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PNAS 102 (22): 8054-8059

Copyright © 2005 by the National Academy of Sciences.

BIOLOGICAL SCIENCES / PLANT BIOLOGY

A central role for S-nitrosothiols in plant disease resistance

Angela Feechan*, Eunjung Kwon*, Byung-Wook Yun*, Yiqin Wang*, Jacqueline A. Pallas{dagger},{ddagger}, and Gary J. Loake*,§

*Institute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, King's Buildings, Edinburgh EH9 3JR, United Kingdom; and {dagger}Trait Research, Syngenta, Jealott's Hill, Bracknell, Berkshire RG42 6EY, United Kingdom

Received for publication February 21, 2005.

Abstract: Animal S-nitrosoglutathione reductase (GSNOR) governs the extent of cellular S-nitrosylation, a key redox-based posttranslational modification. Mutations in AtGSNOR1, an Arabidopsis thaliana GSNOR, modulate the extent of cellular S-nitrosothiol (SNO) formation in this model plant species. Loss of AtGSNOR1 function increased SNO levels, disabling plant defense responses conferred by distinct resistance (R) gene subclasses. Furthermore, in the absence of AtGSNOR1, both basal and nonhost disease resistance are also compromised. Conversely, increased AtGSNOR1 activity reduced SNO formation, enhancing protection against ordinarily virulent microbial pathogens. Here we demonstrate that AtGSNOR1 positively regulates the signaling network controlled by the plant immune system activator, salicylic acid. This contrasts with the function of this enzyme in mice during endotoxic shock, where GSNOR antagonizes inflammatory responses. Our data imply SNO formation and turnover regulate multiple modes of plant disease resistance.

Key Words: S-nitrosylation • salicylic acid • nitric oxide

§ To whom correspondence should be addressed. E-mail: gloake{at}ed.ac.uk.

{ddagger} Present address: Bloomsbury Centre for Bioinformatics, University College London, Gower Street, London WC1E 6BT, United Kingdom.

Edited by Brian J. Staskawicz, University of California, Berkeley, CA, and approved April 18, 2005

Author contributions: G.J.L. designed research; A.F., E.K., B.-W.Y., and Y.W. performed research; A.F., E.K., B.-W.Y., Y.W., J.A.P., and G.J.L. analyzed data; and G.J.L. wrote the paper.

This paper was submitted directly (Track II) to the PNAS office.

Abbreviations: NHR, nonhost disease resistance; R, resistance gene; avr, avirulence; SNO, S-nitrosothiols; GSNO, S-nitrosoglutathione; GSNOR, GSNO reductase; AtGSNOR1, A. thaliana GSNOR; SA, salicylic acid; NOS, NO synthase; SAG, SA-β-glucoside; Pst, Pseudomonas syringae pv. Tomato; Bgt, Blumeria graminis f.sp. tritici; Psp, Pseudomonas syringae pv. phaseolicola.

© 2005 by The National Academy of Sciences of the USA

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