Rapid evolution of bacterial mutualism in the plant rhizosphere

Erqin Li, Ronnie Jonge (), Chen Liu, Henan Jiang, Ville-Petri Friman (), Corné M. J. Pieterse, Peter A. H. M. Bakker and Alexandre Jousset ()
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Erqin Li: Plant-Microbe Interactions
Ronnie Jonge: Plant-Microbe Interactions
Chen Liu: Plant-Microbe Interactions
Henan Jiang: Plant-Microbe Interactions
Ville-Petri Friman: Department of Biology
Corné M. J. Pieterse: Plant-Microbe Interactions
Peter A. H. M. Bakker: Plant-Microbe Interactions
Alexandre Jousset: Department of Biology, Ecology and Biodiversity

Nature Communications, 2021, vol. 12, issue 1, 1-13

Abstract: Abstract While beneficial plant-microbe interactions are common in nature, direct evidence for the evolution of bacterial mutualism is scarce. Here we use experimental evolution to causally show that initially plant-antagonistic Pseudomonas protegens bacteria evolve into mutualists in the rhizosphere of Arabidopsis thaliana within six plant growth cycles (6 months). This evolutionary transition is accompanied with increased mutualist fitness via two mechanisms: (i) improved competitiveness for root exudates and (ii) enhanced tolerance to the plant-secreted antimicrobial scopoletin whose production is regulated by transcription factor MYB72. Crucially, these mutualistic adaptations are coupled with reduced phytotoxicity, enhanced transcription of MYB72 in roots, and a positive effect on plant growth. Genetically, mutualism is associated with diverse mutations in the GacS/GacA two-component regulator system, which confers high fitness benefits only in the presence of plants. Together, our results show that rhizosphere bacteria can rapidly evolve along the parasitism-mutualism continuum at an agriculturally relevant evolutionary timescale.

Date: 2021
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DOI: 10.1038/s41467-021-24005-y

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