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Rapid evolution of bacterial mutualism in the plant rhizosphere

114 Citations2021
Erqin Li, Ronnie de Jonge, Chen Liu

Experimental evolution is used 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), accompanied with increased mutualist fitness via two mechanisms.

Abstract

<jats:title>Abstract</jats:title> <jats:p> 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 <jats:italic>Pseudomonas protegens</jats:italic> bacteria evolve into mutualists in the rhizosphere of <jats:italic>Arabidopsis thaliana</jats:italic> 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 <jats:italic>MYB72</jats:italic> . Crucially, these mutualistic adaptations are coupled with reduced phytotoxicity, enhanced transcription of <jats:italic>MYB72</jats:italic> 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. </jats:p>