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Wheat receptor-kinase-like protein Stb6 controls gene-for-gene resistance to fungal pathogen Zymoseptoria tritici

Nature Genetics volume 50, pages 368–374 (2018)Cite this article

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Abstract

Deployment of fast-evolving disease-resistance genes is one of the most successful strategies used by plants to fend off pathogens1,2. In gene-for-gene relationships, most cloned disease-resistance genes encode intracellular nucleotide-binding leucine-rich-repeat proteins (NLRs) recognizing pathogen-secreted isolate-specific avirulence (Avr) effectors delivered to the host cytoplasm3,4. This process often triggers a localized hypersensitive response, which halts further disease development5. Here we report the map-based cloning of the wheat Stb6 gene and demonstrate that it encodes a conserved wall-associated receptor kinase (WAK)-like protein, which detects the presence of a matching apoplastic effector6,7,8 and confers pathogen resistance without a hypersensitive response9. This report demonstrates gene-for-gene disease resistance controlled by this class of proteins in plants. Moreover, Stb6 is, to our knowledge, the first cloned gene specifying resistance to Zymoseptoria tritici, an important foliar fungal pathogen affecting wheat and causing economically damaging septoria tritici blotch (STB) disease10,11,12.

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Fig. 1: Map-based cloning of the Stb6 resistance gene.
Fig. 2: Functional analysis of candidate genes through barley stripe mosaic virus (BSMV)-mediated VIGS.
Fig. 3: Mutational analysis of TaWAKL4 and TaWAKL3.
Fig. 4: TaWAKL4 confers resistance to Z. tritici IPO323 when stably transferred into a susceptible wheat background.
Fig. 5: Sequence and biochemical characterization of natural and induced Stb6 haplotypes.

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Acknowledgements

We thank the Biological Resource Centre on Small Grain Cereals (INRA, Clermont-Ferrand, France), the National Plant Germplasm System (USDA, US), the Germplasm Resources Unit (John Innes Centre, Norwich, UK), and the breeding companies KWS, Limagrain, RAGT Seeds, Saaten Union, Senova, Syngenta, Agri Obtentions, and Saatzucht Josef Breun GmbH & Co. KG for providing seed samples of different wheat species and varieties; E. Paux and H. Rimbert (INRA GDEC) for providing Stb6 expression data at different developmental stages; A. Doherty, A. Huttly, and C. Sparks (Rothamsted Research, Harpenden, UK) for vectors and wheat transformation; P. Isaac (iDNA Genetics Ltd., Norwich, UK) for transgene copy number analyses; INRA GDEC facilities for genotyping (GENTYANE) and wheat transformation; and S. Thomas (Rothamsted Research, Harpenden, UK) for providing vectors and protocols, and advice on the Y2H assay. We are also grateful to the International Wheat Genome Sequencing Consortium and K. Eversole for prepublication access to the IWGSC v1.0 wheat genome assembly. Research was funded by the Institute Strategic Program Grants ’20:20 Wheat’ (BB/J/00426×/1) and Designing Future Wheat (BB/P016855/1) from the Biotechnology and Biological Sciences Research Council of the UK (BBSRC) and the French National Institute for Agricultural Research (INRA).

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Authors and Affiliations

  1. INRA/UBP UMR 1095 Genetics, Diversity and Ecophysiology of Cereals (GDEC), Clermont-Ferrand, France

    Cyrille Saintenac, Florence Cambon & Thierry Langin

  2. Biointeractions and Crop Protection, Rothamsted Research, Harpenden, UK

    Wing-Sham Lee, Jason J. Rudd, Kim E. Hammond-Kosack & Kostya Kanyuka

  3. Computational and Analytical Sciences, Rothamsted Research, Harpenden, UK

    Robert C. King & Stephen J. Powers

  4. Centre National des Ressources Génomiques Végétales (CNRGV), INRA UPR 1258, Castanet-Tolosan, France

    William Marande & Hélène Bergès

  5. Plant Sciences, Rothamsted Research, Harpenden, UK

    Andy L. Phillips

  6. Crop Genetics, John Innes Centre, Norwich Research Park, Norwich, UK

    Cristobal Uauy

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  1. Cyrille Saintenac
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Contributions

K.K., K.E.H.-K., C.S., and T.L. conceived the project. W.M. and H.B. screened the wheat BAC library. A.L.P., R.C.K., and C.U. provided the TILLING data. R.C.K. performed bioinformatics analyses and analyzed RNA-seq data. W.-S.L. performed VIGS. J.J.R. performed biochemical assays. S.J.P. performed statistical analysis. F.C., C.S., and K.K. carried out all other experiments and analyzed the data. K.K. and C.S. wrote the manuscript, and all authors revised the manuscript.

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Correspondence to Cyrille Saintenac or Kostya Kanyuka.

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Rothamsted Research filed an International Patent Application (no. PCT/GB2016/053929 entitled ‘Plant Fungal Resistance Gene’) related to the content of this manuscript, on behalf of K.K., C.S., F.C., T.L., W.-S.L., and K.E.H.-K.

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Saintenac, C., Lee, WS., Cambon, F. et al. Wheat receptor-kinase-like protein Stb6 controls gene-for-gene resistance to fungal pathogen Zymoseptoria tritici. Nat Genet 50, 368–374 (2018). https://doi.org/10.1038/s41588-018-0051-x

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