Abstract

Accelerated adaptive evolution is a hallmark of plant–pathogen interactions. Plant intracellular immune receptors (NLRs) often occur as allelic series with differential pathogen specificities. The determinants of this specificity remain largely unknown. Here, we unravelled the biophysical and structural basis of expanded specificity in the allelic rice NLR Pik, which responds to the effector AVR-Pik from the rice blast pathogen Magnaporthe oryzae. Rice plants expressing the Pikm allele resist infection by blast strains expressing any of three AVR-Pik effector variants, whereas those expressing Pikp only respond to one. Unlike Pikp, the integrated heavy metal-associated (HMA) domain of Pikm binds with high affinity to each of the three recognized effector variants, and variation at binding interfaces between effectors and Pikp-HMA or Pikm-HMA domains encodes specificity. By understanding how co-evolution has shaped the response profile of an allelic NLR, we highlight how natural selection drove the emergence of new receptor specificities. This work has implications for the engineering of NLRs with improved utility in agriculture.

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Acknowledgements

This work was supported by the BBSRC (grants BB/J00453, BB/P012574 and BB/M02198X), the ERC (proposal 743165), the John Innes Foundation, the Gatsby Charitable Foundation and JSPS KAKENHI 15H05779. We thank the Diamond Light Source (beamlines I03 and I04 under proposals MX9475 and MX13467) for access to X-ray data collection facilities. We also thank D. Lawson and C. Stevenson (JIC X-ray Crystallography/Biophysical Analysis Platform) for help with protein structure determination and SPR.

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Author notes

  1. These authors contributed equally: De la Concepcion, J. C. and Franceschetti, M.

Affiliations

  1. Department of Biological Chemistry, John Innes Centre, Norwich Research Park, Norwich, UK

    • Juan Carlos De la Concepcion
    • , Marina Franceschetti
    • , Abbas Maqbool
    •  & Mark J. Banfield
  2. Laboratory of Plant Symbiotic and Parasitic Microbes, Department of Molecular Microbiology, Faculty of Life Sciences, Tokyo University of Agriculture, Tokyo, Japan

    • Hiromasa Saitoh
  3. Division of Genomics and Breeding, Iwate Biotechnology Research Center, Iwate, Japan

    • Ryohei Terauchi
  4. Laboratory of Crop Evolution, Graduate School of Agriculture, Kyoto University, Kyoto, Japan

    • Ryohei Terauchi
  5. The Sainsbury Laboratory, Norwich Research Park, Norwich, UK

    • Sophien Kamoun

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Contributions

J.C.D.l.C. and M.F. performed all of the experiments. J.C.D.l.C., M.F. and M.J.B. designed the experiments and analysed the data. A.M. and H.S. assisted with construct design and the initial protein production. R.T. and S.K. analysed the data. J.C.D.l.C., M.F. and M.J.B. wrote the manuscript with input from all authors.

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The authors declare no competing interests.

Corresponding author

Correspondence to Mark J. Banfield.

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https://doi.org/10.1038/s41477-018-0194-x