Diversity and functional features of the root-associated bacteriome are dependent on grapevine susceptibility to Plasmopara viticola.

Background: Plant health depends on beneficial interactions between the roots and their microbiomes. Despite recent progress on the role of the grapevine microbiome, the taxonomic identity and functional traits of microbial taxa specific to healthy or Plasmopara viticola-diseased plants, as well as to the susceptible or resistant cultivar are unknown. Using metabarcoding and shotgun metagenomics sequencing, we investigated the effect of downy mildew on the root-associated microbiome (rhizospheric soil, rhizoplane and endosphere) of 41B-grafted susceptible cultivar (Chardonnay) and resistant interspecific hybrid (Voltis) at flowering and veraison stages. The impact of conventional treatment on the rhizomicrobiome assembly of Chardonnay was also evaluated.

Results: Analyses revealed a core bacteriome shared between both susceptible and resistant cultivars. This also highlighted common functional traits between the rhizosphere and rhizoplane bacteriomes in both cultivars. A dysbiosis state was also evidenced by a loss of beneficial communities in the rhizosphere of the P. viticola-infected cultivar. Microbial genome assemblies showed functional differences between healthy and diseased plants, with a loss of Pseudomonas and Phyllobacterium taxa at veraison. This state was mainly characterized by a loss of genes involved in polyamine transport and metabolism in the susceptible cultivar. It was also marked by an increase in population evenness and total bacterial diversity, and the presence of pathogenic species in susceptible plants.

Conclusions: This study reveals distinct and overlapping bacterial communities and functional genes in the rhizospheric soil, rhizoplane and root endosphere of both susceptible and resistant grapevine cultivars to downy mildew. Microbial diversity and abundant taxa of grapevine roots are influenced by downy mildew and cultivar susceptibility. Common bacterial functions are shared among rhizocompartments of susceptible and resistant cultivars, revealing a dysbiosis state and functional signatures related to plant immunity, especially in the infected-susceptible plants.