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.

  • Letter
  • Published:

Co-option of a default secretory pathway for plant immune responses

Nature volume 451, pages 835–840 (2008)Cite this article

Abstract

Cell-autonomous immunity is widespread in plant–fungus interactions and terminates fungal pathogenesis either at the cell surface or after pathogen entry. Although post-invasive resistance responses typically coincide with a self-contained cell death of plant cells undergoing attack by parasites, these cells survive pre-invasive defence. Mutational analysis in Arabidopsis identified PEN1 syntaxin as one component of two pre-invasive resistance pathways against ascomycete powdery mildew fungi1,2,3. Here we show that plasma-membrane-resident PEN1 promiscuously forms SDS-resistant soluble N-ethylmaleimide sensitive factor attachment protein receptor (SNARE) complexes together with the SNAP33 adaptor and a subset of vesicle-associated membrane proteins (VAMPs). PEN1-dependent disease resistance acts in vivo mainly through two functionally redundant VAMP72 subfamily members, VAMP721 and VAMP722. Unexpectedly, the same two VAMP proteins also operate redundantly in a default secretory pathway, suggesting dual functions in separate biological processes owing to evolutionary co-option of the default pathway for plant immunity. The disease resistance function of the secretory PEN1–SNAP33–VAMP721/722 complex and the pathogen-induced subcellular dynamics of its components are mechanistically reminiscent of immunological synapse formation in vertebrates, enabling execution of immune responses through focal secretion.

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

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

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

Figure 1: PEN1-3 fails to form SDS-resistant SNARE complexes with VAMP722.
Figure 2: VAMP721 and VAMP722 are required for PEN1-mediated immune responses.
Figure 3: Focal accumulation and directed movement of VAMP722-containing intracellular compartments to powdery-mildew entry sites.
Figure 4: Compromised pre- and post-invasion resistance by lowered gene dosage of VAMP721 and VAMP722.

Similar content being viewed by others

References

  1. Collins, N. C. et al. SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425, 973–977 (2003)

    Article  CAS  ADS  Google Scholar 

  2. Lipka, V. et al. Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis . Science 310, 1180–1183 (2005)

    Article  CAS  ADS  Google Scholar 

  3. Stein, M. et al. Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18, 731–746 (2006)

    Article  CAS  Google Scholar 

  4. Ungar, D. & Hughson, F. M. SNARE protein structure and function. Annu. Rev. Cell Dev. Biol. 19, 493–517 (2003)

    Article  CAS  Google Scholar 

  5. Spafford, J. D. & Zamponi, G. W. Functional interactions between presynaptic calcium channels and the neurotransmitter release machinery. Curr. Opin. Neurobiol. 13, 308–314 (2003)

    Article  CAS  Google Scholar 

  6. Zhang, Z. et al. A SNARE-protein has opposing functions in penetration resistance and defense signalling pathways. Plant J. 49, 302–312 (2007)

    Article  CAS  Google Scholar 

  7. Sutton, R. B., Fasshauer, D., Jahn, R. & Brunger, A. T. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 °A resolution. Nature 395, 347–353 (1998)

    Article  CAS  ADS  Google Scholar 

  8. Sanderfoot, A. A., Assaad, F. F. & Raikhel, N. V. The Arabidopsis genome. An abundance of soluble N-ethylmaleimide-sensitive factor adaptor protein receptors. Plant Physiol. 124, 1558–1569 (2000)

    Article  CAS  Google Scholar 

  9. Hayashi, T. et al. Synaptic vesicle membrane fusion complex: action of clostridial neurotoxins on assembly. EMBO J. 13, 5051–5061 (1994)

    Article  CAS  Google Scholar 

  10. Heese, M. et al. Functional characterization of the KNOLLE-interacting t-SNARE AtSNAP33 and its role in plant cytokinesis. J. Cell Biol. 155, 239–250 (2001)

    Article  CAS  Google Scholar 

  11. Mayer, A. Membrane fusion in eukaryotic cells. Annu. Rev. Cell Dev. Biol. 18, 289–314 (2002)

    Article  CAS  Google Scholar 

  12. Assaad, F. F. et al. The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. Mol. Biol. Cell 15, 5118–5129 (2004)

    Article  CAS  Google Scholar 

  13. Roslan, H. A. et al. Characterization of the ethanol-inducible alc gene-expression system in Arabidopsis thaliana . Plant J. 28, 225–235 (2001)

    Article  CAS  Google Scholar 

  14. Bhat, R. A., Miklis, M., Schmelzer, E., Schulze-Lefert, P. & Panstruga, R. Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain. Proc. Natl Acad. Sci. USA 102, 3135–3140 (2005)

    Article  CAS  ADS  Google Scholar 

  15. Pickett, J. A. & Edwardson, J. M. Compound exocytosis; mechanisms and functional significance. Traffic 7, 109–116 (2006)

    Article  CAS  Google Scholar 

  16. Nishimura, M. T. et al. Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301, 969–972 (2003)

    Article  CAS  ADS  Google Scholar 

  17. Jacobs, A. K. et al. An Arabidopsis callose synthase, GSL5, is required for wound and papillary callose formation. Plant Cell 15, 2503–2513 (2003)

    Article  CAS  Google Scholar 

  18. Kalde, M., Nühse, T. S., Findlay, K. & Peck, S. C. The syntaxin SYP132 contributes to plant resistance against bacteria and secretion of pathogenesis-related protein 1. Proc. Natl Acad. Sci. USA 104, 11850–11855 (2007)

    Article  CAS  ADS  Google Scholar 

  19. van Loon, L. C., Rep, M. & Pieterse, C. M. J. Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44, 135–162 (2006)

    Article  CAS  Google Scholar 

  20. Kobayashi, Y. et al. Dynamic reorganization of microfilaments and microtubules is necessary for the expression of non-host resistance in barley coleoptile cells. Plant J. 11, 525–537 (1997)

    Article  CAS  Google Scholar 

  21. Takemoto, D., Jones, D. A. & Hardham, A. R. GFP-tagging of cell components reveals the dynamics of subcellular re-organization in response to infection of Arabidopsis by oomycete pathogens. Plant J. 33, 775–792 (2003)

    Article  CAS  Google Scholar 

  22. Koh, S., Andre, A., Edwards, H., Ehrhardt, D. & Somerville, S. Arabidopsis thaliana subcellular responses to compatible Erysiphe cichoracearum infections. Plant J. 44, 516–529 (2005)

    Article  CAS  Google Scholar 

  23. Baluska, F., Volkmann, D. & Menzel, D. Plant synapses: actin-based domains for cell-to-cell commmunication. Trends Plant Sci. 10, 106–111 (2005)

    Article  CAS  Google Scholar 

  24. Kwon, C., Panstruga, R. & Schulze-Lefert, P. Les liaisons dangereuses: immunological synapse formation in animals and plants. Trends Immunol. (in the press)

  25. Lieberman, J. The ABCs of granule-mediated cytotoxicity: new weapons in the arsenal. Nature Rev. Immunol. 3, 361–370 (2003)

    Article  CAS  Google Scholar 

  26. Huse, M., Lillemeier, B. F., Kuhns, M. S., Chen, D. S. & Davis, M. M. T cells use two directionally distinct pathways for cytokine secretion. Nature Immunol. 7, 247–255 (2006)

    Article  CAS  Google Scholar 

  27. Shen, Q. H. et al. Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315, 1098–1103 (2007)

    Article  CAS  ADS  Google Scholar 

  28. Feys, B. J. et al. Arabidopsis senescence-associated gene101 stabilizes and signals within an enhanced disease susceptibility1 complex in plant innate immunity. Plant Cell 17, 2601–2613 (2005)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank E. Schmelzer, J. Bautor, A. Reinstädler and H. Häweker for technical assistance, H. Thordal-Christensen for PEN1 antiserum, and Riyaz Bhat for initial FRET–FLIM measurements. This work was supported by funds from the Max Planck Society, the Deutsche Forschungsgemeinschaft (SFB670 and SPP1212) and the Bundesminsterium für Bildung und Forschung (GABI Nonhost Resistance Consortium). C.K. was supported by a post-doctoral fellowship from the Korean Research Foundation (KRF) and M.H. by the Alexander von Humboldt Foundation.

Author Contributions C.K., R.P., V.L. and P.S.-L. designed all experiments. C.K., C.N., S.P., H.S.Y., U.L., M.H. S.B., M.S., M.K., H.R. and F.E.K. performed the experiments. C.K., V.L., G.J., R.P. and P.S.-L. analysed the data. C.K. and P.S.-L. wrote the paper.

Author information

Author notes

  1. Christina Neu, Ulrike Lipka & Volker Lipka

    Present address: Present addresses: Sainsbury Laboratory, John Innes Centre, Norwich, Norfolk NR4 7UH, UK (U.L. and V.L.); Institut für Biologie II, Universität Freiburg, Sonnenstrasse 5, D-79104 Freiburg, Germany (C.N.).,

Authors and Affiliations

  1. Department of Plant Microbe Interactions, Max-Planck-Institut für Züchtungsforschung, Carl-von-Linné-Weg 10, D-50829 Köln, Germany,

    Chian Kwon, Christina Neu, Simone Pajonk, Hye Sup Yun, Ulrike Lipka, Matt Humphry, Stefan Bau, Marco Straus, Mark Kwaaitaal, Jane Parker, Ralph Panstruga, Volker Lipka & Paul Schulze-Lefert

  2. ZMBP, Plant Biochemistry, Eberhard-Karls-Universität Tübingen, Auf der Morgenstelle 5, D-72076 Tübingen, Germany ,

    Ulrike Lipka, Heike Rampelt & Volker Lipka

  3. ZMBP, Developmental Genetics, Eberhard-Karls-Universität Tübingen, Auf der Morgenstelle 3, D-72076 Tübingen, Germany ,

    Farid El Kasmi & Gerd Jürgens

Authors
  1. Chian Kwon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christina Neu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Simone Pajonk
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hye Sup Yun
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ulrike Lipka
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Matt Humphry
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Stefan Bau
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Marco Straus
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Mark Kwaaitaal
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Heike Rampelt
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Farid El Kasmi
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Gerd Jürgens
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Jane Parker
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Ralph Panstruga
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Volker Lipka
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Paul Schulze-Lefert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Ralph Panstruga, Volker Lipka or Paul Schulze-Lefert.

Supplementary information

Supplementary Information

This file contains Supplementary Table 1, Supplementary Figures 1-8 with Legends and Supplementary Notes detailing authors’ contributions in a form of a table. (PDF 1400 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kwon, C., Neu, C., Pajonk, S. et al. Co-option of a default secretory pathway for plant immune responses. Nature 451, 835–840 (2008). https://doi.org/10.1038/nature06545

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature06545

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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