Host-dependent fungus-fungus competition suppresses fungal pathogenesis in<i>Arabidopsis thaliana</i>

<jats:title>Abstract</jats:title><jats:p>Like animals, plants accommodate a rich diversity of microbes, typically without discernible disease symptoms. How their pathogenesis is prevented in the host remains obscure. Here, we show that the root-infecting fungus<jats:italic>Colletotrichum fructicola</jats:italic>of the<jats:italic>C</jats:italic>.<jats:italic>gloeosporioides</jats:italic>clade (CgE), isolated from field-grown healthy Brassicaceae plants, inhibits growth of pathogenic fungi in<jats:italic>Arabidopsis thaliana</jats:italic>, in a phosphate status-dependent manner. Loss of host ethylene signaling or phytoalexins, camalexin or indole glucosinolates, however, allows CgE to display pathogenesis, suggesting host contributions to endophytic CgE colonization and benefit. Compared to a closely-related<jats:italic>C. gloeosporioides</jats:italic>pathogen (CgP), CgE is characterized by genome expansion and >700 fungal genes (4.34%) specifically induced in the host roots when co-inoculated with CgP, including genes related to fungal secondary metabolism. This may underlie antimicrobial tolerance of CgE and its dominance over pathogenic fungi within the host, pointing to a role for fungus-fungus competition in asymptomatic fungal colonization in plants.</jats:p>