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Title: Phylogenetic analyses of RPB1 and RPB2 support a middle Cretaceous origin for a clade comprising all agriculturally and medically important fusaria

item O Donnell, Kerry
item Rooney, Alejandro - Alex
item Proctor, Robert
item Brown, Daren
item McCormick, Susan
item Ward, Todd
item FRANDSEN, RASMUS J - Technical University Of Denmark
item LYSOE, ERIK - Bioforsk
item Rehner, Stephen
item AOKI, TAKAYUKI - National Institute Of Agrobiological Sciences (NIAS)

Submitted to: Fungal Genetics and Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/20/2012
Publication Date: 3/1/2013
Citation: O'Donnell, K., Rooney, A.P., Proctor, R., Brown, D.W., McCormick, S.P., Ward, T.J., Frandsen, R.N., Lysoe, E., Rehner, S.A., Aoki, T., et al. 2013. Phylogenetic analyses of RPB1 and RPB2 support a middle Cretaceous origin for a clade comprising all agriculturally and medically important fusaria. Fungal Genetics and Biology. 52:20-31.

Interpretive Summary: Fusarium species rank among the most economically destructive plant pathogens and mycotoxigenic fungi, posing a constant threat to plant and animal health and food safety. The diverse toxins these fungi elaborate are responsible for multi-billion U.S. dollar losses to world agriculture annually. Because Fusarium species differ significantly in their ability to produce toxins and cause diseases of plants and animals, including humans, it is critical that robust and comprehensive web-accessible molecular data bases be developed to facilitate the rapid detection and accurate identification these fungi in our food supply. Towards this end, we have used DNA sequence data to clarify the limits of diversity within Fusarium and to assess the distribution and evolution of toxigenic and pathogenic diversity within this group of fungi. These data will facilitate identification and differentiation of Fusarium, and also enable prediction of the toxigenic or pathogenic potential of poorly studied species within this group. The data included in the present study have been incorporated into Fusarium-ID ( at the Pennsylvania State University and Fusarium MLST ( at the Centraalbureau voor Schimmelcultures (CBS-KNAW) Biodiversity Center, two web-accessible sites dedicated to promoting DNA sequence-based identifications of fusaria via the Internet. Lastly, our results provide a robust framework and a useful guide for future analyses of this agriculturally and medically important genus. Results of the present study will be of interest to plant pathologists, mycotoxicologists, plant breeders and quarantine officials who are charged with controlling fusarial disease, developing cultivars with broad-based resistance to these pathogens, and preventing these pathogens and their toxins from entering the world’s food supply.

Technical Abstract: 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 RNA polymerase 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 analysis revealed that Cylindrocarpon formed a basal monophyletic sister to a ‘terminal Fusarium clade’ (TFC, sensu Gräfenhan et al., 2011) comprising 20 strongly supported species complexes and nine monotypic lineages. The basal-most divergences within the TFC were only significantly supported by Bayesian posterior probabilities (B-PP = 0.99-1), with the ventricosum and dimerum species complexes forming the two earliest diverging lineages. An internode supporting the remaining TFC, however, was strongly supported by MP and ML bootstrapping (ML-BS 100%, MP-BS 87%) and by a B-PP of 1. By way of contrast, reanalysis of the Gräfenhan et al. two-locus data set (portions of RPB2 and ATP citrate lyase) did not resolve any strongly supported relationship among the eight basal-most lineages within the TFC. Diversification time estimates date the origin of the TFC to the middle Cretaceous 91.3 million years ago (Mya) (95% highest posterior density [HPD] interval: 44.7, 149.3). We also dated the evolutionary origin of several bioactive secondary metabolites, including three mycotoxins and the gibberellin phytohormones, as well as the economically devastating plant pathogenic lineage responsible for Fusarium head blight (FHB) of cereals. Dating of several plant-associated species complexes (e.g., fujikuroi, sambucinum, tricinctum and nisikadoi) suggests their evolution may have been driven by angiosperm diversification during the Miocene. Our results support two explicit competing hypotheses for the circumscription of Fusarium and provide a robust framework for future comparative phylogenetic and genomic analyses of this agronomically and medically important genus.