Are specific microbiota from the phyllosphere of American Vitis species involved to their resistance to downy mildew?

Abstract

The oomycete Plasmopara viticola (Berk. & M.A. Curtis) Berl. & De Toni, the causal agent of grapevine downy mildew, originated in the northeastern United States and was accidentally introduced into Europe in the mid-19th century. It has since caused major economic losses in viticulture worldwide. All it’s invasive populations outside the US belong to the narrow clade P. viticola f. sp. aestivalis, to which cultivated grapevine (Vitis vinifera L.) is highly susceptible. P. viticola f. sp. aestivalis naturally parasitizes two North American wild Vitisspecies, V. aestivalis and V. labrusca, whose accessions display variable levels of susceptibility but are consistently more resistant than V. vinifera. These species are therefore considered the original hosts of the P. viticola populations that have invaded worldwide vineyards. We hypothesized that a longer coevolutionary history between these wild hosts and the pathogen has led to the evolution of resistance genes in the plant genome, but also to the establishment of a specific foliar microbiota contributing to disease resistance.

During 2023, we sampled leaves from wild populations of V. labrusca and V. aestivalis along the eastern coast of the United States as well as repository-grown plants of V. vinifera, V. labrusca, V. aestivalis, and their interspecific hybrids in the USA and France. Leaves collected in USA were phenotyped for downy mildew resistance in a controlled experiment, and both epiphytic and whole-leaf microbiota were characterized for fungal and bacterial communities. In total, 329 leaf samples were collected, 122 from wild populations and 207 in repositories. A continuous gradient of susceptibility to downy mildew was observed across plant genotypes and environments, ranging from complete resistance to high susceptibility. Differential abundance and TITAN analyses revealed that resistant plants harbored higher relative abundances of specific taxa within their microbiota. In particular, basidiomycete yeasts, known as biocontrol agents, were consistently associated with resistance phenotypes in plants grown under repository conditions in the United States.

Ongoing analyses aim to determine whether these microbial associations are conserved in repository-grown plants in France. Genome-wide association analyses are currently underway to identify host loci influencing microbiota composition, particularly those involved in the recruitment of microorganisms associated with downy mildew resistance.