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S-nitrosylation of NADPH oxidase regulates cell death in plant immunity

Byung-Wook Yun, Angela Feechan, Minghui Yin, Noor B. B. Saidi, Thierry Le Bihan, Manda Yu, John W. Moore, Jeong-Gu Kang, Eunjung Kwon, Steven H. Spoel, Jacqueline A. Pallas and Gary J. Loake ()
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Byung-Wook Yun: Institute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, King’s Buildings, Edinburgh EH9 3JH, UK
Angela Feechan: Institute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, King’s Buildings, Edinburgh EH9 3JH, UK
Minghui Yin: Institute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, King’s Buildings, Edinburgh EH9 3JH, UK
Noor B. B. Saidi: Institute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, King’s Buildings, Edinburgh EH9 3JH, UK
Thierry Le Bihan: University of Edinburgh, Centre for Systems Biology, Edinburgh EH9 3JR, UK
Manda Yu: Institute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, King’s Buildings, Edinburgh EH9 3JH, UK
John W. Moore: Institute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, King’s Buildings, Edinburgh EH9 3JH, UK
Jeong-Gu Kang: Institute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, King’s Buildings, Edinburgh EH9 3JH, UK
Eunjung Kwon: Institute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, King’s Buildings, Edinburgh EH9 3JH, UK
Steven H. Spoel: Institute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, King’s Buildings, Edinburgh EH9 3JH, UK
Jacqueline A. Pallas: Trait Research, Syngenta, Jealott’s Hill, Bracknell, Berkshire RG42 6EY, UK
Gary J. Loake: Institute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, King’s Buildings, Edinburgh EH9 3JH, UK

Nature, 2011, vol. 478, issue 7368, 264-268

Abstract: Abstract Changes in redox status are a conspicuous feature of immune responses in a variety of eukaryotes1,2, but the associated signalling mechanisms are not well understood. In plants, attempted microbial infection triggers the rapid synthesis of nitric oxide3,4 and a parallel accumulation of reactive oxygen intermediates, the latter generated by NADPH oxidases related to those responsible for the pathogen-activated respiratory burst in phagocytes5. Both nitric oxide and reactive oxygen intermediates have been implicated in controlling the hypersensitive response, a programmed execution of plant cells at sites of attempted infection3,5,6. However, the molecular mechanisms that underpin their function and coordinate their synthesis are unknown. Here we show genetic evidence that increases in cysteine thiols modified using nitric oxide, termed S-nitrosothiols, facilitate the hypersensitive response in the absence of the cell death agonist salicylic acid and the synthesis of reactive oxygen intermediates. Surprisingly, when concentrations of S-nitrosothiols were high, nitric oxide function also governed a negative feedback loop limiting the hypersensitive response, mediated by S-nitrosylation of the NADPH oxidase, AtRBOHD, at Cys 890, abolishing its ability to synthesize reactive oxygen intermediates. Accordingly, mutation of Cys 890 compromised S-nitrosothiol-mediated control of AtRBOHD activity, perturbing the magnitude of cell death development. This cysteine is evolutionarily conserved and specifically S-nitrosylated in both human and fly NADPH oxidase, suggesting that this mechanism may govern immune responses in both plants and animals.

Date: 2011
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DOI: 10.1038/nature10427

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