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.

Expanded type III effector recognition by the ZAR1 NLR protein using ZED1-related kinases

Nature Plants volume 3, Article number: 17027 (2017) Cite this article

Subjects

Abstract

Nucleotide-binding domain and leucine-rich repeat domain-containing (NLR) proteins are sentinels of plant immunity that monitor host proteins for perturbations induced by pathogenic effector proteins. Here we show that the Arabidopsis ZAR1 NLR protein requires the ZRK3 kinase to recognize the Pseudomonas syringae type III effector (T3E) HopF2a. These results support the hypothesis that ZAR1 associates with an expanded ZRK protein family to broaden its effector recognition spectrum.

Gram-negative bacterial phytopathogens can suppress plant immunity using the type III secretion system (T3SS), a needle-like structure capable of injecting type III secreted effector proteins (T3Es) directly into plant cells1. In response, NLR proteins have evolved to recognize T3Es and induce a resistance response referred to as effector-triggered immunity (ETI), which is typically associated with a programmed cell death response called the hypersensitive response (HR)2. Pathogen recognition by plant NLR proteins has been compared to a trap whereby the prey (T3E) modifies a bait (sensor) thereby activating the trap (NLR) and promoting ETI3–5. For example, the P. syringae T3E HopZ1a is an acetyltransferase that activates an ETI response in Arabidopsis that is dependent on the NLR ZAR1 and the ZED1 pseudokinase6–9. It is hypothesized that acetylation of ZED1 by HopZ1a activates ZAR18. ZAR1 also recognizes the Xanthomonas campestris T3E AvrAC, requiring the ZED1-related kinase ZRK1 (aka RKS1) instead of ZED110. Here we demonstrate that ZAR1 recognizes the T3E HopF2a and activates ETI in a ZRK3-dependent manner. Since ZRK3 lies in the same genomic cluster as ZED1 and ZRK1, expansion of this T3E sensor family has likely contributed to the broadened T3E recognition range of ZAR18.

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: HopF2a induces ETI in Arabidopsis.
Figure 2: HopF2a recognition requires ZAR1 and ZRK3.

References

  1. Büttner, D. & He, S. Y. Plant Physiol. 150, 1656–1664 (2009).

    Google Scholar 

  2. Jones, J. D. & Dangl, J. L. Nature 444, 323–329 (2006).

    Google Scholar 

  3. Collier, S. M. & Moffett, P. Trends Plant Sci. 14, 521–529 (2009).

    Google Scholar 

  4. Ntoukakis, V. et al. PLoS Pathog. 9, e1003123 (2013).

    Google Scholar 

  5. Kim, S. H., Qi, D., Ashfield, T., Helm, M. & Innes, R. W. Science 351, 684–687 (2016).

    Google Scholar 

  6. Lewis, J. D., Wu, R., Guttman, D. S. & Desveaux, D. PLoS Genet. 6, e1000894 (2010).

    Google Scholar 

  7. Lee, A. H.-Y. et al. PLoS Pathog. 8, e1002523 (2012).

    Google Scholar 

  8. Lewis, J. D. et al. Proc. Natl Acad. Sci. USA 110, 18722–18727 (2013).

    Google Scholar 

  9. Khan, M., Subramaniam, R. & Desveaux, D. Curr. Opin. Microbiol. 29, 49–55 (2016).

    Google Scholar 

  10. Wang, G. et al. Cell Host Microbe 18, 285–295 (2015).

    Google Scholar 

  11. Lo, T., Koulena, N., Seto, D., Guttman, D. S. & Desveaux, D. Mol. Plant Pathol. (2016).

  12. Singer, A. U. et al. Structure 12, 1669–1681 (2004).

    Google Scholar 

  13. Wang, Y. et al. Plant Cell 22, 2033–2044 (2010).

    Google Scholar 

  14. Hinsch, M. & Staskawicz, B. Mol. Plant Microbe Interact. 9, 55–61 (1996).

    Google Scholar 

  15. Gassmann, W. Mol. Plant Microbe Interact. 18, 1054–1060 (2005).

    Google Scholar 

  16. Menna, A., Nguyen, D., Guttman, D. S. & Desveaux, D. Front. Plant Sci. 6, 995 (2015).

    Google Scholar 

  17. Huard-Chauveau, C. et al. PLoS Genet. 9, e1003766 (2013).

    Google Scholar 

Download references

Acknowledgements

We thank members of the Desveaux and Guttman laboratories for valuable input on the project. This work was supported by Ontario Graduate Scholarships and the Natural Sciences and Engineering Research Council of Canada (NSERC) postgraduate awards (D.S. and T.L.), NSERC Discovery Grants (D.D. and D.S.G.), a Canada Research Chair in Plant-Microbe Systems Biology (D.D.) or Comparative Genomics (D.S.G.) and the Centre for the Analysis of Genome Evolution and Function (D.D. and D.S.G.). T-DNA lines were obtained from the ABRC.

Author information

Author notes

  1. Derek Seto and Noushin Koulena: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Cell & Systems Biology, University of Toronto, 25 Willcocks Street, Toronto, M5S 3B2, Ontario, Canada

    Derek Seto, Noushin Koulena, Timothy Lo, Alexandra Menna, David S. Guttman & Darrell Desveaux

  2. Centre for the Analysis of Genome Evolution & Function, University of Toronto, Toronto, M5S 3B2, Ontario, Canada

    David S. Guttman & Darrell Desveaux

Authors
  1. Derek Seto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Noushin Koulena
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Timothy Lo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alexandra Menna
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. David S. Guttman
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Darrell Desveaux
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

D.S., N.K., T.L., A.M. and D.D. designed experiments. D.S., N.K., T.L. and A.M. conducted experiments. D.S., N.K., T.L., A.M., D.S.G. and D.D. analysed data. D.S. and D.D. wrote the manuscript.

Corresponding author

Correspondence to Darrell Desveaux.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Methods, Supplementary References, Supplementary Figure Legends 1–4 and Supplementary Figures 1–4. (PDF 10830 kb)

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Seto, D., Koulena, N., Lo, T. et al. Expanded type III effector recognition by the ZAR1 NLR protein using ZED1-related kinases. Nature Plants 3, 17027 (2017). https://doi.org/10.1038/nplants.2017.27

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nplants.2017.27

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