Rapid evolution of bacterial mutualism in the plant rhizosphere  

Li et al., 2021

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.

Panel a shows the initially antagonistic effect of Pseudomonas protegens CHA0 on A. thaliana after one plant growth cycle in the sterile sand study system (n = 5; aboveground biomass ***P = 0.0001). Panels b–f compare the effects of ancestral and evolved Pseudomonas protegens CHA0 phenotypes on plant performance-related traits in a separate plant growth assays performed on agar plates at the end of the selection experiment (n = 3 for control and n = 5 for each evolved phenotype). Different panels show the shoot biomass in grams (b), root biomass in grams (c), number of lateral roots (d), root length in cm (e), and the amount of plant ‘greenness’ in terms of green-to-white pixel ratio (f) after 14 days of bacterial inoculation. Bacterial phenotype groups are displayed in different colours (black: ancestor; dark grey: ancestral-like; light grey: transient; orange: stress-sensitive, light green: mutualist 1 and dark green: mutualist 2) and were classified and named based on K-means clustering using 14 phenotypic traits linked to growth, stress tolerance, production of bioactive compounds and antimicrobial activity. All boxplots show median (centre line), interquartile range (25–75%) and whiskers that extend 1.5 times the interquartile range overlaid with a scatter plot showing independent replicates. Statistical testing in all panels was carried out using one-way ANOVA, and asterisks above plots indicate significant differences between control and bacteria-treated plants (*P = 0.05, **P = 0.01, ***P = 0.001; n.s. = non-significant). Data for all panels are provided in the Source Data file.

https://www.nature.com/articles/s41467-021-24005-y

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