Genus-wide comparative genomics of Colletotrichum reveals evolutionary conservation and divergent ecological adaptations

Abstract

Abstract Colletotrichum spp. are widespread fungal pathogens that cause anthracnose in numerous economically important crops and, exhibiting extensive taxonomic, host plant, and lifestyle diversity. Here, we analyzed the genome sequences of 150 strains representing 97 species across 15 species complexes and four singletons, including and integrating both newly assembled and publicly available genomes. Phylogenomic investigation clarified the taxonomy of Colletotrichum and resolved misidentifications. We identified variations in genome architecture contributed by phylogenetic lineages, host types, and lifestyles, with transposable element proliferation playing significant roles. Interestingly, codon usage bias followed phylogenetic patterns, with species complexes forming distinct clusters and exhibiting a significant bistable co-evolutionary relationship with tRNA genes. Functional gene repertoires displayed coordinated shifts, with higher abundance in broad host-range species complexes and in strains associated with woody or dicotyledonous hosts. Although most functional categories retained strong phylogenetic signals, co-occurrence analysis of weak-signal categories identified modules related to host cell wall disruption, fungal cell wall remodeling, and virulence that were significantly associated with ecological differentiation. Evolutionary trajectories and gene family dynamics further revealed divergent ecological strategies, with oxidative versus rapid-response detoxification in woody- and herbaceous-associated lineages, respectively. The diversifications were accompanied by woody-specific expansion of GH39 and alkaline proteases and progressive differentiation of pectin-degrading capacity, including contraction in woody lineages and divergence between dicot- and monocot-associated herbaceous lineages. The C. gloeosporioides species complex emerged with a comprehensive expansion of detoxification and cell wall-degrading capacities, likely contributing to its broad host range. In contrast, endophytic lineages exhibited convergent gene family contraction in adhesion and cell wall remodeling. Together, this study revealed concordance of codon usage and functional gene abundance with phylogeny, along with diverse host- and lifestyle-associated adaptive strategies in this important group of plant pathogens.