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). 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.

Knocking on the heaven’s wall: pathogenesis of and resistance to biotrophic fungi at the cell wall

“…This is consistent with an earlier hypothesis that plants limit pathogen growth even in compatible interactions by mounting inefficient resistance responses [26]. Of the 24 Arabidopsis syntaxins, PEN1 has the greatest resemblance to barley ROR2 [21 ]. PEN1 can complement the barley ror2 mutant phenotype, hence the dicot PEN1 and monocot ROR2 syntaxin genes appear to be functionally synonymous.…”

“…In living barley leaf epidermal cells, the transiently expressed fluorescent reporter fusion proteins MLO::yellow fluorescent protein (YFP) and ROR2:: cyan fluorescent protein (CFP) produce a strong fluorescence resonance energy transfer (FRET) signal, indicating that a direct MLO-ROR2 interaction occurs in vivo (R Bhat, R Panstruga, P Schulze- Lefert, unpublished;[43]). A mutant ROR2 protein, which lacked 31 amino acids in the amino-terminal autoinhibitory domain, accumulated like the wildtype protein in the plasma membrane but failed to generate a FRET signal upon co-expression with MLO-YFP (R Bhat, R Panstruga, P Schulze- Lefert, unpublished;[21 ,44]). Thus, MLO might sequester monomeric ROR2 in an inactive complex, thereby inhibiting/delaying productive cycling between free ROR2 and a SNARE complex that involves both HvSNAP34 and a putative v-SNARE.…”

“…In wildtype Arabidopsis, nonhost resistance to the grass powdery mildew fungus Blumeria graminis f. sp. hordei (Bgh) is tightly associated with CWA formation and the failure of fungal sporelings to enter attacked leaf epidermal cells at most interaction sites [21 ]. Recessive mutations in PENETRATION1 (PEN1), PEN2 or PEN3 result in cell wall penetration rates of Bgh sporelings that are enhanced by up to seven-fold and allow the subsequent differentiation of haustorial complexes in leaf epidermal cells.…”

“…The apparent conservation of an isoformspecific syntaxin function in barley and Arabidopsis demonstrates that basal penetration resistance and nonhost resistance to Bgh share at least one common component. Further evidence for the involvement of SNARE-dependent resistance at the cell periphery came from the observation that a barley SNAP25 homologue, designated HvSNAP34, is required for basal penetration resistance to Bgh, contains two SNARE domains, and is capable of forming a binary SNARE complex together with ROR2 [21 ].…”

Construction of a dense SNP map of a highly heterozygous diploid potato population and QTL analysis of tuber shape and eye depth

“…The SNP confidence intervals are given in Table 2 protein is predicted to interact in a SNARE (SNAP [Soluble NSF [N-ethylmaleimide-Sensitive Factor] Attachment Protein] REceptor) complex. Proteins in Arabidopsis thaliana interacting in SNARE complexes were shown to be responsible for non-host resistance to powdery mildew of barley (Collins et al 2003). VIT_14s0068g01970, which is involved in xylan biosynthesis, is another promising candidate gene because the presence of xylan, a type of hemicellulose, was shown to be associated with increased infection of Fusarium herbarum on wheat (Wingard 1941).…”