Comparative Genomic Insights into the Diversification of Agaricomycotina Within the Phylum Basidiomycota

Basidiomycota is a diverse fungal phylum whose major subphyla exhibit contrasting evolutionary histories, with Agaricomycotina representing the most species-rich and morphologically diverse lineage. To investigate the genomic patterns associated with these differences, we conducted a comparative phylogenomic analysis of 353 Basidiomycota and eight outgroup genomes. A time-calibrated tree indicated Agaricomycotina as the youngest of the major basidiomycete subphyla, originating approximately 295.32 million years ago (Ma), with major diversification of Agaricomycetes occurring during the Jurassic and Cretaceous. Reconciliation of 1123 conserved BUSCO ortholog gene trees revealed distinct patterns of inferred gene duplication and loss among the major subphyla, with the largest inferred duplication event occurring within Agaricomycetes. Comparative analyses further showed that Agaricomycotina possessed significantly larger repertoires of carbohydrate-active enzymes (CAZymes) and biosynthetic gene clusters (BGCs) than Pucciniomycotina and Ustilaginomycotina, particularly among filamentous saprotrophic lineages with complex fruitbody morphologies. In addition, Agaricomycotina exhibited greater root-to-tip evolutionary distances and gene numbers, whereas Pucciniomycotina possessed larger genomes and Ustilaginomycotina exhibited compact, GC-rich genomes. Collectively, these findings suggest that ecological timing, inferred patterns of genome evolution, expanded functional repertoires, and distinct genome characteristics were associated with the diversification and exceptional species richness of Agaricomycotina. This study provides a comparative phylogenomic framework for investigating evolutionary diversification across the major Basidiomycota subphyla.