Revealing microbial consortia that interfere with grapevine downy mildew through microbiome epidemiology

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Fournier, Paola | Pellan, Lucile | Jaswa, Aarti | Cambon, Marine, C. | Chataigner, Alexandre | Bonnard, Olivier | Raynal, Marc | Debord, Christian | Poeydebat, Charlotte | Labarthe, Simon | Delmotte, François | This, Patrice | Vacher, Corinne

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Availability of data and materials: The raw sequence data obtained from Illumina and PacBio sequencing were deposited in the European Nucleotide Archive (ENA) under the project numbers PRJEB79310 and PRJEB79661, respectively. The raw sequence data obtained from Sanger sequencing were deposited in the National Center for Biotechnology Information (NCBI) under the Accession Numbers PQ348104—PQ348540 for bacteria and PQ350423—PQ350897 for fungi and yeasts. The filtered and assembled sequence data, the metadata, and the scripts for bioinformatic and statistical analyses are available on Recherche Data Gouv under the DOI [https://doi.org/https://doi.org/10.57745/XNEH5O].. International audience. Background: Plant and soil microbiomes can interfere with pathogen life cycles, but their influence on disease epidemiology remains understudied. Here, we analyzed the relationships between plant and soil microbiomes and longterm epidemiological records of grapevine downy mildew, a major disease caused by the oomycete Plasmopara viticola. Results: We found that certain microbial taxa were consistently more abundant in plots with lower disease incidence and severity and that the microbial community composition could predict disease incidence and severity. Microbial diversity was not strongly linked to epidemiological records, suggesting that disease incidence and severity is more related to the abundance of specific microbial taxa. These key taxa were identified in the topsoil, where the pathogen's oospores overwinter, and in the phyllosphere, where zoospores infect leaves. By contrast, the leaf endosphere, where the pathogen's mycelium develops, contained few taxa of interest. Surprisingly, the soil microbiota was a better predictor of disease incidence and severity than the leaf microbiota, suggesting that the soil microbiome could be a key indicator of the dynamics of this primarily aerial disease. Conclusion: Our study integrates long-term epidemiological data with microbiome profiles of healthy plants to reveal fungi and bacteria relevant for the biocontrol of grapevine downy mildew. The resulting database provides a valuable resource for designing microbial consortia with potential biocontrol activity. The framework can be applied to other crop systems to guide the development of biocontrol strategies and reduce pesticide use in agriculture.

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