A barley MLA immune receptor is activated by a fungal nonribosomal peptide effector for disease susceptibility

Abstract

• The barley Mla locus contains functionally diversified genes that encode intracellular nucleotide-binding leucine-rich repeat receptors (NLRs) and confer strain-specific immunity to biotrophic and hemibiotrophic fungal pathogens.
• In this study, we isolated a barley gene Scs6, which is an allelic variant of Mla genes but confers susceptibility to the isolate ND90Pr (Bs_ND90Pr) of the necrotrophic fungus Bipolaris sorokiniana. We generated Scs6 transgenic barley lines and showed that Scs6 is sufficient to confer susceptibility to Bs_ND90Pr in barley genotypes naturally lacking the receptor. The Scs6-encoded NLR (SCS6) is activated by a nonribosomal peptide (NRP) effector produced by Bs_ND90Pr to induce cell death in barley and Nicotiana benthamiana. Domain swaps between MLAs and SCS6 reveal that the SCS6 leucine-rich repeat domain is a specificity determinant for receptor activation by the NRP effector.
• Scs6 is maintained in both wild and domesticated barley populations. Our phylogenetic analysis suggests that Scs6 is a Hordeum-specific innovation.
• We infer that SCS6 is a bona fide immune receptor that is likely directly activated by the nonribosomal peptide effector of Bs_ND90Pr for disease susceptibility in barley. Our study provides a stepping stone for the future development of synthetic NLR receptors in crops that are less vulnerable to modification by necrotrophic pathogens.