Anthracnose drives assembly of phyllosphere epiphytic bacterial communities to increase disease resistance

The phyllosphere microbiome plays crucial roles in plant health, but evidence of 'cry for help' strategy in the face of pathogen attack in the phyllosphere remains limited, particularly for the microbiomes of distinct leaf ecological niches. We investigated whether foliar pathogen anthracnose (Colletotrichum lentis) influenced the assembly and functions of microbiomes in epiphytic and endophytic niches of the phyllosphere of common vetch (Vicia sativa) leaves. We also evaluated synthetic microbial communities (SynComs), including representatives of disease-associated strains, for pathogen protection. Anthracnose mediated the deterministic assembly process of epiphytic bacterial and endophytic fungal communities, and increased the complexity of bacterial co-occurrence networks. Iron competition and antifungal genes were also enriched in the epiphytic bacteria, which produce siderophores and degrade fungal cell walls to counteract pathogens. SynComs of beneficial epiphytic bacteria partially protect hosts by regulating bacterial interactions and inducing host immune responses. These findings suggest that disease drives the deterministic assembly of distinct phyllosphere microbiomes, their diversity and their function. Moreover, SynComs from the epiphytic niche can confer host plant disease resistance.