Asymmetrical diversification of the receptor-ligand interaction controlling self-incompatibility in Arabidopsis

Abstract

How two-component genetic systems accumulate evolutionary novelty and diversify in the course of evolution is a fundamental problem in evolutionary systems biology. In the Brassicaceae, self-incompatibility (SI) is a spectacular example of a diversified allelic series in which numerous highly diverged receptor-ligand combinations are segregating in natural populations. However, the evolutionary mechanisms by which new SI specificities arise have remained elusive. Using in planta ancestral protein reconstruction, we demonstrate that two allelic variants segregating as distinct receptor-ligand combinations diverged through an asymmetrical process whereby one variant has retained the same recognition specificity as their (now extinct) putative ancestor, while the other has functionally diverged and now represents a novel specificity no longer recognized by the ancestor. Examination of the structural determinants of the shift in binding specificity suggests that qualitative rather than quantitative changes of the interaction are an important source of evolutionary novelty in this highly diversified receptor-ligand system.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Maxime Chantreau

    UMR 8198-Evo-Eco-Paléo, CNRS, Université de Lille, Villeneuve d'Ascq, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2844-1989
  2. Céline Poux

    UMR 8198-Evo-Eco-Paléo, CNRS, Université de Lille, Villeneuve d'Ascq, France
    For correspondence
    Celine.Poux@univ-lille1.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9379-2769
  3. Marc F Lensink

    UMR 8576 UGSF, CNRS, Université de Lille, Villeneuve d'Ascq, France
    For correspondence
    marc.lensink@univ-lille.fr
    Competing interests
    The authors declare that no competing interests exist.
  4. Guillaume Brysbaert

    UMR 8576 UGSF, CNRS, Université de Lille, Villeneuve d'Ascq, France
    For correspondence
    guillaume.brysbaert@univ-lille1.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6807-6621
  5. Xavier Vekemans

    UMR 8198-Evo-Eco-Paléo, CNRS, Université de Lille, Villeneuve d'Ascq, France
    For correspondence
    Xavier.Vekemans@univ-lille.fr
    Competing interests
    The authors declare that no competing interests exist.
  6. Vincent Castric

    UMR 8198-Evo-Eco-Paléo, CNRS, Université de Lille, Villeneuve d'Ascq, France
    For correspondence
    vincent.castric@univ-lille.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4461-4915

Funding

H2020 European Research Council (Novel project grant #648321)

  • Vincent Castric

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

Copyright

© 2019, Chantreau 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. Maxime Chantreau
  2. Céline Poux
  3. Marc F Lensink
  4. Guillaume Brysbaert
  5. Xavier Vekemans
  6. Vincent Castric
(2019)
Asymmetrical diversification of the receptor-ligand interaction controlling self-incompatibility in Arabidopsis
eLife 8:e50253.
https://doi.org/10.7554/eLife.50253

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https://doi.org/10.7554/eLife.50253

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