Host-mediated endophyte-pathogen competition in roots enables asymptomatic fungal colonization in Arabidopsis thaliana

Summary Seed plants frequently accommodate pathogenic microbes without showing disease symptoms. However, the mechanisms preventing disease progression within the host remain poorly understood. Here, we reveal a root-colonizing endophytic fungus, Colletotrichum fructicola (designated CfE), and a closely related pathogen, C. gloeosporioides (CgP), from asymptomatic field-grown Brassicaceae plants. In Arabidopsis thaliana, CgP grows hyphae into the central cylinder of the root and causes necrosis, an outcome that is effectively suppressed in the presence of CfE co-colonization. Transcriptome analyses of roots inoculated individually and simultaneously with CfE and CgP revealed over 700 CfE genes specifically induced during co-inoculation, while the extent of reprogramming in the host transcriptome was much less pronounced. These induced genes were enriched in secondary metabolism pathways, suggesting that CfE suppresses pathogenic fungal growth through the production of antifungal metabolites. Moreover, the endophytic colonization and host-protective function of CfE depend on host-derived tryptophan-based antimicrobial metabolites. Our findings highlight a critical role for fungus-fungus competition, mediated by anti-microbial metabolites and potentially orchestrated by the host, in enabling asymptomatic colonization and maintaining plant health.