Genomic features and evolution of lifestyles support the recognition of distinct genera among fusarioid fungi

Abstract

The family Nectriaceae (Hypocreales, Sordariomycetes) includes saprobes, endophytes and numerous important pathogens, several of which are of high commercial interest. Presently there are numerous genera scattered throughout the Nectriaceae that have a fusarioid asexual morph (i.e., genera with fusarium-like macroconidia). Fusarioid fungi encompass diverse lifestyles, including plant, human, and animal pathogens or associates, saprobes, lichenicolous species, endophytes, and mycophilic taxa. The fusarioid genera in Nectriaceae do not only differ in their sexual morphs, but also in their asexual morphology and biology, although their ecology has remained rather unclear. While genome data are available for numerous species, this has been mostly focused on Fusarium sensu stricto, as the genus encompasses most of the economically important species in this generic complex. To compliment this, we expanded the sampling, and generated whole genome sequences for 40 isolates representing the genera Atractium, Bisifusarium, Cinnamomeonectria, Corinectria, Cosmospora, Cyanonectria, Cylindrodendrum, Dialonectria, Fusarium, Fusicolla, Geejayessia, Ilyonectria, Macroconia, Macronectria, Microcera, Neocosmospora, Neonectria, Pseudofusicolla, Rectifusarium, Rugonectria, Scolecofusarium, Thelonectria, and Tumenectria. Phylogenomic ancestral reconstructions showed that plant pathogenicity is most likely ancestral to Fusarium and cylindrocarpioid genera, and revealed multiple and frequent lifestyle transitions. Although many species are prolific generalists, several genera appear to be more specialised, being primarily plant pathogens, mycophilic, or insect associated, while endophytism or plant pathogenicity evolved several times, and more recently in Fusarium. The broadly sampled Nectriaceae genomes supported morphological differences between most genera of Nectriaceae, mirrored by genome sizes, lactic enzymes, biosynthetic gene clusters, and small secreted proteins. Furthermore, it also supported a narrow circumscription of Fusarium in Nectriaceae that equals its morphology (Gibberella sexual morphs), and biology.