Host genetic determinants drive compartment-specific assembly of tea plant microbiomes.

Diverse host factors drive microbial variation in plant-associated environments, whereas their genetic mechanisms remain largely unexplored. To address this, we coupled the analyses of plant genetics and microbiomes in this study. Using 100 tea plant (Camellia sinensis) cultivars, the microbiomes of rhizosphere, root endosphere and phyllosphere showed clear compartment-specific assembly, whereas the subpopulation differentiation of tea cultivars exhibited small effects on microbial variation in each compartment. Through microbiome genome-wide association studies, we examined the interactions between tea genetic loci and microbial variation. Notably, genes related to the cell wall and carbon catabolism were heavily linked to root endosphere microbial composition, whereas genes related to the metabolism of metal ions and small organic molecules were overrepresented in association with rhizosphere microbial composition. Moreover, a set of tea genetic variants, including the cytoskeleton-related formin homology interacting protein 1 gene, were strongly associated with the β-diversity of phyllosphere microbiomes, implying their interactions with the overall structure of microbial communities. Our results create a catalogue of tea genetic determinants interacting with microbiomes and reveal the compartment-specific microbiome assembly driven by host genetics.