A monophyletic Fusarium that includes the Fusarium solani species complex is strongly supported by a 19-gene phylogenomic analysis

Authors: GEISER, DAVID - Pennsylvania State University; AL-HATMI, ABDULLAH - Ministry Of Health; AOKI, TAKAYUKI - National Agriculture And Food Research Organization (NARO), Agricultrual Research Center; ARIE, TSUTOMU - Tokyo University Of Agriculture & Technology; BALMAS, VIRGILIO - Dipartimento Di Agraria, Universita Degli Studi Di Sassari; BARNES, IRENE - University Of Pretoria; BERGSTROM, GARY - Cornell University; BHATTACHARYYA, MADAN - Iowa State University; BLOOMQUIST, CHERYL - California Department Of Food And Agriculture; Bowden, Robert; BRANKOVICS, BALAZS - Wageningen University And Research Center; Brown, Daren; BURGESS, LESTER - University Of Sydney; BUSHLEY, KATHRYN - University Of Minnesota; Busman, Mark; CANO-LIRA, JOSE - University Rovira I Virgili; CARILLO, JOSEPH - University Of Florida; CHANG, HAO-XUN - National Taiwan University; CHEN, CHI-YU - National Chung-Hsing University; CHEN, WANQUAN - Chinese Academy Of Agricultural Sciences; CHILVERS, MARTIN - Michigan State University; CHULZE, SOFIA - National University Of Rio Cuarto; COLEMAN, JEFFREY - Auburn University; CUOMO, CHRISTINA - Broad Institute Of Mit/harvard; DE BEER, WILHELM - University Of Pretoria; DE HOOG, SYBREN - Radboud University; DEL CASTILLO-MUNERA, JOHANNA - University Of California, Davis; DEL PONTE, EMERSON - Universidade Federal De Vicosa; DIEGUEZ-URIBEONDO, JAVIER - Real Jardin Bolancio Csic; DI PIETRO, ANTONIO - Universidad De Cordoba; EDEL-HERMANN, VERONIQUE - French National Institute For Agricultural Research; ELMER, WADE - Connecticut Agricultural Experiment Station; EPSTEIN, LYNN - University Of California, Davis; ESKALEN, AKIF - University Of California, Davis; ESPOSTO, MARIA CARMELA - Universita Degli Studi Di Salerno; EVERTS, KATHRYNE - University Of Maryland; FERNANDEZ-PAVIA, SYLVIA - Universidad Michoacana De San Nicolas De Hidalgo; FERREIRA DA SILVA, GILVAN - Embrapa; FOROUD, NORA - Lethbridge Research Center; FOURIE, GERDA - University Of Pretoria; FRANDSEN, RASMUS J.N. - Technical University Of Denmark; FREEMAN, STANLEY - Volcani Center (ARO); FREITAG, MICHAEL - Oregon State University; FRENKEL, OMER - Volcani Center (ARO); FULLER, KEVIN - University Of Oklahoma Health Sciences Center; GAGKAEVA, TATIANA - All-Russian Institute For Plant Protection; GARDINER, DONALD - Csiro European Laboratory; Glenn, Anthony - Tony; Gold, Scott; GORDON, THOMAS - University Of California, Davis; GRYZENHOUT, MARIEKA - University Of The Free State; GUARRO, JOSEP - University Rovira I Virgili; GUGINO, BETH - Pennsylvania State University; GUTIERREZ, SANTIAGO - University Of Leon; Kim, Hye-Seon; Kistler, Harold; Lofton, Lily; LARABA, IMANE - Oak Ridge Institute For Science And Education (ORISE); Martin, Frank; McCormick, Susan; O Donnell, Kerry; Proctor, Robert; Rehner, Stephen; Vaughan, Martha; Ward, Todd

Submitted to: Phytopathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/13/2020
Publication Date: 9/9/2021
Citation: Geiser, D.M., Al-Hatmi, A., Aoki, T., Arie, T., Balmas, V., Barnes, I., Bergstrom, G.C., Bhattacharyya, M.K., Bloomquist, C.L., Bowden, R.L., Brankovics, B., Brown, D.W., Burgess, L.W., Bushley, K., Busman, M., Cano-Lira, J.F., Carillo, J.D., Chang, H., Chen, C., Chen, W., Chilvers, M., Chulze, S., Coleman, J.J., Cuomo, C.A., De Beer, W., De Hoog, S., Del Castillo-Munera, J., Del Ponte, E.M., Dieguez-Uribeondo, J., Di Pietro, A., Edel-Hermann, V., Elmer, W.H., Epstein, L., Eskalen, A., Esposto, M., Everts, K.L., Fernandez-Pavia, S.P., Ferreira Da Silva, G., Foroud, N.A., Fourie, G., Frandsen, R., Freeman, S., Freitag, M., Frenkel, O., Fuller, K.K., Gagkaeva, T., Gardiner, D.M., Glenn, A.E., Gold, S.E., Gordon, T., Gryzenhout, M., Guarro, J., Gugino, B.K., Gutierrez, S., Kim, H., Kistler, H.C., Lofton, L., Laraba, I., Martin, F.N., Mccormick, S.P., O Donnell, K., Proctor, R., Rehner, S.A., Vaughan, M.M., Ward, T.J. 2021. A monophyletic Fusarium that includes the Fusarium solani species complex is strongly supported by a 19-gene phylogenomic analysis. Phytopathology. https://doi.org/10.1094/PHYTO-08-20-0330-LE.
DOI: https://doi.org/10.1094/PHYTO-08-20-0330-LE

Interpretive Summary: Fusarium is regarded as one of the most economically destructive groups of toxin-producing plant pathogens and emergent human pathogens. The diverse toxins they produce frequently contaminate food and feed, making it unsuitable for consumption by humans and other animals. Thus, they pose a significant global threat to food safety, agricultural biosecurity, and plant, human and animal health. Reduction in yields and quality due to Fusarium-induced diseases are responsible for multibillion-dollar annual losses to the global agricultural economy. Therefore, in our interconnected global economy, it is essential that plant disease specialists and quarantine officials worldwide use the same name for the same pathogen responsible for an outbreak or epidemic. DNA data is the current gold standard for rapidly and accurately identifying Fusarium pathogens throughout the world. In this study, which is coauthored by a nearly unanimous global Fusarium community, DNA sequences of 19 genes from 84 fusaria and closely related species were analyzed genetically to evaluate evolutionary relationships and determine what groups were supported as belonging in Fusarium. The comparative genomics analysis provided strong statistical support for inclusion of several early branching lineages in Fusarium, including the F. solani species complex (FFSC). The FSSC comprises more than 90 species that were recently misclassified in the genus Neocosmospora. There are potentially serious consequences associated with using the name Neocosmospora for Fusarium species because clinicians and plant pathologists need to be aware that fusaria are broadly resistant to the spectrum of antifungals/fungicides that are currently available. To fix this problem, the Neocosmospora species were reclassified here as Fusarium where they belong. The research reported here, which represents the most detailed evolutionary genetic assessment of the genus Fusarium to date, will be of interest to plant pathologists, mycotoxicologists, medical mycologists and quarantine officials worldwide.

Technical Abstract: The Fusarium solani species complex (FSSC) represents a monophyletic group of phylogenetically diagnosable species, including many important plant pathogens. Previously (Geiser et al. 2013 Phytopathology 103:400-408. 2013), the Fusarium community nearly unanimously voiced support for a concept of Fusarium that represented a clade comprising all economically important Fusarium species, including the FSSC. Since then, papers published from the Westerdijk Insititute in the Netherlands (Lombard et al. 2015; Sandoval-Denis and Crous 2018; Sandoval-Denis et al. 2018, 2019) have promoted splitting Fusarium into seven genera, including the FSSC as the genus Neocosmospora. One of these publications (Sandoval-Denis and Crous 2018) claims that the Geiser et al. (2013) concept of Fusarium is polyphyletic, and that their concept of Neocosmospora reflected a "more natural" taxonomic approach. Here we point out that these claims are incontrovertibly false, bolstered with a phylogeny based on 19 orthologous protein-coding genes that demonstrates robust monophyly of Fusarium inclusive of the FSSC. In recognition of this, we recombined 40 species recently described as Neocosmospora into Fusarium, and renamed nine others. We re-assert the practical and scientific argument in support of a Fusarium that includes the FSSC and several other basal lineages, consistent with the longstanding use of this name among plant pathologists, medical mycologists and other citizens, students and researchers with a stake in its taxonomy. The nearly unanimous global Fusarium community will continue to view the FSSC as Fusarium, as it is the best scientific, nomenclatural and practical taxonomic option available.