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

Authors: LENG, YUEQIANG - North Dakota State University; KUMMEL, FLORIAN - Max Planck Institute For Plant Breeding Research; ZHAO, MINGXIA - North Dakota State University; MOLNAR, ISTVAN - Academy Of Sciences Of The Czech Republic (ASCR); DOLEZEL, JAROSLAV - Academy Of Sciences Of The Czech Republic (ASCR); LOGEMANN, ELKE - Max Planck Institute For Plant Breeding Research; KOCHNER, PETRA - Max Planck Institute For Plant Breeding Research; XI, PINGGEN - North Dakota State University; Yang, Shengming; Moscou, Matthew; Fiedler, Brett; DU, YANG - Valley City State University; STEUERNAGEL, BURKHARD - John Innes Center; MEINHARDT, STEVEN - North Dakota State University; STEFFENSON, BRIAN - University Of Minnesota; SCHULZE-LEFERT, PAUL - Max Planck Institute For Plant Breeding Research; ZHONG, SHAOBIN - North Dakota State University

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/1/2024
Publication Date: N/A
Citation: N/A

Interpretive Summary: Spot blotch, caused by a necrotrophic fungal pathogen is an economically important disease of barley. This pathogen can only feed on dead plant tissues, and killing infected plant cells is critical for the pathogen to thrive in the host. As a result, understanding the mechanism underlying the induced cell death by this pathogen will provide avenues to defense barley plants from spot botch infection. However, knowledge in this regard is incomplete. In this study, we cloned a gene named Scs6 which is required for disease susceptibility to spot blotch in barley. Activated by a special chemical secreted by this pathogen, Scs6 triggers cell death in barley leaves, forming nutrient source for the invading pathogen. Therefore, cloning of Scs6 advances our knowledge of disease susceptibility to spot blotch and provides a target for geneticists to manipulate for barley variety improvement.

Technical Abstract: The evolutionary history of plant interactions with necrotrophic pathogens that feed on dying host cells and their virulence mechanisms remain fragmentary. We have isolated the barley gene Scs6, required for the necrotrophic fungus Bipolaris sorokiniana isolate ND90Pr, to cause spot blotch disease. Scs6 is located at the disease resistance gene locus mildew Mildew locus aA (Mla) and encodes an intracellular nucleotide-binding leucine-rich repeat receptor (NLR). In transgenic barley, Scs6 is sufficient to confer susceptibility to ND90Pr in accessions naturally lacking the receptor, resulting in infection-associated host cell death. Expression of Scs6 in evolutionarily distant Nicotiana benthamiana reconstitutes a cell death response to an uncharacterized non-ribosomal peptide effector produced by ND90Pr-specific non-ribosomal peptide synthetases (NRPSs) encoded at the VHv1 virulence locus of the pathogen. Our data suggest that the effector directly activates the SCS6 receptor. Scs6 is an allelic variant of functionally diversified Mla resistance genes, each which conferring strain-specific immunity to barley powdery mildew strains with a matching proteinaceous pathogen effector. Domain swaps between MLA and SCS6 NLRs and expression of the resulting hybrid proteins in N. benthamiana reveal that the SCS6 leucine-rich repeat domain is a specificity determinant for the NRPS-derived effector to activate the receptor. Scs6 evolved after the divergence of barley from its sister species wheat and is maintained in several wild barley populations with an incidence of 8%, suggesting a beneficial function for the host. Evolution of the bona fide immune receptor SCS6 targeted by the NRPS-derived effector was key for the emergence of a strain-specific spot blotch disease in domesticated barley.