MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health
By Ioannis A. Stringlis, K. Yu, Kirstin Feussner, R. de Jonge, Sietske van Bentum, M. V. Van Verk, R. Berendsen, P. Bakker, I. Feussner, C. Pieterse. Proceedings of the National Academy of Sciences of the United States of America, 2018
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Significance Plant roots nurture a large diversity of soil microbes via exudation of chemical compounds into the rhizosphere. In turn, beneficial root microbiota promote plant growth and immunity. The root-specific transcription factor MYB72 has emerged as a central regulator in this process. Here, we show that MYB72 regulates the excretion of the coumarin scopoletin, an iron-mobilizing phenolic compound with selective antimicrobial activity that shapes the root-associated microbial community. Selected soil-borne fungal pathogens appeared to be highly sensitive to the antimicrobial activity of scopoletin, while two MYB72-inducing beneficial rhizobacteria were tolerant. Our results suggest that probiotic root-associated microbes that activate the iron-deficiency response during colonization stimulate MYB72-dependent excretion of scopoletin, thereby potentially improving their niche establishment and enhancing plant growth and protection. Plant roots nurture a tremendous diversity of microbes via exudation of photosynthetically fixed carbon sources. In turn, probiotic members of the root microbiome promote plant growth and protect the host plant against pathogens and pests. In the Arabidopsis thaliana–Pseudomonas simiae WCS417 model system the root-specific transcription factor MYB72 and the MYB72-controlled β-glucosidase BGLU42 emerged as important regulators of beneficial rhizobacteria-induced systemic resistance (ISR) and iron-uptake responses. MYB72 regulates the biosynthesis of iron-mobilizing fluorescent phenolic compounds, after which BGLU42 activity is required for their excretion into the rhizosphere. Metabolite fingerprinting revealed the antimicrobial coumarin scopoletin as a dominant metabolite that is produced in the roots and excreted into the rhizosphere in a MYB72- and BGLU42-dependent manner. Shotgun-metagenome sequencing of root-associated microbiota of Col-0, myb72, and the scopoletin biosynthesis mutant f6′h1 showed that scopoletin selectively impacts the assembly of the microbial community in the rhizosphere. We show that scopoletin selectively inhibits the soil-borne fungal pathogens Fusarium oxysporum and Verticillium dahliae, while the growth-promoting and ISR-inducing rhizobacteria P. simiae WCS417 and Pseudomonas capeferrum WCS358 are highly tolerant of the antimicrobial effect of scopoletin. Collectively, our results demonstrate a role for coumarins in microbiome assembly and point to a scenario in which plants and probiotic rhizobacteria join forces to trigger MYB72/BGLU42-dependent scopolin production and scopoletin excretion, resulting in improved niche establishment for the microbial partner and growth and immunity benefits for the host plant.
Subfields: Molecular Biology, Plant Science
View Paper: https://www.semanticscholar.org/paper/b3d987cfdbeee7dca25c29823960229e8d526cdc
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Citations in the corpus
- A specialized metabolic network selectively modulates Arabidopsis root microbiota (2019, background): “Plants are estimated to utilize ~20% of their photosynthesized carbon to make root-derived organic molecules, stimulating the formation of distinctive root microbiota from surrounding soil (5-8).”
- Rhizosphere Engineering With Plant Growth-Promoting Microorganisms for Agriculture and Ecological Sustainability (2021, background): “Rhizobacteria mediated ISR induction in plants stimulates the release of some antimicrobial components such as benzoxazinoids and coumarin, which further increase the induction of ISR triggering strains (Hu et al., 2018; Stringlis et al., 2018).”
- The effect of microbial inoculant origin on the rhizosphere bacterial community composition and plant growth-promotion (2020, background): “…evolved an intimate association with their soil microbiome (Vezzani et al. 2018), which can confer various benefits to the plants such as suppression of bacterial and fungal diseases, promotion of plant growth and assimilation of important nutrient (Berendsen et al. 2012; Stringlis et al. 2018).”
- Climate change impacts on plant pathogens, food security and paths forward (2023, positive): “For example, when exposed to soil-borne pathogens, the root-specific transcription factor MYB72 and the β -glucosidase BGLU42 regulate the synthesis and secretion of a coumarin molecule that inhibits pathogens but favours rhizobacteria, which induce systemic resistance 109 .”