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.

Fusarium is one of the most important genera of plant-pathogenic fungi in the world and arguably the world's most important mycotoxin-producing genus. Fusarium species produce a staggering array of toxic metabolites that contribute to plant disease and mycotoxicoses in humans and other animals. A thorough understanding of the mycotoxin potential of individual species is crucial for assessing the toxicological risks associated with Fusarium diseases. There are thousands of reports of mycotoxin production by various species, and there have been numerous attempts to summarize them. These efforts have been complicated by competing classification systems based on morphology, sexual compatibility, and phylogenetic relationships. The current depth of knowledge of Fusarium genomes and mycotoxin biosynthetic pathways provides insights into how mycotoxin production is distributedamong species and multispecies lineages (species complexes) in the genus as well as opportunities to clarify and predict mycotoxin risks connected with known and newly described species. Here, we summarize mycotoxin production in the genus Fusarium and how mycotoxin risk aligns with current phylogenetic species concepts.

Summary: Trichothecenes are terpene‐derived secondary metabolites produced by multiple genera of filamentous fungi, including many plant pathogenic species of Fusarium. These metabolites are of interest because they are toxic to animals and plants and can contribute to pathogenesis of Fusarium on some crop species. Fusarium graminearum and F. sporotrichioides have trichothecene biosynthetic genes (TRI) at three loci: a 12‐gene TRI cluster and two smaller TRI loci that consist of one or two genes. Here, comparisons of additional Fusarium species have provided evidence that TRI loci have a complex evolutionary history that has included loss, non‐functionalization and rearrangement of genes as well as trans‐species polymorphism. The results also indicate that the TRI cluster has expanded in some species by relocation of two genes into it from the smaller loci. Thus, evolutionary forces have driven consolidation of TRI genes into fewer loci in some fusaria but have maintained three distinct TRI loci in others.

This study was conducted to determine the species identity and mycotoxin potential of 158 Fusarium strains originally archived in the South African Medical Research Council’s Mycotoxigenic Fungal Collection (MRC) that were reported to comprise 17 morphologically distinct species in the classic 1984 compilation by Marasas et al., Toxigenic Fusarium Species: Identity and Mycotoxicology. Maximum likelihood and maximum parsimony molecular phylogenetic analyses of single and multilocus DNA sequence data indicated that the strains represented 46 genealogically exclusive phylogenetically distinct species distributed among eight species complexes. Moreover, the phylogenetic data revealed that 80/158 strains were received under a name that is not accepted today (ex F. moniliforme) or classified under a different species name. In addition, gas chromatography–mass spectrometry (GC-MS) and/or high-performance liquid chromatography–mass spectrometry (HPLC-MS)-based mycotoxin analyses were conducted to determine which toxins the strains could produce in liquid and/or solid cultures. All of the trichothecene toxin–producing fusaria were nested within the F. sambucinum (FSAMSC) or F. incarnatum-equiseti (FIESC) species complexes. Consistent with this finding, GC-MS analyses detected trichothecenes in agmatine-containing broth or rice culture extracts of all 13 FSAMSC and 10/12 FIESC species tested. Species in six and seven of the eight species complexes were able to produce moniliformin and beauvericin, respectively, whereas B-type fumonisins were only detected in extracts of cracked maize kernel cultures of three species in the F. fujikuroi (FFSC) species complex.