate phytochrome phototransduction. Cell 77, 73–81 (1994).
Noritake, T., Kawakita, K. & Doke, N. Nitric oxide induces phytoalexin accumulation in potato tuber tissues. Plant Cell Physiol. 37, 113–116 (1996).
Levine, A., Pennell, R. I., Alvarez, M. E., Palmer, R. & Lamb, C. Calcium-stimulated apoptosis in a plant hypersensitive disease resistance response. Curr. Biol. 6, 427–437 (1996).
Berridge, M. J. Atale of two messengers. Nature 365, 388–389 (1993).
Groom, Q. J. et al. rbohA, a rice homologue of the mammalian gp91phox respiratory burst oxidase gene. Plant J. 10, 515–522 (1996).
Keller, T. et al. Aplant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca2+-binding domains. Plant Cell 10, 255–266 (1998).
Jaffrey, S. R. & Snyder, S. H. PIN: an associated protein inhibitor of neuronal nitric oxide synthase. Science 274, 774–777 (1996).
Keen, N. T. & Buzzell, R. I. New disease resistance genes in soybean against Pseudomonas syringae pv. glycinea: Evidence that one of them interacts with a bacterial elicitor. Theor. Appl. Genet. 81, 133–138 (1991).
Cameron, R. K., Dixon, R. A. & Lamb, C. J. Biologically induced systemic acquired resistance in Arabidopsis thaliana. Plant J. 5, 715–725 (1994).
Hevel, J. M. & Marletta, M. A. Nitric oxide synthase assays. Meth. Enzymol. 23, 251–258 (1994).
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(in the press).
Acknowledgements
Y.X. is a Noble/Salk postdoctoral fellow. This research was supported by grants to M.D. and C.L. from the Italian National Research Council and the Noble Foundation, respectively.
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Delledonne, M., Xia, Y., Dixon, R. et al. Nitric oxide functions as a signal in plant disease resistance. Nature 394, 585–588 (1998). https://doi.org/10.1038/29087
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DOI: https://doi.org/10.1038/29087
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