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SNARE-protein-mediated disease resistance at the plant cell wall


Failure of pathogenic fungi to breach the plant cell wall constitutes a major component of immunity of non-host plant species—species outside the pathogen host range—and accounts for a proportion of aborted infection attempts on ‘susceptible’ host plants (basal resistance)1,2,3,4. Neither form of penetration resistance is understood at the molecular level. We developed a screen for penetration (pen) mutants of Arabidopsis, which are disabled in non-host penetration resistance against barley powdery mildew, Blumeria graminis f. sp. hordei, and we isolated the PEN1 gene. We also isolated barley ROR2 (ref. 2), which is required for basal penetration resistance against B. g. hordei. The genes encode functionally homologous syntaxins, demonstrating a mechanistic link between non-host resistance and basal penetration resistance in monocotyledons and dicotyledons. We show that resistance in barley requires a SNAP-25 (synaptosome-associated protein, molecular mass 25 kDa) homologue capable of forming a binary SNAP receptor (SNARE) complex with ROR2. Genetic control of vesicle behaviour at penetration sites, and plasma membrane location of PEN1/ROR2, is consistent with a proposed involvement of SNARE-complex-mediated exocytosis and/or homotypic vesicle fusion events in resistance. Functions associated with SNARE-dependent penetration resistance are dispensable for immunity mediated by race-specific resistance (R) genes, highlighting fundamental differences between these two resistance forms.

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Figure 1: PEN1 and ROR2 are functionally homologous syntaxins.
Figure 2: The barley SNAP-25 homologue HvSNAP34 is required for penetration resistance.
Figure 3: ROR2 interactions and overexpression.
Figure 4: Blumeria graminis hordei-induced vesicles.


  1. Johnson, L. E. B., Bushnell, W. R. & Zeyen, R. J. Defense patterns in nonhost higher plant species against two powdery mildew fungi. I. Monocotyledonous species. Can. J. Bot. 60, 1068–1083 (1982)

    Article  Google Scholar 

  2. Freialdenhoven, A., Peterhänsel, C., Kurth, J., Kreuzaler, F. & Schulze-Lefert, P. Identification of genes required for the function of non-race-specific mlo resistance to powdery mildew in barley. Plant Cell 8, 5–14 (1996)

    CAS  Article  Google Scholar 

  3. Hoogkamp, T. J. H., Chen, W. Q. & Niks, R. E. Specificity of prehaustorial resistance to Puccinia hordei and to two inappropriate rust fungi in barley. Phytopathology 88, 856–861 (1998)

    CAS  Article  Google Scholar 

  4. Mellersh, D. G., Foulds, I. V., Higgins, V. J. & Heath, M. C. H2O2 plays different roles in determining penetration failure in three diverse plant-fungal interactions. Plant J. 29, 257–268 (2002)

    CAS  Article  Google Scholar 

  5. Hammond-Kosack, K. E. & Parker, J. E. Deciphering plant-pathogen communication: fresh perspecitives for molecular resistance breeding. Curr. Opin. Biotechnol. 14, 177–193 (2003)

    CAS  Article  Google Scholar 

  6. Peterhänsel, C., Freialdenhoven, A., Kurth, J., Kolsch, R. & Schulze-Lefert, P. Interaction analyses of genes required for resistance responses to powdery mildew in barley reveal distinct pathways leading to leaf cell death. Plant Cell 9, 1397–1409 (1997)

    Article  Google Scholar 

  7. 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)

    CAS  Article  Google Scholar 

  8. Blatt, M. R. Toward understanding vesicle traffic and the guard cell model. New Phytol. 153, 405–413 (2002)

    CAS  Article  Google Scholar 

  9. Jahn, R., Lang, T. & Südhof, T. C. Membrane fusion. Cell 112, 519–533 (2003)

    CAS  Article  Google Scholar 

  10. Fasshauer, D., Sutton, R. B., Brunger, A. T. & Jahn, R. Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs. Proc. Natl Acad. Sci. USA 95, 15781–15786 (1998)

    ADS  CAS  Article  Google Scholar 

  11. Shen, Q. H. et al. Recognition specificity and RAR1/SGT1 dependence in barley Mla disease resistance genes to the powdery mildew fungus. Plant Cell 15, 732–744 (2003)

    CAS  Article  Google Scholar 

  12. Lerman, J. C., Robblee, J., Fairman, R. & Hughson, F. M. Structural analsysis of the neuronal SNARE protein syntaxin-1A. Biochemistry 39, 8470–8479 (2000)

    CAS  Article  Google Scholar 

  13. Munson, M., Chen, X., Cocina, A. E., Schultz, S. M. & Hughson, F. M. Interactions within the yeast t-SNARE Sso1p that control SNARE complex assembly. Nature Struct. Biol. 7, 894–902 (2000)

    CAS  Article  Google Scholar 

  14. Misura, K. M. S., Scheller, R. H. & Weis, W. I. Self-association of the H3 region of syntaxin 1A. J. Biol. Chem. 276, 13273–13282 (2001)

    CAS  Article  Google Scholar 

  15. Hückelhoven, R., Fodor, J., Preis, C. & Kogel, K. H. Hypersensitive cell death and papilla formation in barley attacked by the powdery mildew fungus are associated with hydrogen peroxide but not with salicylic acid accumulation. Plant Physiol. 119, 1251–1260 (1999)

    Article  Google Scholar 

  16. Lauber, M. H. et al. The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. J. Cell Biol. 139, 1485–1493 (1997)

    CAS  Article  Google Scholar 

  17. Betz, W. J. & Richards, D. A. What goes out must come in. Nature Neurosci. 3, 636–637 (2000)

    CAS  Article  Google Scholar 

  18. Emans, N., Zimmerman, S. & Fischer, R. Uptake of fluorescent marker in plant cells is sensitive to brefeldin A and wortmannin. Plant Cell 14, 71–86 (2002)

    CAS  Article  Google Scholar 

  19. Lamb, C. & Dixon, R. A. The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 251–275 (1997)

    CAS  Article  Google Scholar 

  20. Snyder, B. A. & Nicholson, R. L. Synthesis of phytoalexins in sorghum as a site-specific response to fungal ingress. Science 248, 1637–1639 (1990)

    ADS  CAS  Article  Google Scholar 

  21. Adam, L. & Somerville, S. C. Genetic characterization of five powdery mildew disease resistance loci in Arabidopsis thaliana. Plant J. 9, 341–356 (1996)

    CAS  Article  Google Scholar 

  22. Yu, Y. et al. A bacterial artificial chromosome library for barley (Hordeum vulgare L.) and the identification of clones containing putative resistance genes. Theor. Appl. Genet. 101, 1093–1099 (2000)

    CAS  Article  Google Scholar 

  23. Koga, H., Bushnell, W. R. & Zeyen, R. J. Specificity of cell type and timing of events associated with papilla formation and the hypersensitive reaction in leaves of Hordeum vulgare attacked by Erysiphe graminis f. sp hordei. Can. J. Bot. 68, 2344–2352 (1990)

    Article  Google Scholar 

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

    ADS  CAS  Article  Google Scholar 

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This work was supported by Syngenta, the Max Planck Society, the Gatsby Charitable Foundation, the Danish Agricultural and Veterinary Research Council, the GABI Non-host Resistance Consortium (Bundesministerium für Bildung und Forschung), the Carnegie Institution of Washington, and the US Department of Energy. M.S. was supported in part by a Stanford Graduate Fellowship. N.C.C. thanks the host group of K. Shirasu in the Sainsbury Laboratory. We thank R. Bradbourne and H. Tippmann for technical assistance; M. Gale for microsatellite primers; M. Miklis and J. Uhrig for silencing and yeast two-hybrid vectors; R. Serrano and R. Napier for H+-ATPase and CALRETICULIN antisera; and R. Oliver for the GUS reporter construct.

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Correspondence to Paul Schulze-Lefert.

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Collins, N., Thordal-Christensen, H., Lipka, V. et al. SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425, 973–977 (2003).

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