Long-term balancing selection drives evolution of immunity genes in Capsella

  1. Daniel Koenig  Is a corresponding author
  2. Jörg Hagmann
  3. Rachel Li
  4. Felix Bemm
  5. Tanja Slotte
  6. Barbara Nueffer
  7. Stephen I Wright
  8. Detlef Weigel  Is a corresponding author
  1. Max Planck Institute for Developmental Biology, Germany
  2. Stockholm University, Sweden
  3. University of Osnabrück, Germany

Abstract

Genetic drift is expected to remove polymorphism from populations over long periods of time, with the rate of polymorphism loss being accelerated when species experience strong reductions in population size. Adaptive forces that maintain genetic variation in populations, or balancing selection, might counteract this process. To understand the extent to which natural selection can drive the retention of genetic diversity, we document genomic variability after two parallel species-wide bottlenecks in the genus Capsella. We find that ancestral variation preferentially persists at immunity related loci, and that the same collection of alleles has been maintained in different lineages that have been separated for several million years. By reconstructing the evolution of the disease related locus MLO2b, we find that divergence between ancient haplotypes can be obscured by referenced based re-sequencing methods, and that trans-specific alleles can encode substantially diverged protein sequences. Our data point to long term balancing selection as an important factor shaping the genetics of immune systems in plants and as the predominant driver of genomic variability after a population bottleneck.

Data availability

All raw sequencing data are depsoited under the accession codes PRJEB6689.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Daniel Koenig

    Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany
    For correspondence
    dkoenig@ucr.edu
    Competing interests
    No competing interests declared.
  2. Jörg Hagmann

    Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    No competing interests declared.
  3. Rachel Li

    Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8112-4237
  4. Felix Bemm

    Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    No competing interests declared.
  5. Tanja Slotte

    Department of Ecology, Environment, and Plant Sciences, Stockholm University, Stockholm, Sweden
    Competing interests
    No competing interests declared.
  6. Barbara Nueffer

    Department of Biology, University of Osnabrück, Osnabrück, Germany
    Competing interests
    No competing interests declared.
  7. Stephen I Wright

    Department of Biology, University of Osnabrück, Osnabrück, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9973-9697
  8. Detlef Weigel

    Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany
    For correspondence
    weigel@tue.mpg.de
    Competing interests
    Detlef Weigel, Deputy editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2114-7963

Funding

European Research Council (IMMUNEMESIS)

  • Detlef Weigel

Human Frontier Science Program (LT000783/2010-L)

  • Daniel Koenig

Deutsche Forschungsgemeinschaft (WE 2897/4-2)

  • Detlef Weigel

Max-Planck-Gesellschaft (Open-access funding)

  • Detlef Weigel

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Molly Przeworski, Columbia University, United States

Version history

  1. Received: November 13, 2018
  2. Accepted: February 26, 2019
  3. Accepted Manuscript published: February 26, 2019 (version 1)
  4. Version of Record published: March 20, 2019 (version 2)
  5. Version of Record updated: April 29, 2019 (version 3)

Copyright

© 2019, Koenig et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Daniel Koenig
  2. Jörg Hagmann
  3. Rachel Li
  4. Felix Bemm
  5. Tanja Slotte
  6. Barbara Nueffer
  7. Stephen I Wright
  8. Detlef Weigel
(2019)
Long-term balancing selection drives evolution of immunity genes in Capsella
eLife 8:e43606.
https://doi.org/10.7554/eLife.43606

Share this article

https://doi.org/10.7554/eLife.43606

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