Spatio-temporal control of mutualism in legumes helps spread symbiotic nitrogen fixation

  1. Benoit Daubech
  2. Philippe Remigi
  3. Ginaini Doin de Moura
  4. Marta Marchetti
  5. Cécile Pouzet
  6. Marie-Christine Auriac
  7. Chaitanya S Gokhale
  8. Catherine Masson-Boivin  Is a corresponding author
  9. Delphine Capela
  1. Université de Toulouse, France
  2. Massey University, New Zealand
  3. Fédération de Recherches Agrobiosciences, Interactions, Biodiversity, France
  4. Max Planck Institute for Evolutionary Biology, Germany

Abstract

Mutualism is of fundamental importance in ecosystems. Which factors help to keep the relationship mutually beneficial and evolutionarily successful is a central question. We addressed this issue for one of the most significant mutualistic interactions on Earth, which associates plants of the leguminosae family and hundreds of nitrogen (N2)-fixing bacterial species. Here we analyze the spatio-temporal dynamics of fixers and non-fixers along the symbiotic process in the Cupriavidus taiwanensis-Mimosa pudica system. N2-fixing symbionts progressively outcompete isogenic non-fixers within root nodules, where N2-fixation occurs, even when they share the same nodule. Numerical simulations, supported by experimental validation, predict that rare fixers will invade a population dominated by non-fixing bacteria during serial nodulation cycles with a probability that is function of initial inoculum, plant population size and nodulation cycle length. Our findings provide insights into the selective forces and ecological factors that may have driven the spread of the N2-fixation mutualistic trait.

Article and author information

Author details

  1. Benoit Daubech

    LIPM, Université de Toulouse, Castanet-Tolosan, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Philippe Remigi

    New Zealand Institute for Advanced Study, Massey University, Auckland, New Zealand
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9023-3788
  3. Ginaini Doin de Moura

    LIPM, Université de Toulouse, Castanet-Tolosan, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Marta Marchetti

    LIPM, Université de Toulouse, Castanet-Tolosan, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Cécile Pouzet

    Plateforme d'Imagerie TRI, Fédération de Recherches Agrobiosciences, Interactions, Biodiversity, Castanet-Tolosan, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Marie-Christine Auriac

    LIPM, Université de Toulouse, Castanet-Tolosan, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Chaitanya S Gokhale

    Research Group for Evolutionary Theory, Max Planck Institute for Evolutionary Biology, Ploen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5749-3665
  8. Catherine Masson-Boivin

    LIPM, Université de Toulouse, Castanet-Tolosan, France
    For correspondence
    catherine.masson@inra.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3506-3808
  9. Delphine Capela

    LIPM, Université de Toulouse, Castanet-Tolosan, France
    Competing interests
    The authors declare that no competing interests exist.

Funding

Agence Nationale de la Recherche (ANR-12-ADAP-0014-01)

  • Marta Marchetti
  • Catherine Masson-Boivin
  • Delphine Capela

Institut National de la Recherche Agronomique

  • Benoit Daubech

Max Planck society

  • Chaitanya S Gokhale

Agence Nationale de la Recherche (ANR-16-CE20-0011-01)

  • Marta Marchetti
  • Catherine Masson-Boivin
  • Delphine Capela

Agence Nationale de la Recherche (ANR-10-LABX-41)

  • Benoit Daubech
  • Marta Marchetti
  • Cécile Pouzet
  • Marie-Christine Auriac
  • Catherine Masson-Boivin
  • Delphine Capela

Agence Nationale de la Recherche (ANR-11-IDEX-0002-02)

  • Benoit Daubech
  • Marta Marchetti
  • Cécile Pouzet
  • Marie-Christine Auriac
  • Catherine Masson-Boivin
  • Delphine Capela

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

Copyright

© 2017, Daubech 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. Benoit Daubech
  2. Philippe Remigi
  3. Ginaini Doin de Moura
  4. Marta Marchetti
  5. Cécile Pouzet
  6. Marie-Christine Auriac
  7. Chaitanya S Gokhale
  8. Catherine Masson-Boivin
  9. Delphine Capela
(2017)
Spatio-temporal control of mutualism in legumes helps spread symbiotic nitrogen fixation
eLife 6:e28683.
https://doi.org/10.7554/eLife.28683

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https://doi.org/10.7554/eLife.28683