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

Abstract

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.

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Acknowledgements

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). https://doi.org/10.1038/nature02076

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