Genetic factors driving multi-host infection in a core member of the root mycobiota

Core members of the fungal root microbiota often include pathogens capable of colonizing diverse host plants, yet the underlying genetic determinants driving multi-host infection remain unknown. Here, we report that Plectosphaerella cucumerina is a pathogenic, yet core member of the Arabidopsis root microbiota and a widespread multi-host root colonizer. Culture collection establishment followed by whole-genome sequencing of 72 strains revealed limited phenotypic and genotypic variation that did not associate with host plant phylogeny. Multi-host recolonization experiments combined with in planta fungal transcriptomics uncovered transcriptional states involved in both general and host-specific infection. Notably, host variation in root cell wall composition associated with activation of fungal genes encoding cognate cell wall-degrading enzymes, thereby representing a strategy for plastic adaptation to multiple hosts. Using CRISPR/Cas9-mediated genome editing, we also demonstrated that a glucanase-encoding gene serves as a crucial fungal determinant, facilitating multi-host colonization and disease development in plants that diverged 110 million years ago.