Genome evolution and transposable element expansion reveal host-associated genomic features in Cladosporium cucumerinum

How pathogens adapt to specific hosts remains an open question. Here, we investigate Cladosporium cucumerinum, a pathogen largely associated with Cucurbitaceae. Comparative genomic analysis of five newly Cladosporium sequenced genomes together with 19 publicly available genomes indicates that the diversification of C. cucumerinum occurred after that of its cucumber host lineage. We observe gene family contraction alongside lineage-specific expansion of long terminal repeat retrotransposons, accompanied by variation in gene repertoires including carbohydrate-active enzymes and secondary metabolite gene clusters. A lineage-specific β-glucosidase, CcBGL258, is required for pathogenicity but is dispensable for vegetative growth under in vitro conditions. Transcriptomic analyses reveal dynamic changes in gene expression during infection in both the pathogen and the host. Together, these results provide a genomic framework for host-associated features in C. cucumerinum, although we highlight that several associations observed in the study remain correlative and require further functional validation. Comparative genomics and transcriptomics, together with gene knockout experiments, identify CcBGL258 as a pathogenicity-associated factor and provide a framework for studying host-associated features in Cladosporium cucumerinum.