Differential contributions of an antimicrobial effector from Verticillium dahliae to virulence and tomato microbiota assembly across natural soils

Abstract Background Throughout their life cycle, plants associate with diverse and complex microbial communities collectively known as their microbiota. These microbiota contribute to plant performance and health by enhancing nutrient acquisition, modulating immunity, and providing a microbial barrier against pathogens. To successfully colonize their hosts, pathogens must overcome not only plant immune defenses but also this microbial barrier. For example, the soil-borne fungal pathogen Verticillium dahliae secretes the antimicrobial effector Ave1 to suppress antagonistic microbes and facilitate infection. Although many plant pathogens, including V. dahliae , inhabit both plant-associated and soil environments, how antimicrobial effectors contribute to pathogen establishment across these diverse ecological contexts remains poorly understood. Results To explore this question, we assembled a collection of natural soils differing in physicochemical properties and microbiota composition. Using three host plant species—barley, tomato, and cotton—we found that root-associated bacterial and fungal communities were primarily shaped by type of soil, whereas phyllosphere microbiota were mainly determined by plant species identity. On tomato, we further observed that the effector Ave1 differentially contributed to V. dahliae virulence depending on the soil of origin. While Ave1 consistently altered tomato-associated microbiota across all soils tested, the specific microbial taxa affected varied between soils. Conclusions Our findings demonstrate that the impact of the antimicrobial effector Ave1 on microbiota composition and pathogen virulence is context-dependent, influenced by the specific soil-derived microbial community that assembles on the host. This work highlights the ecological complexity of effector functions and suggests that pathogen success in natural environments depends on dynamic interactions with both the plant host and its microbiota.