Exploring criteria for constructing suprageneric classifications of fungi in the genomic era: a case study of suborders Agaricineae, Pluteineae, and Tricholomatineae (Agaricales)

The burgeoning accumulation of genomic data in recent years has revolutionized our understanding of fungal phylogenies and classifications. However, the genomic era also brings new challenges, as phylogenetic incongruences make the appearance of monophyly in some phylogenetic trees questionable. Existing criteria for constructing taxonomic systems, such as diagnostic characters and divergence time, become insufficient to address this challenge. Through order-level analyses of genomic data of the Subkingdom Dikarya within the Kingdom Fungi, we introduce the extended quadripartition internode certainty (EQP-IC) value as a novel criterion for constructing high-level fungal classifications, with a recommended threshold of 0.1 for each taxonomic rank. Suprageneric taxa with an EQP-IC value exceeding 0.1 exhibit reduced topological variation, suggesting a stronger correspondence with natural taxonomic category. This new criterion was also put into practice to investigate the derived suborders of mushroom-forming Agaricales, including three suborders, Agaricineae, Pluteineae, and Tricholomatineae (APT), that had been long-standing problems in phylogenetic analyses. In total, 142 genomes, including 64 newly generated ones, were utilized to reconstruct the phylogenetic relationships and delve into the phylogenetic incongruencies and evolutionary histories of APT. Our data suggested widespread and high-level incomplete lineage sorting (ILS) and introgression/hybridization (IH) present among suborders within the APT. Therefore, a dichotomous phylogenetic tree may not reflect the real relationships among the clades within the APT. Instead, their natural relationships may be reticulate. Three newly named suborders, Amanitineae, Macrocystidiineae, and Omphalinineae are added to the clade including APT. The new combination Baisuzhenia humphreyi, new genus Baisuzhenia, new family Baisuzheniaceae, and new suborder Baisuzheniineae are proposed to accommodate Stereopsis humphreyi, which shows an independent, but close relationship, with the clade formed by the six above-mentioned derived suborders of Agaricales.