A barley <scp>MLA</scp> immune receptor is activated by a fungal nonribosomal peptide effector for disease susceptibility
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<sub>ND90Pr</sub>) of the necrotrophic fungus Bipolaris sorokiniana. We generated Scs6 transgenic barley lines and showed that Scs6 is sufficient to confer susceptibility to Bs<sub>ND90Pr</sub> in barley genotypes naturally lacking the receptor. The Scs6-encoded NLR (SCS6) is activated by a nonribosomal peptide (NRP) effector produced by Bs<sub>ND90Pr</sub> 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<sub>ND90Pr</sub> 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.
Authors
- Paul Schulze‐Lefert (ORCID: https://orcid.org/0000-0002-8978-1717)
- Florian Kümmel (ORCID: https://orcid.org/0009-0006-2169-0890)
- Shengming Yang (ORCID: https://orcid.org/0000-0002-4558-8448)
- Jaroslav Doležel (ORCID: https://orcid.org/0000-0002-6263-0492)
- Petra Köchner (ORCID: https://orcid.org/0009-0003-6322-2487)
- Jason D. Fiedler (ORCID: https://orcid.org/0000-0001-7736-4484)
- Pinggen Xi (ORCID: https://orcid.org/0000-0002-1247-3898)
- Elke Logemann (ORCID: https://orcid.org/0000-0002-0478-8072)
- Burkhard Steuernagel (ORCID: https://orcid.org/0000-0002-8284-7728)
- Brian J. Steffenson (ORCID: https://orcid.org/0000-0001-7961-5363)
- Matthew Moscou (ORCID: https://orcid.org/0000-0003-2098-6818)
- Yueqiang Leng (ORCID: https://orcid.org/0009-0008-5085-7623)
- Shaobin Zhong (ORCID: https://orcid.org/0000-0003-1928-0877)
- Mingxia Zhao (ORCID: https://orcid.org/0000-0003-3247-9899)
- Yang Du (ORCID: https://orcid.org/0000-0001-5497-1898)
- István Molnár (ORCID: https://orcid.org/0000-0002-7167-9319)
- Steven W. Meinhardt (ORCID: https://orcid.org/0009-0001-0029-3136)
Institutions
- John Innes Centre (GB)
- South China Agricultural University (CN)
- University of Minnesota (US)
- Valley City State University (US)
- Norwich Research Park (GB)
- Cluster of Excellence on Plant Sciences (DE)
- Max Planck Institute for Plant Breeding Research (DE)
- HUN-REN Centre for Agricultural Research (HU)
- Czech Academy of Sciences, Institute of Experimental Botany (CZ)
- Cereal Disease Laboratory (US)
- Edward T. Schafer Agricultural Research Center (US)
- North Dakota State University (US)
Publication Details
- Journal
- New Phytologist
- Published
- 2024-12-06
- DOI
- https://doi.org/10.1111/nph.20289
- Citations
- 3
- Primary Topic
- Plant-Microbe Interactions and Immunity
- Type
- article
- Field-Weighted Citation Impact
- 1.80
Funders
- Deutsche Forschungsgemeinschaft
- National Institute of Food and Agriculture
- Agricultural Research Service