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Nature. 2014 Aug 28;512(7515):436-440. doi: 10.1038/nature13439. Epub 2014 Jul 6.

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

Author information

1
Department of Ecology and Evolution, University of Chicago, Chicago, Illinois 60637, USA.
2
Committee on Genetics Genomics and Systems Biology, University of Chicago, Chicago, Illinois 60637, USA.
3
Department of Biology, Indiana University, Bloomington, Indiana 47405, USA.
4
INRA, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR441, F-31326 Castanet-Tolosan, France.
5
CNRS, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR2594, F-31326 Castanet-Tolosan, France.
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.
#
Contributed equally

Abstract

Plant resistance (R) genes are a crucial component in plant defence against pathogens. Although R genes often fail to provide durable resistance in an agricultural context, they frequently persist as long-lived balanced polymorphisms in nature. 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 pair. However, many plant-pathogen interactions lack such specificity. Whether, and how, balanced polymorphisms are maintained in diffusely interacting species 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.

PMID:
25043057
PMCID:
PMC4696508
DOI:
10.1038/nature13439
[Indexed for MEDLINE]
Free PMC Article

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