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

Author:

Daubech Benoit1,Remigi Philippe2ORCID,Doin de Moura Ginaini1,Marchetti Marta1,Pouzet Cécile3,Auriac Marie-Christine13,Gokhale Chaitanya S4ORCID,Masson-Boivin Catherine1ORCID,Capela Delphine1

Affiliation:

1. The Laboratory of Plant-Microbe Interactions, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France

2. New Zealand Institute for Advanced Study, Massey University, Auckland, New Zealand

3. Fédération de Recherches Agrobiosciences, Interactions et Biodiversité, Plateforme d’Imagerie TRI, CNRS - UPS, Castanet-Tolosan, France

4. Research Group for Theoretical Models of Eco-evolutionary Dynamics, Department of Evolutionary Theory, Max Planck Institute for Evolutionary Biology, Plön, 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.

Funder

Agence Nationale de la Recherche

Institut National de la Recherche Agronomique

Max-Planck-Gesellschaft

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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