Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

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.

References

  1. Doke, N. Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiol. Plant Pathol. 23, 345–357 (1983).

    Article  CAS  Google Scholar 

  2. Bestwick, C.S., Brown, I.R., Bennett, M.H.R. & Mansfield, J.W. Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv. phaseolicola. Plant Cell 9, 209–221 (1997).

    Article  CAS  PubMed  Google Scholar 

  3. Apel, K. & Hirt, H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373–399 (2004).

    Article  CAS  PubMed  Google Scholar 

  4. Torres, M.A., Dangl, J.L. & Jones, J.D.G. Arabidopsis gp91-phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl. Acad. Sci. USA 99, 523–528 (2002).

    Article  Google Scholar 

  5. Cross, A.R. & Segal, A.W. The NADPH oxidase of professional phagocytes–prototype of the NOX electron transport chain systems. Biochim. Biophys. Acta 1657, 1–22 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Durrant, W.E. & Dong, X. Systemic acquired resistance. Annu. Rev. Phytopathol. 42, 185–209 (2004).

    Article  CAS  PubMed  Google Scholar 

  7. Torres, M.A. & Dangl, J.L. Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr. Opin. Plant Biol. 8, 397–403 (2005).

    Article  CAS  PubMed  Google Scholar 

  8. Levine, A., Tenhaken, R., Dixon, R. & Lamb, C.J. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79, 583–593 (1994).

    Article  CAS  PubMed  Google Scholar 

  9. Kwak, J.M. et al. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J. 22, 2623–2633 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Foreman, J. et al. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422, 442–446 (2003).

    Article  CAS  PubMed  Google Scholar 

  11. Dietrich, R.A., Richberg, M.H., Schmidt, R., Dean, C. & Dangl, J.L. A novel zinc-finger protein is encoded by the Arabidopsis lsd1 gene and functions as a negative regulator of plant cell death. Cell 88, 685–694 (1997).

    Article  CAS  PubMed  Google Scholar 

  12. Jabs, T., Dietrich, R.A. & Dangl, J.L. Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273, 1853–1856 (1996).

    Article  CAS  PubMed  Google Scholar 

  13. Rustérucci, C., Aviv, D.H., Holt, B.F. III, Dangl, J.L. & Parker, J.E. The disease resistance signaling components EDS1 and PAD4 are essential regulators of the cell death pathway controlled by LSD1 in Arabidopsis. Plant Cell 13, 2211–2224 (2001).

    Article  PubMed  PubMed Central  Google Scholar 

  14. Aviv, D.H. et al. Runaway cell death, but not basal disease resistance, in lsd1 is SA- and NIM1/NPR1-dependent. Plant J. 29, 381–391 (2002).

    Article  CAS  PubMed  Google Scholar 

  15. Joo, J.H., Wang, S., Chen, J.G., Jones, A.M. & Fedoroff, N.V. Different signaling and cell death roles of heterotrimeric G protein {alpha} and {beta} subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell 17, 957–970 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Govrin, E. & Levine, A. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr. Biol. 10, 751–757 (2000).

    Article  CAS  PubMed  Google Scholar 

  17. Enyedi, A.J., Yalpani, N., Silverman, P. & Raskin, I. Localization, conjugation and function of salicylic acid in tobacco during the hypersensitive reaction to tobacco mosaic virus. Proc. Natl. Acad. Sci. USA 89, 2480–2484 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Dorey, S. et al. Spatial and temporal induction of cell death, defense genes, and accumulation of salicylic acid in tobacco leaves reacting hypersensitively to a fungal glycoprotein elicitor. Mol. Plant Microbe Interact. 10, 646–655 (1997).

    Article  CAS  Google Scholar 

  19. Shirasu, K., Nakajima, H., Rajasekhar, V.K., Dixon, R.A. & Lamb, C.J. Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell 9, 261–270 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Draper, J. Salicylate, superoxide synthesis and cell suicide in plant defense. Trends Plant Sci. 2, 162–165 (1997).

    Article  Google Scholar 

  21. Wildermuth, M.C., Dewdney, J., Wu, G. & Ausubel, F.M. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414, 562–565 (2001).

    Article  CAS  PubMed  Google Scholar 

  22. Reeves, E.P. et al. Killing activity of neutrophils is mediated through activation of proteases by K+ flux. Nature 416, 291–297 (2002).

    Article  CAS  PubMed  Google Scholar 

  23. 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, 13454–13459 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Wendehenne, D., Durner, J. & Klessig, D.F. Nitric oxide: a new player in plant signalling and defence responses. Curr. Opin. Plant Biol. 7, 449–455 (2004).

    Article  CAS  PubMed  Google Scholar 

  25. Auh, C.-K. & Murphy, T.M. Plama membrane redox enzyme is involved in the synthesis of O2- and H2O2 by Phytophthora elicitor-stimulated rose cells. Plant Physiol. 107, 1241–1247 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Guo, F.Q., Okamoto, M. & Crawford, N.M. Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302, 100–103 (2003).

    Article  CAS  PubMed  Google Scholar 

  27. Allan, A.C. & Fluhr, R. Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells. Plant Cell 9, 1559–1572 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Levine, A., Pennell, R., Palmer, R. & Lamb, C.J. Calcium-mediated apoptosis in a plant hypersensitive response. Curr. Biol. 6, 427–437 (1996).

    Article  CAS  PubMed  Google Scholar 

  29. Davletova, S. et al. Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17, 268–281 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Kliebenstein, D.J., Dietrich, R.A., Martin, A.C., Last, R.L. & Dangl, J.L. LSD1 regulates salicylic acid induction of copper-zinc superoxide dismutase in Arabidopsis thaliana. Mol. Plant Microbe Interact. 12, 1022–1026 (1999).

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

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

Authors
  1. Miguel Angel Torres
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jonathan D G Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jeffery L Dangl
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jeffery L Dangl.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ng1639

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing