Local plant leaf fungi act as weapons against invasive plants

Native community resistance to plant invasion may be mediated by microbial effects on invader establishment. Here, we compared how the aboveground and belowground microbes, as well as the leaf functional traits of 25 native plant species, affect the germination and survival of the invader Ageratina adenophora. The results showed that leaf physical and chemical traits varied among species and shaped the aboveground microbial community. Local plants that were more phylogenetically closely related to A. adenophora harbored pathogen communities more similar to those found in A. adenophora. Inoculations using aboveground tissues had stronger adverse effects on A. adenophora establishment than soil inoculations, by delaying germination, reducing the germination rate, and decreasing seedling survival. Aboveground tissues from native plants that were more closely related to A. adenophora caused longer germination time and higher seedling mortality. Furthermore, it was the aboveground fungi, rather than bacteria, from local plants that negatively impacted seedling survival, with most of the detrimental fungal amplicon sequence variants (ASVs) being specialist pathogens. Several fungal strains isolated from dead seedlings following aboveground tissue inoculations—belonging to Alternaria, Fusarium, and Stagonosporopsis—were confirmed to kill over 60% of A. adenophora seedlings, demonstrating their high potential as biocontrol agents. This study provides evidence that phylogenetic relatedness and leaf traits (both functional and microbial) can influence local community resistance to invaders by regulating germination and seedling survival.