Scientific communication is facilitated by a data-driven, scientifically sound taxonomy that considers the end-user’s needs and established successful practice. In 2013, the Fusarium community voiced near unanimous support for a concept of Fusarium that represented a clade comprising all agriculturally and clinically important Fusarium species, including the F. solani species complex (FSSC). Subsequently, this concept was challenged in 2015 by one research group who proposed dividing the genus Fusarium into seven genera, including the FSSC described as members of the genus Neocosmospora, with subsequent justification in 2018 based on claims that the 2013 concept of Fusarium is polyphyletic. Here, we test this claim and provide a phylogeny based on exonic nucleotide sequences of 19 orthologous protein-coding genes that strongly support the monophyly of Fusarium including the FSSC. We reassert the practical and scientific argument in support of a genus Fusarium that includes the FSSC and several other basal lineages, consistent with the longstanding use of this name among plant pathologists, medical mycologists, quarantine officials, regulatory agencies, students, and researchers with a stake in its taxonomy. In recognition of this monophyly, 40 species described as genus Neocosmospora were recombined in genus Fusarium, and nine others were renamed Fusarium. Here the global Fusarium community voices strong support for the inclusion of the FSSC in Fusarium, as it remains the best scientific, nomenclatural, and practical taxonomic option available.

Trichothecenes are a family of terpenoid toxins produced by multiple genera of fungi, including plant and insect pathogens. Some trichothecenes produced by the fungus Fusarium are among the mycotoxins of greatest concern to food and feed safety because of their toxicity and frequent occurrence in cereal crops, and trichothecene production contributes to pathogenesis of some Fusarium species on plants. Collectively, fungi produce over 150 trichothecene analogs: i.e., molecules that share the same core structure but differ in patterns of substituents attached to the core structure. Here, we carried out genomic, phylogenetic, gene-function, and analytical chemistry studies of strains from nine fungal genera to identify genetic variation responsible for trichothecene structural diversity and to gain insight into evolutionary processes that have contributed to the variation. The results indicate that structural diversity has resulted from gain, loss, and functional changes of trichothecene biosynthetic (TRI) genes. The results also indicate that the presence of some substituents has arisen independently in different fungi by gain of different genes with the same function. Variation in TRI gene duplication and number of TRI loci was also observed among the fungi examined, but there was no evidence that such genetic differences have contributed to trichothecene structural variation. We also inferred ancestral states of the TRI cluster and trichothecene biosynthetic pathway, and proposed scenarios for changes in trichothecene structures during divergence of TRI cluster homologs. Together, our findings provide insight into evolutionary processes responsible for structural diversification of toxins produced by pathogenic fungi. Toxins produced by pathogens can contribute to infection and/or colonization of hosts. Some toxins consist of a family of metabolites with similar but distinct chemical structures. This structural variation can affect biological activity, which in turn likely contributes to adaptation to different environments, including to different hosts. Trichothecene toxins consist of over 150 structurally distinct molecules produced by certain fungi, including some plant and insect pathogens. In multiple systems that have been examined, trichothecenes contribute to pathogenesis on plants. To elucidate the evolutionary processes that have given rise to trichothecene structural variation, we conducted comparative analyses of nine fungal genera, most of which produce different trichothecene structures. Using genomic, molecular biology, phylogenetic, and analytical chemistry approaches, we obtained evidence that trichothecene structural variation has arisen primarily from gain, loss, and functional changes of trichothecene biosynthetic genes. Our results also indicate that some structural changes have arisen independently in different fungi. Our findings provide insight into genetic and biochemical changes that can occur in toxin biosynthetic pathways as fungi with the pathways adapt to different environmental conditions.

Fumonisins are mycotoxins produced by some Fusarium species and can contaminate maize or maize products. Ingestion of fumonisins is associated with diseases, including cancer and neural tube defects, in humans and animals. In fungi, genes involved in the synthesis of mycotoxins and other secondary metabolites are often located adjacent to each other in gene clusters. Such genes can encode structural enzymes, regulatory proteins, and/or proteins that provide self-protection. The fumonisin biosynthetic gene cluster includes 16 genes, none of which appear to play a role in regulation. In this study, we identified a previously undescribed gene ( FUM21 ) located adjacent to the fumonisin polyketide synthase gene, FUM1 . The presence of a Zn(II)2Cys6 DNA-binding domain in the predicted protein suggested that FUM21 was involved in transcriptional regulation. FUM21 deletion (Δ fum21 ) mutants produce little to no fumonisin in cracked maize cultures but some FUM1 and FUM8 transcripts in a liquid GYAM medium. Complementation of a Δ fum21 mutant with a wild-type copy of the gene restored fumonisin production. Analysis of FUM21 cDNAs identified four alternative splice forms (ASFs), and microarray analysis indicated the ASFs were differentially expressed. Based on these data, we present a model for how FUM21 ASFs may regulate fumonisin biosynthesis.

The Fusarium incarnatum-equiseti species complex (FIESC) comprises 33 phylogenetically distinct species that have been recovered from diverse biological sources, but have been most often isolated from agricultural plants and soils. Collectively, members of FIESC can produce diverse mycotoxins. However, because the species diversity of FIESC has been recognized only recently, the potential of species to cause mycotoxin contamination of crop plants is unclear. In this study, therefore, we used comparative genomics to investigate the distribution of and variation in genes and gene clusters responsible for the synthesis of mycotoxins and other secondary metabolites (SMs) in FIESC. We examined genomes of 13 members of FIESC that were selected based primarily on their phylogenetic diversity and/or occurrence on crops. The presence and absence of SM biosynthetic gene clusters varied markedly among the genomes. For example, the trichothecene mycotoxin as well as the carotenoid and fusarubin pigment clusters were present in all genomes examined, whereas the enniatin, fusarin, and zearalenone mycotoxin clusters were present in only some genomes. Some clusters exhibited discontinuous patterns of distribution in that their presence and absence was not correlated with the phylogenetic relationships of species. We also found evidence that cluster loss and horizontal gene transfer have contributed to such distribution patterns. For example, a combination of multiple phylogenetic analyses suggest that five NRPS and seven PKS genes were introduced into FIESC from other Fusarium lineages. Our results suggest that although the portion of the genome devoted to SM biosynthesis has remained similar during the evolutionary diversification of FIESC, the ability to produce SMs could be affected by the different distribution of related functional and complete gene clusters.