A barley MLA receptor is targeted by a non-ribosomal peptide effector of the necrotrophic spot blotch fungus for disease susceptibility

Abstract

AbstractThe evolutionary history of plant interactions with necrotrophic pathogens that feed on dying host cells and their virulence mechanisms remains fragmentary. We have isolated the barley geneScs6, which is required for the necrotrophic fungusBipolaris sorokinianaisolate ND90Pr to cause spot blotch disease.Scs6is located at the disease resistance gene locusMildew locus a(Mla) and encodes an intracellular nucleotide-binding leucine-rich repeat receptor (NLR). In transgenic barley,Scs6is sufficient to confer susceptibility to ND90Pr in accessions naturally lacking the receptor, resulting in infection-associated host cell death. Expression ofScs6in evolutionarily distantNicotiana benthamianareconstitutes a cell death response to an uncharacterized non-ribosomal peptide effector produced by ND90Pr-specific non-ribosomal peptide synthetases (NRPSs) encoded at theVHv1virulence locus. Our data suggest that the heat-resistant effector directly activates the SCS6 receptor.Scs6is an allelic variant of functionally diversifiedMlaresistance genes each conferring strain-specific immunity to barley powdery mildew isolates with a matching proteinaceous pathogen effector. Domain swaps between MLA and SCS6 NLRs and expression of the resulting hybrid proteins inN. benthamianareveal that the SCS6 leucine-rich repeat domain is a specificity determinant for the NRPS-derived effector to activate the receptor.Scs6evolved after the divergence of barley from wheat and is maintained in several wild barley populations with an incidence of 8%, suggesting a beneficial function for the host. Evolution of thebona fideimmune receptor SCS6 targeted by the NRPS-derived effector was key for the emergence of strain-specific spot blotch disease in domesticated barley.