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Polymorphic residues in rice NLRs expand binding and response to effectors of the blast pathogen

Nature Plants volume 4, pages 576–585 (2018)Cite this article

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A Publisher Correction to this article was published on 20 August 2018

This article has been updated

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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Fig. 1: The Pikm-mediated cell death response to AVR-Pik effector variants in N. benthamiana phenocopies the Pikm resistance profile in rice.
Fig. 2: Different affinities underpin the recognition and response of Pik NLR alleles to AVR-Pik effector variants.
Fig. 3: Structures of Pikm-HMA in complex with AVR-Pik effectors.
Fig. 4: Different interactions at interface 3 in the complexes of Pikm-HMA and Pikp-HMA with AVR-PikD support recognition and response.
Fig. 5: Altered interactions across the interfaces of Pikp-HMA with AVR-PikD and AVR-PikE underpin the differences in recognition and response.
Fig. 6: Mutations at different interfaces in the Pik-HMA–effector complexes have differential effects on interactions and phenotypes.

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Change history

  • 20 August 2018

    In the version of this Article originally published, in Fig. 1b the single-letter code for the amino acid polymorphism at position 46 in the schematic of the AVR-PikE variant was incorrectly given as ‘H’. The correct amino acid is ‘N’. This has now been amended in all versions of the Article.

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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.

Authors and 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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Correspondence to Mark J. Banfield.

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De la Concepcion, J.C., Franceschetti, M., Maqbool, A. et al. Polymorphic residues in rice NLRs expand binding and response to effectors of the blast pathogen. Nature Plants 4, 576–585 (2018). https://doi.org/10.1038/s41477-018-0194-x

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