Yueqiang Leng, Florian Kümmel, Mingxia Zhao, István Molnár, Jaroslav Doležel, Elke Logemann, Petra Köchner, Pinggen Xi, Shengming Yang, Matthew J. Moscou, Jason D. Fiedler, Yang Du, Burkhard Steuernagel, Steven Meinhardt, Brian J. Steffenson, Paul Schulze-Lefert, Shaobin Zhong
{"title":"A barley MLA immune receptor is activated by a fungal nonribosomal peptide effector for disease susceptibility","authors":"Yueqiang Leng, Florian Kümmel, Mingxia Zhao, István Molnár, Jaroslav Doležel, Elke Logemann, Petra Köchner, Pinggen Xi, Shengming Yang, Matthew J. Moscou, Jason D. Fiedler, Yang Du, Burkhard Steuernagel, Steven Meinhardt, Brian J. Steffenson, Paul Schulze-Lefert, Shaobin Zhong","doi":"10.1111/nph.20289","DOIUrl":null,"url":null,"abstract":"<p>\n</p><ul>\n<li>The barley <i>Mla</i> 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.</li>\n<li>In this study, we isolated a barley gene <i>Scs6</i>, which is an allelic variant of <i>Mla</i> genes but confers susceptibility to the isolate ND90Pr (<i>Bs</i><sub>ND90Pr</sub>) of the necrotrophic fungus <i>Bipolaris sorokiniana</i>. We generated <i>Scs6</i> transgenic barley lines and showed that <i>Scs6</i> is sufficient to confer susceptibility to <i>Bs</i><sub>ND90Pr</sub> in barley genotypes naturally lacking the receptor. The <i>Scs6-</i>encoded NLR (SCS6) is activated by a nonribosomal peptide (NRP) effector produced by <i>Bs</i><sub>ND90Pr</sub> to induce cell death in barley and <i>Nicotiana benthamiana</i>. 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.</li>\n<li><i>Scs6</i> is maintained in both wild and domesticated barley populations. Our phylogenetic analysis suggests that <i>Scs6</i> is a <i>Hordeum</i>-specific innovation.</li>\n<li>We infer that SCS6 is a <i>bona fide</i> immune receptor that is likely directly activated by the nonribosomal peptide effector of <i>Bs</i><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.</li>\n</ul><p></p>","PeriodicalId":214,"journal":{"name":"New Phytologist","volume":"81 1","pages":""},"PeriodicalIF":8.3000,"publicationDate":"2024-12-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"New Phytologist","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1111/nph.20289","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PLANT SCIENCES","Score":null,"Total":0}
引用次数: 0
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 (BsND90Pr) of the necrotrophic fungus Bipolaris sorokiniana. We generated Scs6 transgenic barley lines and showed that Scs6 is sufficient to confer susceptibility to BsND90Pr in barley genotypes naturally lacking the receptor. The Scs6-encoded NLR (SCS6) is activated by a nonribosomal peptide (NRP) effector produced by BsND90Pr 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 BsND90Pr 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.
期刊介绍:
New Phytologist is an international electronic journal published 24 times a year. It is owned by the New Phytologist Foundation, a non-profit-making charitable organization dedicated to promoting plant science. The journal publishes excellent, novel, rigorous, and timely research and scholarship in plant science and its applications. The articles cover topics in five sections: Physiology & Development, Environment, Interaction, Evolution, and Transformative Plant Biotechnology. These sections encompass intracellular processes, global environmental change, and encourage cross-disciplinary approaches. The journal recognizes the use of techniques from molecular and cell biology, functional genomics, modeling, and system-based approaches in plant science. Abstracting and Indexing Information for New Phytologist includes Academic Search, AgBiotech News & Information, Agroforestry Abstracts, Biochemistry & Biophysics Citation Index, Botanical Pesticides, CAB Abstracts®, Environment Index, Global Health, and Plant Breeding Abstracts, and others.