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A complex resistance locus in Solanum americanum recognizes a conserved Phytophthora effector

Nature Plants volume 7, pages 198–208 (2021)Cite this article

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Abstract

Late blight caused by Phytophthora infestans greatly constrains potato production. Many Resistance (R) genes were cloned from wild Solanum species and/or introduced into potato cultivars by breeding. However, individual R genes have been overcome by P. infestans evolution; durable resistance remains elusive. We positionally cloned a new R gene, Rpi-amr1, from Solanum americanum, that encodes an NRC helper-dependent CC-NLR protein. Rpi-amr1 confers resistance in potato to all 19 P. infestans isolates tested. Using association genomics and long-read RenSeq, we defined eight additional Rpi-amr1 alleles from different S. americanum and related species. Despite only ~90% identity between Rpi-amr1 proteins, all confer late blight resistance but differentially recognize Avramr1 orthologues and paralogues. We propose that Rpi-amr1 gene family diversity assists detection of diverse paralogues and alleles of the recognized effector, facilitating durable resistance against P. infestans.

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Fig. 1: Map-based cloning of Rpi-amr1 and its resistance to P. infestans.
Fig. 2: Rpi-amr1 homologues and their phenotypes in transient assays.
Fig. 3: Differential recognition of Rpi-amr1 and Avramr1 homologues.
Fig. 4: Rpi-amr1 is NRC2- or NRC3-dependent.

Data availability

Supporting raw reads were deposited in European Nucleotide Archive under project number PRJEB38240. BAC and Rpi-amr1 allele sequences were deposited in GenBank under accession numbers MW345286-95 and MW348763. Detailed accession information is shown in Supplementary Table 7. All the materials in this study are available upon request.

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Acknowledgements

This research was financed from BBSRC grant no. BB/P021646/1 and the Gatsby Charitable Foundation. This research was supported in part by the NBI Computing infrastructure for Science (CiS) group through the provision of a High-Performance Computing Cluster. We would like to thank TSL bioinformatics team, transformation team and horticultural team for their support. We thank Experimental Garden and Genebank of Radboud University (Nijmegen, the Netherlands), IPK Gatersleben (Germany) and S. Knapp (Natural History Museum, London, United Kingdom) for access to S. americanum, S. nigrescens and S. nigrum genetic diversity and G. Kessel, F. Govers and P. Birch for providing P. infestans isolates.

Author information

Author notes

  1. Hari S. Karki

    Present address: US Department of Agriculture–Agricultural Research Service, Madison, WI, USA

  2. Florian Jupe

    Present address: Bayer Crop Science, Chesterfield, MO, USA

  3. William Barrett

    Present address: The New Zealand Institute for Plant & Food Research Ltd, Nelson, New Zealand

  4. Chih-Hang Wu

    Present address: Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan

  5. Tianqiao Song

    Present address: Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing, P. R. China

  6. These authors contributed equally: K. Witek, X. Lin, H. S. Karki.

Authors and Affiliations

  1. The Sainsbury Laboratory, University of East Anglia, Norwich Research Park, Norwich, UK

    Kamil Witek, Xiao Lin, Hari S. Karki, Florian Jupe, Agnieszka I. Witek, Sebastian Fairhead, Robert Heal, William Barrett, Chih-Hang Wu, Hiroaki Adachi, Tianqiao Song, Sophien Kamoun, Laurence Tomlinson & Jonathan D. G. Jones

  2. John Innes Centre, Norwich Research Park, Norwich, UK

    Burkhard Steuernagel & Brande B. H. Wulff

  3. Phytopathology, Technical University Munich, Freising, Germany

    Remco Stam

  4. School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich, UK

    Cock van Oosterhout

  5. Faculty of Biological Sciences, University of Leeds, Leeds, UK

    Jonathan M. Cocker

  6. University of Hull, Hull, UK

    Jonathan M. Cocker

  7. Plant Breeding, Wageningen University and Research, Wageningen, the Netherlands

    Shivani Bhanvadia & Vivianne G. A. A. Vleeshouwers

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Contributions

K.W., X.L., F.J., R.S., C.O. and J.D.G.J. designed the study. K.W., X.L., H.S.K., F.J., A.I.W., S.B., R.H., W.B., L.T. and T.S. performed the experiments. K.W., X.L., H.S.K., F.J., A.I.W., B.S., R.S., C.O., S.F. and J.M.C. analysed the data. K.W., X.L., H.S.K., F.J. and J.D.G.J. wrote the manuscript with input from all authors. V.G.A.A.V., B.B.H.W, C.-H.W., H.A. and S.K. contributed resources. All authors approved the manuscript.

Corresponding author

Correspondence to Jonathan D. G. Jones.

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Competing interests

K.W., H.S.K., F.G.J. and J.D.G.J. are named inventors on a patent application (PCT/US2017/066691) pertaining to Rpi-amr1 that was filed by the 2Blades Foundation on behalf of the Sainsbury Laboratory. The other authors declare no competing interests.

Additional information

Peer review information Nature Plants thanks Erik Andreasson, Marc Ghislain and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–8 and Tables 1–4.

Reporting Summary

Supplementary Tables 5–7

Table 5. Population genetics summary statistics calculated for Rpi-amr1 and Avramr1 homologues. Table 6. Evidence of sequence exchange between Rpi-amr1 orthologues and paralogues from SP2273 using 3SEQ. An exact non-parametric mosaicism statistic algorithm was implemented in 3SEQ; we found statistical evidence of recombination (the null hypothesis of clonal evolution was rejected). Table 7. Accession numbers of all sequencing data in this study.

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Witek, K., Lin, X., Karki, H.S. et al. A complex resistance locus in Solanum americanum recognizes a conserved Phytophthora effector. Nat. Plants 7, 198–208 (2021). https://doi.org/10.1038/s41477-021-00854-9

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