Rapid evolution of bacterial mutualism in the plant rhizosphere

Erqin Li; Ronnie de Jonge; Chen Liu; Henan Jiang; Ville-Petri Friman; Corné M J Pieterse; Peter A H M Bakker; Alexandre Jousset

doi:10.1038/s41467-021-24005-y

Rapid evolution of bacterial mutualism in the plant rhizosphere

Erqin Li
, Ronnie de Jonge
, Chen Liu
, Henan Jiang
, Ville-Petri Friman
, Corné M J Pieterse
, Peter A H M Bakker
, Alexandre Jousset

Research output: Contribution to journal › Article › Academic › peer-review

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.

Original language	English
Article number	3829
Pages (from-to)	1-13
Journal	Nature Communications
Volume	12
Issue number	1
DOIs	https://doi.org/10.1038/s41467-021-24005-y
Publication status	Published - Dec 2021

Bibliographical note

Funding Information:
We thank Roy van der Meijs for his excellent work on the scopoletin sensitivity assays and Ke Yu, Roeland Berendsen and members of the Plant-Microbe Interactions Lab for helpful discussions. This work was supported by a China Scholarship Council fellowship (to E.L.) and a postdoctoral fellowship of the Research Foundation Flanders (FWO 12B8116RN) (to R.d.J.). V.-P.F. is funded by the Royal Society (RSG\R1\180213 and CHL \R1\180031) and jointly by a grant from UKRI, Defra, and the Scottish Government, under the Strategic Priorities Fund Plant Bacterial Diseases programme (BB/T010606/1) at the University of York.

Publisher Copyright:
© 2021, The Author(s).

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s41467-021-24005-yFinal published version, 1.19 MBLicence: CC BY

Cite this

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title = "Rapid evolution of bacterial mutualism in the plant rhizosphere",

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.",

author = "Erqin Li and \{de Jonge\}, Ronnie and Chen Liu and Henan Jiang and Ville-Petri Friman and Pieterse, \{Corn{\'e} M J\} and Bakker, \{Peter A H M\} and Alexandre Jousset",

note = "Funding Information: We thank Roy van der Meijs for his excellent work on the scopoletin sensitivity assays and Ke Yu, Roeland Berendsen and members of the Plant-Microbe Interactions Lab for helpful discussions. This work was supported by a China Scholarship Council fellowship (to E.L.) and a postdoctoral fellowship of the Research Foundation Flanders (FWO 12B8116RN) (to R.d.J.). V.-P.F. is funded by the Royal Society (RSG\textbackslash{}R1\textbackslash{}180213 and CHL \textbackslash{}R1\textbackslash{}180031) and jointly by a grant from UKRI, Defra, and the Scottish Government, under the Strategic Priorities Fund Plant Bacterial Diseases programme (BB/T010606/1) at the University of York. Publisher Copyright: {\textcopyright} 2021, The Author(s).",

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AU - Pieterse, Corné M J

AU - Bakker, Peter A H M

AU - Jousset, Alexandre

N1 - Funding Information: We thank Roy van der Meijs for his excellent work on the scopoletin sensitivity assays and Ke Yu, Roeland Berendsen and members of the Plant-Microbe Interactions Lab for helpful discussions. This work was supported by a China Scholarship Council fellowship (to E.L.) and a postdoctoral fellowship of the Research Foundation Flanders (FWO 12B8116RN) (to R.d.J.). V.-P.F. is funded by the Royal Society (RSG\R1\180213 and CHL \R1\180031) and jointly by a grant from UKRI, Defra, and the Scottish Government, under the Strategic Priorities Fund Plant Bacterial Diseases programme (BB/T010606/1) at the University of York. Publisher Copyright: © 2021, The Author(s).

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N2 - 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.

AB - 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.

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Rapid evolution of bacterial mutualism in the plant rhizosphere

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