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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.

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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.

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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.

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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

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

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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)

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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

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