Letter | Published:

The long-term maintenance of a resistance polymorphism through diffuse interactions

Nature volume 512, pages 436440 (28 August 2014) | Download Citation

Abstract

Plant resistance (R) genes are a crucial component in plant defence against pathogens1. Although R genes often fail to provide durable resistance in an agricultural context, they frequently persist as long-lived balanced polymorphisms in nature2,3,4. Standard theory explains the maintenance of such polymorphisms through a balance of the costs and benefits of resistance and virulence in a tightly coevolving host–pathogen pair5,6. However, many plant–pathogen interactions lack such specificity7. Whether, and how, balanced polymorphisms are maintained in diffusely interacting species8 is unknown. Here we identify a naturally interacting R gene and effector pair in Arabidopsis thaliana and its facultative plant pathogen, Pseudomonas syringae. The protein encoded by the R gene RPS5 recognizes an AvrPphB homologue (AvrPphB2) and exhibits a balanced polymorphism that has been maintained for over 2 million years (ref. 3). Consistent with the presence of an ancient balanced polymorphism, the R gene confers a benefit when plants are infected with P. syringae carrying avrPphB2 but also incurs a large cost in the absence of infection. RPS5 alleles are maintained at intermediate frequencies in populations globally, suggesting ubiquitous selection for resistance. However, the presence of P. syringae carrying avrPphB is probably insufficient to explain the RPS5 polymorphism. First, avrPphB homologues occur at very low frequencies in P. syringae populations on A. thaliana. Second, AvrPphB only rarely confers a virulence benefit to P. syringae on A. thaliana. Instead, we find evidence that selection for RPS5 involves multiple non-homologous effectors and multiple pathogen species. These results and an associated model suggest that the R gene polymorphism in A. thaliana may not be maintained through a tightly coupled interaction involving a single coevolved R gene and effector pair. More likely, the stable polymorphism is maintained through complex and diffuse community-wide interactions.

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Acknowledgements

We thank G. Dwyer, M. Kreitman, L. Merwin, C. Morris and M. Nordborg for discussions, D. Baltrus, D. Dahlbeck, J. Greenberg and B. Vinatzer for supplying plasmids, N. Faure for help collecting the French isolates of P. syringae, C. Godé, J. Higgins and A. Stathos for contributions to genotyping RPS5 presence/absence, G. Sperone for mapping, and T. Morton and the staff of the University of Chicago greenhouse for planting and maintaining A. thaliana. T.L.K. was supported by a Department of Education GAANN fellowship, J.M.K. and L.G.B. were supported by postdoctoral fellowships from the Dropkin Foundation, and R.L. was supported by a National Institutes of Health (NIH) Postbaccalaureate Research Education Program award. F.R. was supported by the Laboratory of Excellence (Labex) TULIP (ANR-10-LABX-41; ANR-11-IDEX-0002-02). This work was supported by grants NIH-NIGMS R01 GM046451 to R.W.I., and grants NSF MCB0603515, NIH-NIGMS R01 GM057994 and NIH-NIGMS R01 GM083068 to J.B.

Author information

Author notes

    • Talia L. Karasov
    •  & Joel M. Kniskern

    These authors contributed equally to this work.

    • Joel M. Kniskern
    • , Jing Ding
    •  & Luke G. Barrett

    Present addresses: Monsanto Vegetable Seeds, 37437 State Highway 16, Woodland, California 95695, USA (J.M.K.); State Key Laboratory of Plant Genetics and Germplasm Enhancement and College of Horticulture, Nanjing Agricultural University, Nanjing, China (J.D.); CSIRO Plant Industry, GPO Box 1600, Canberra, ACT 2601, Australia (L.G.B.).

Affiliations

  1. Department of Ecology and Evolution, University of Chicago, Chicago, Illinois 60637, USA

    • Talia L. Karasov
    • , Joel M. Kniskern
    • , Liping Gao
    • , Jing Ding
    • , Ruben O. Lastra
    • , Sumitha Nallu
    • , Luke G. Barrett
    • , Richard R. Hudson
    •  & Joy Bergelson
  2. Committee on Genetics Genomics and Systems Biology, University of Chicago, Chicago, Illinois 60637, USA

    • Talia L. Karasov
  3. Department of Biology, Indiana University, Bloomington, Indiana 47405, USA

    • Brody J. DeYoung
    • , Ullrich Dubiella
    •  & Roger W. Innes
  4. INRA, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR441, F-31326 Castanet-Tolosan, France

    • Fabrice Roux
  5. CNRS, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR2594, F-31326 Castanet-Tolosan, France

    • Fabrice Roux
  6. Laboratoire Génétique et Evolution des Populations Végétales, UMR CNRS 8198, Université des Sciences et Technologies de Lille – Lille 1, F-59655 Villeneuve d’Ascq Cedex, France

    • Fabrice Roux

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Contributions

J.B. conceived the project and organized components; J.M.K. and R.L. cloned AvrPphB2 and performed functional analyses, J.M.K. mapped and cloned RPS5; L.G. performed fitness trials; B.J.D. and U.D. performed effector biochemical analyses; T.L.K. performed sequence divergence analyses; J.M.K., F.R. and J.D. assayed RPS5 frequencies in A. thaliana; J.M.K., S.N. and T.L.K. performed P. syringae fitness assays; T.L.K. cloned AvrPphB homologues; T.L.K. and R.R.H. designed the population genetics analyses and R.W.I. designed the biochemical analyses; T.L.K. performed the modelling; J.B., L.B., T.L.K. and J.M.K. were involved in the study design, the experiments and the analyses; T.L.K. and J.B. wrote the manuscript. All authors discussed the results and commented on the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Joy Bergelson.

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    Supplementary Information

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DOI

https://doi.org/10.1038/nature13439

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