Fusarium (Hypocreales, Nectriaceae) is one of the most economically important and systematically challenging groups of mycotoxigenic phytopathogens and emergent human pathogens. We conducted maximum likelihood (ML), maximum parsimony (MP) and Bayesian (B) analyses on partial DNA-directed RNA polymerase II largest (RPB1) and second largest subunit (RPB2) nucleotide sequences of 93 fusaria to infer the first comprehensive and well-supported phylogenetic hypothesis of evolutionary relationships within the genus and 20 of its near relatives. Our analyses revealed that Cylindrocarpon formed a basal monophyletic sister to a 'terminal Fusarium clade' (TFC) comprising 20 strongly supported species complexes and nine monotypic lineages, which we provisionally recognize as Fusarium (hypothesis F1). The basal-most divergences within the TFC were only significantly supported by Bayesian posterior probabilities (B-PP 0.99-1). An internode of the remaining TFC, however, was strongly supported by MP and ML bootstrapping and B-PP (hypothesis F2). Analysis of seven Fusarium genome sequences and Southern analysis of fusaria elucidated the distribution of genes required for synthesis of 26 families of secondary metabolites within the phylogenetic framework. Diversification time estimates date the origin of the TFC to the middle Cretaceous 91.3 million years ago. We also dated the origin of several agriculturally important secondary metabolites as well as the lineage responsible for Fusarium head blight of cereals. Dating of several plant-associated species complexes suggests their evolution may have been driven by angiosperm diversification during the Miocene. Our results support two competing hypotheses for the circumscription of Fusarium and provide a framework for future comparative phylogenetic and genomic analyses of this agronomically and medically important genus.

Panama disease of banana, caused by the fungus Fusarium oxysporum f. sp. cubense, is a serious constraint both to the commercial production of banana and cultivation for subsistence agriculture. Previous work has indicated that F. oxysporum f. sp. cubense consists of several clonal lineages that may be genetically distant. In this study we tested whether lineages of the Panama disease pathogen have a monophyletic origin by comparing DNA sequences of nuclear and mitochondrial genes. DNA sequences were obtained for translation elongation factor 1alpha and the mitochondrial small subunit ribosomal RNA genes for F. oxysporum strains from banana, pathogenic strains from other hosts and putatively nonpathogenic isolates of F. oxysporum. Cladograms for the two genes were highly concordant and a partition-homogeneity test indicated the two datasets could be combined. The tree inferred from the combined dataset resolved five lineages corresponding to "F. oxysporum f. sp. cubense" with a large dichotomy between two taxa represented by strains most commonly isolated from bananas with Panama disease. The results also demonstrate that the latter two taxa have significantly different chromosome numbers. F. oxysporum isolates collected as nonpathogenic or pathogenic to other hosts that have very similar or identical elongation factor 1alpha and mitochondrial small subunit genotypes as banana pathogens were shown to cause little or no disease on banana. Taken together, these results indicate Panama disease of banana is caused by fungi with independent evolutionary origins.