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Pathogen-induced, NADPH oxidase–derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana

Nature Genetics volume 37, pages 1130–1134 (2005)Cite this article

Abstract

Plant immune responses are usually accompanied by the production of extracellular superoxide at and surrounding infection sites1,2,3. Extracellular reactive oxygen intermediates (ROIs) in plants were proposed to drive programmed cell death correlated with disease resistance (the hypersensitive response). ROIs derived from this oxidative burst are generated by plasma membrane NADPH oxidases, anchored by gp91phox proteins related to those responsible for the respiratory oxidative burst activated in mammalian neutrophils during infection4,5. Mutation of Arabidopsis thaliana respiratory burst oxidase (Atrboh) genes eliminated pathogen-induced ROI production but had only a modest effect on the hypersensitive response4. We show that Atrboh function can be activated by exogenous ROIs. Unexpectedly, the subsequent oxidative burst can suppress cell death in cells surrounding sites of NADPH oxidase activation. This cell death requires salicylic acid, a plant immune system activator6. Thus, ROIs generated by Atrboh proteins can antagonize salicylic acid–dependent pro-death signals. These results have implications for understanding how salicylic acid activates defense signaling in cells spatially removed from infection sites without causing cell death.

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Figure 1: Plant NADPH oxidase gp91phox can negatively regulate cell death.
Figure 2: The AtrbohD-dependent oxidative burst is activated by exogenous ROIs and negatively regulates superoxide-induced RCD in lsd1.
Figure 3: ROIs produced by AtrbohD limits the spread of the cell death induced by pathogens.
Figure 4: LSD1 and AtrbohD antagonize a salicylic acid–dependent pro-death pathway.

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Acknowledgements

We thank K. Overmyer and J. McDowell for comments on the manuscript. This work was supported by grants from the US National Science Foundation and the US National Institutes of Health to J.L.D. The Sainsbury Laboratory is supported by the Gatsby Charitable Trust.

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Authors and Affiliations

  1. Department of Biology, University of North Carolina, CB# 3280, Coker Hall, Room 108, Chapel Hill, 27599-3280, North Carolina, USA

    Miguel Angel Torres & Jeffery L Dangl

  2. Sainsbury Laboratory, John Innes Center, Colney, Norwich, NR4 7UH, UK

    Jonathan D G Jones

  3. Department of Microbiology and Immunology and Carolina Center for Genome Sciences, Curriculum in Genetics, University of North Carolina, CB# 3280, Coker Hall, Room 108, Chapel Hill, 27599-3280, North Carolina, USA

    Jeffery L Dangl

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Correspondence to Jeffery L Dangl.

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Torres, M., Jones, J. & Dangl, J. Pathogen-induced, NADPH oxidase–derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat Genet 37, 1130–1134 (2005). https://doi.org/10.1038/ng1639

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