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A root pathogen drives rhizosphere enrichment of antagonistic Pseudomonas and induces production of an antimicrobial metabolite

Abstract

In plants, the development of soil-borne diseases has been shown to trigger the recruitment of beneficial microbes, which contribute to defense against pathogens. However, the underlying mechanisms driving this recruitment remain elusive. Here, we used a gnotobiotic system combined with a synthetic bacterial community (SynCom) derived from the Medicago truncatula rhizosphere to dissect microbiota pathogen interaction and its role in the development of root rot caused by Aphanomyces euteiches, a devastating soilborne oomycete pathogen of legumes. Through integrated metabarcoding, metabolomics and transcriptomics, we reveal that pathogen infection restructures the bacterial SynCom, selectively enriching the microbial community with specific Pseudomonas spp. strains displaying anti A. euteiches activity. This shift alleviates root rot symptoms, triggers the biosynthesis of the antibiotic 2,4-diacetylphloroglucinol (DAPG), a Pseudomonas specialized metabolite inhibiting A. euteiches growth, and amplifies the plant endogenous isoflavonoid defense responses. Unexpectedly, we found that A. euteiches directly activates DAPG production in beneficial bacteria independently of the plant, through the production of a heat-stable, high-molecular-weight (30 - 100 kDa) extracellular components. These findings uncover a novel mechanism whereby a pathogen inadvertently activates antibiotic production in beneficial bacteria, extending the plant immune system. Our research underscores the critical role of microbial interactions in the rhizosphere in determining root disease outcomes, paving the way for microbiome-based strategies to combat root diseases.

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BibTeX
@misc{zouaoui2026root,
  title = {{A root pathogen drives rhizosphere enrichment of antagonistic Pseudomonas and induces production of an antimicrobial metabolite}},
  author = {Mohamed Zouaoui and Marie Solau and Aurélien Amiel and Alice Penrose and Jean Belleville and Quentin Bazerque and Sylvie Fournier and Amélie Perez and Laurent Camborde and Elodie Gaulin and Thomas Rey and Bernard Dumas},
  howpublished = {HAL},
  year = {2026},
  month = aug,
  doi = {10.64898/2026.08.26.747274},
  url = {https://hal.science/hal-05760234v1},
  note = {CC BY-NC-ND},
}
RIS
TY  - UNPB
TI  - A root pathogen drives rhizosphere enrichment of antagonistic Pseudomonas and induces production of an antimicrobial metabolite
AU  - Mohamed Zouaoui
AU  - Marie Solau
AU  - Aurélien Amiel
AU  - Alice Penrose
AU  - Jean Belleville
AU  - Quentin Bazerque
AU  - Sylvie Fournier
AU  - Amélie Perez
AU  - Laurent Camborde
AU  - Elodie Gaulin
AU  - Thomas Rey
AU  - Bernard Dumas
PY  - 2026
DA  - 2026/08/26
PB  - HAL
DO  - 10.64898/2026.08.26.747274
UR  - https://hal.science/hal-05760234v1
AB  - In plants, the development of soil-borne diseases has been shown to trigger the recruitment of beneficial microbes, which contribute to defense against pathogens. However, the underlying mechanisms driving this recruitment remain elusive. Here, we used a gnotobiotic system combined with a synthetic bacterial community (SynCom) derived from the Medicago truncatula rhizosphere to dissect microbiota pathogen interaction and its role in the development of root rot caused by Aphanomyces euteiches, a devastating soilborne oomycete pathogen of legumes. Through integrated metabarcoding, metabolomics and transcriptomics, we reveal that pathogen infection restructures the bacterial SynCom, selectively enriching the microbial community with specific Pseudomonas spp. strains displaying anti A. euteiches activity. This shift alleviates root rot symptoms, triggers the biosynthesis of the antibiotic 2,4-diacetylphloroglucinol (DAPG), a Pseudomonas specialized metabolite inhibiting A. euteiches growth, and amplifies the plant endogenous isoflavonoid defense responses. Unexpectedly, we found that A. euteiches directly activates DAPG production in beneficial bacteria independently of the plant, through the production of a heat-stable, high-molecular-weight (30 - 100 kDa) extracellular components. These findings uncover a novel mechanism whereby a pathogen inadvertently activates antibiotic production in beneficial bacteria, extending the plant immune system. Our research underscores the critical role of microbial interactions in the rhizosphere in determining root disease outcomes, paving the way for microbiome-based strategies to combat root diseases.
ER  -