Phylogenomic Analysis of a 55.1-kb 19-Gene Dataset Resolves a Monophyletic Fusarium that Includes the Fusarium solani Species Complex

Author:

Geiser David M.1ORCID,Al-Hatmi Abdullah M. S.2ORCID,Aoki Takayuki3,Arie Tsutomu4,Balmas Virgilio5,Barnes Irene6ORCID,Bergstrom Gary C.7ORCID,Bhattacharyya Madan K.8,Blomquist Cheryl L.9,Bowden Robert L.10ORCID,Brankovics Balázs11ORCID,Brown Daren W.12,Burgess Lester W.13,Bushley Kathryn14,Busman Mark12,Cano-Lira José F.15ORCID,Carrillo Joseph D.16,Chang Hao-Xun17ORCID,Chen Chi-Yu18ORCID,Chen Wanquan19,Chilvers Martin20,Chulze Sofia21,Coleman Jeffrey J.22ORCID,Cuomo Christina A.23ORCID,de Beer Z. Wilhelm6,de Hoog G. Sybren24,Del Castillo-Múnera Johanna25,Del Ponte Emerson M.26ORCID,Diéguez-Uribeondo Javier27,Di Pietro Antonio28,Edel-Hermann Véronique29,Elmer Wade H.30,Epstein Lynn25ORCID,Eskalen Akif25,Esposto Maria Carmela31ORCID,Everts Kathryne L.32ORCID,Fernández-Pavía Sylvia P.33,da Silva Gilvan Ferreira34,Foroud Nora A.35ORCID,Fourie Gerda6,Frandsen Rasmus J. N.36,Freeman Stanley37,Freitag Michael38,Frenkel Omer37,Fuller Kevin K.39,Gagkaeva Tatiana40,Gardiner Donald M.41ORCID,Glenn Anthony E.42ORCID,Gold Scott E.42,Gordon Thomas R.25,Gregory Nancy F.43,Gryzenhout Marieka44,Guarro Josep45,Gugino Beth K.1,Gutierrez Santiago46,Hammond-Kosack Kim E.47,Harris Linda J.48ORCID,Homa Mónika49,Hong Cheng-Fang18ORCID,Hornok László50ORCID,Huang Jenn-Wen18,Ilkit Macit51ORCID,Jacobs Adriaana52ORCID,Jacobs Karin53ORCID,Jiang Cong54,Jiménez-Gasco María del Mar1,Kang Seogchan1,Kasson Matthew T.55,Kazan Kemal41,Kennell John C.56,Kim Hye-Seon12,Kistler H. Corby57,Kuldau Gretchen A.1,Kulik Tomasz58ORCID,Kurzai Oliver59ORCID,Laraba Imane12,Laurence Matthew H.60,Lee Theresa61,Lee Yin-Won62,Lee Yong-Hwan62,Leslie John F.63ORCID,Liew Edward C. Y.60,Lofton Lily W.42,Logrieco Antonio F.64,S. López-Berges Manuel28,Luque Alicia G.65,Lysøe Erik66,Ma Li-Jun67ORCID,Marra Robert E.30,Martin Frank N.68,May Sara R.1ORCID,McCormick Susan P.12,McGee Chyanna1,Meis Jacques F.24ORCID,Migheli Quirico69,Mohamed Nor N. M. I.70ORCID,Monod Michel71,Moretti Antonio64,Mostert Diane72ORCID,Mulè Giuseppina64,Munaut Françoise73,Munkvold Gary P.74ORCID,Nicholson Paul75,Nucci Marcio76ORCID,O’Donnell Kerry12,Pasquali Matias77,Pfenning Ludwig H.78,Prigitano Anna31,Proctor Robert H.12,Ranque Stéphane79ORCID,Rehner Stephen A.80ORCID,Rep Martijn81ORCID,Rodríguez-Alvarado Gerardo33,Rose Lindy Joy72,Roth Mitchell G.82ORCID,Ruiz-Roldán Carmen28,Saleh Amgad A.83ORCID,Salleh Baharuddin70,Sang Hyunkyu84ORCID,Scandiani María Mercedes65,Scauflaire Jonathan85,Schmale David G.86,Short Dylan P. G.87,Šišić Adnan88,Smith Jason A.89,Smyth Christopher W.90,Son Hokyoung62ORCID,Spahr Ellie55ORCID,Stajich Jason E.91ORCID,Steenkamp Emma6ORCID,Steinberg Christian92ORCID,Subramaniam Rajagopal48,Suga Haruhisa93,Summerell Brett A.60,Susca Antonella64,Swett Cassandra L.25,Toomajian Christopher63ORCID,Torres-Cruz Terry J.1ORCID,Tortorano Anna M.31ORCID,Urban Martin47,Vaillancourt Lisa J.94,Vallad Gary E.16,van der Lee Theo A. J.11,Vanderpool Dan95,van Diepeningen Anne D.11,Vaughan Martha M.12ORCID,Venter Eduard96ORCID,Vermeulen Marcele97ORCID,Verweij Paul E.24,Viljoen Altus72,Waalwijk Cees11,Wallace Emma C.1,Walther Grit59ORCID,Wang Jie98,Ward Todd J.12,Wickes Brian L.99,Wiederhold Nathan P.100,Wingfield Michael J.6,Wood Ana K. M.47ORCID,Xu Jin-Rong100,Yang Xiao-Bing75,Yli-Mattila Tapani101,Yun Sung-Hwan102,Zakaria Latiffah70,Zhang Hao19,Zhang Ning103,Zhang Sean X.104ORCID,Zhang Xue54

Affiliation:

1. Department of Plant Pathology and Environmental Microbiology, Pennsylvania State University, University Park, PA 16802, U.S.A.

2. Directorate General of Health Services, Ministry of Health, Ibri, Oman

3. Genetic Resources Center, National Agriculture and Food Research Organization, Tsukuba, Japan

4. Tokyo University of Agriculture and Technology, Fuchu, Japan

5. Dipartimento di Agraria, Università degli Studi di Sassari, Sassari, Italy

6. Department of Biochemistry, Genetics and Microbiology, University of Pretoria, Pretoria, South Africa

7. Plant Pathology and Plant-Microbe Biology Section, Cornell University, Ithaca, NY 14853, U.S.A.

8. Department of Agronomy, Iowa State University, Ames, IA 50011, U.S.A.

9. Plant Pest Diagnostics Branch, California Department of Food and Agriculture, Sacramento, CA 95832, U.S.A.

10. Hard Winter Wheat Genetics Research Unit, U.S. Department of Agriculture Agricultural Research Service (USDA-ARS), Manhattan, KS 66506, U.S.A.

11. Wageningen Plant Research, Wageningen University and Research, Wageningen, The Netherlands

12. Mycotoxin Prevention and Applied Microbiology Research Unit, USDA-ARS, Peoria, IL 61604, U.S.A.

13. Sydney Institute of Agriculture, Faculty of Science, University of Sydney, Sydney, Australia

14. Department of Plant and Microbial Biology, University of Minnesota, St. Paul, MN 55108, U.S.A.

15. Mycology Unit and IISPV, Universitat Rovira i Virgili Medical School, Reus, Spain

16. Gulf Coast Research and Education Center, University of Florida, Wimauma, FL 33598, U.S.A.

17. Department of Plant Pathology and Microbiology, National Taiwan University, Taipei, Taiwan

18. Department of Plant Pathology, National Chung Hsing University, Taichung, Taiwan

19. State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agriculture Sciences, Beijing, People’s Republic of China

20. Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, MI 48824, U.S.A.

21. Research Institute on Mycology and Mycotoxicology, National Scientific and Technical Research Council, National University of Rio Cuarto, Rio Cuarto, Córdoba, Argentina

22. Department of Entomology and Plant Pathology, Auburn University, Auburn, AL 36849, U.S.A.

23. Broad Institute of Harvard and MIT, Cambridge, MA 02142, U.S.A.

24. Department of Medical Mycology and Infectious Diseases, Center of Expertise in Mycology, Radboud University Medical Center, Canisius Wilhelmina Hospital, Nijmegen, The Netherlands

25. Department of Plant Pathology, University of California, Davis, CA 95616, U.S.A.

26. Departamento de Fitopatologia, Universidade Federal de Viçosa, Viçosa, Brazil

27. Department of Mycology, Real Jardín Botánico CSIC, Madrid, Spain

28. Departamento de Genética, Campus de Excelencia Internacional Agroalimentario, Universidad de Córdoba, Córdoba, Spain

29. French National Institute for Agriculture, Food, and Environment (INRAE), Dijon, France

30. Department of Plant Pathology and Ecology, Connecticut Agricultural Experiment Station, New Haven, CT 06504, U.S.A.

31. Department of Biomedical Sciences for Health, University of Milano, Milan, Italy

32. Wye Research and Education Center, University of Maryland, Queenstown, MD 21658, U.S.A.

33. Laboratorio de Patología Vegetal, Instituto de Investigaciones Agropecuarias y Forestales, Universidad Michoacana de San Nicolás de Hidalgo, Tarímbaro, Michoacán 58880, México

34. Embrapa Amazônia Ocidental, Manaus, Brazil

35. Lethbridge Research and Development Centre, Agriculture and Agri-Food Canada, Lethbridge, Alberta T1J 4B1, Canada

36. Department of Biotechnology and Biomedicine, Technical University of Denmark, Lyngby, Denmark

37. Department of Plant Pathology and Weed Research, Agricultural Research Organization, Volcani Center, Rishon LeZion, Israel

38. Department of Biochemistry and Biophysics, Oregon State University, Corvallis, OR 97331, U.S.A.

39. Department of Microbiology and Immunology, University of Oklahoma Health Sciences Center, Oklahoma City, OK 73104, U.S.A.

40. Laboratory of Mycology and Phytopathology, All-Russian Institute of Plant Protection, St. Petersburg-Pushkin, Russia

41. CSIRO Agriculture and Food, St. Lucia, Australia

42. Toxicology and Mycotoxin Research Unit, USDA-ARS, Athens, GA 30605, U.S.A.

43. Department of Plant and Soil Sciences, University of Delaware, DE 19716, U.S.A.

44. Department of Genetics, University of the Free State, Bloemfontein, South Africa

45. Unitat de Microbiologia, Departament de Ciències Mèdiques Bàsiques, Universitat Rovira i Virgili, Reus, Spain

46. Department of Molecular Biology, Universidad de Leon, Leon, Spain

47. Department of Biointeractions and Crop Protection, Rothamsted Research, Harpenden, United Kingdom

48. Ottawa Research and Development Centre, Agriculture and Agri-Food Canada, Ottawa, Ontario K1A 0C6, Canada

49. MTA-SZTE Fungal Pathogenicity Mechanisms Research Group, Hungarian Academy of Sciences, University of Szeged, Szeged, Hungary

50. Institute of Plant Protection, Szent István University, Gödöllő, Hungary

51. Division of Mycology, Faculty of Medicine, University of Çukurova, Sarıçam, Adana, Turkey

52. Biosystematics Unit, Plant Health and Protection, Agricultural Research Council, Pretoria, South Africa

53. Department of Microbiology, Stellenbosch University, Matieland, South Africa

54. College of Plant Protection, Northwest Agriculture and Forestry University, Xianyang, People’s Republic of China

55. Division of Plant and Soil Sciences, West Virginia University, Morgantown, WV 26506, U.S.A.

56. Biology Department, St. Louis University, St. Louis, MO 63101, U.S.A.

57. USDA-ARS Cereal Disease Laboratory, University of Minnesota, St. Paul, MN 55108, U.S.A.

58. Department of Botany and Nature Protection, University of Warmia and Mazury in Olsztyn, Olsztyn, Poland

59. German National Reference Center for Invasive Fungal Infections NRZMyk, Leibniz Institute for Natural Product Research and Infection Biology, Hans Knoell Institute, Jena, Germany

60. Australian Institute of Botanical Science, Royal Botanic Garden and Domain Trust, Sydney, Australia

61. Microbial Safety Team, National Institute of Agricultural Sciences, Rural Development Administration, Wanju, Republic of Korea

62. Department of Agricultural Biotechnology, Seoul National University, Seoul, Republic of Korea

63. Department of Plant Pathology, Kansas State University, Manhattan, KS 66506, U.S.A.

64. Institute of Sciences of Food Production, Research National Council, Bari, Italy

65. Facultad de Ciencias Bioquímicas y Farmacéuticas, Centro de Referencia de Micología, Universidad Nacional de Rosario, Rosario, Argentina

66. Division of Biotechnology and Plant Health, Norwegian Institute of Bioeconomy Research, Høgskoleveien, Ås, Norway

67. Department of Biochemistry and Molecular Biology, University of Massachusetts, Amherst, MA 01003, U.S.A.

68. Crop Improvement and Protection Research Unit, ARS-USDA, Salinas, CA 93905, U.S.A.

69. Dipartimento di Agraria and Nucleo Ricerca Desertificazione, Università degli Studi di Sassari, Sassari, Italy

70. School of Biological Sciences, Universiti Sains Malaysia, Penang, Malaysia

71. Laboratoire de Mycologie, Service de Dermatologie, Centre Hospitalier Universitaire Vaudois, 1011 Lausanne, Switzerland

72. Department of Plant Pathology, Stellenbosch University, Matieland, South Africa

73. Brussels, Belgium

74. Department of Plant Pathology and Microbiology, Iowa State University, Ames, IA 50011, U.S.A.

75. Department of Crop Genetics, John Innes Centre, Norwich Research Park, Norwich, United Kingdom

76. Hospital Universitário, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

77. Department of Food, Environmental and Nutritional Sciences, University of Milano, Milan, Italy

78. Departamento de Fitopatologia, Universidade Federal de Lavras, Lavras, Minas Gerais State, Brazil

79. Institut Hospitalier Universitaire Méditerranée Infection, Aix Marseille University, Marseille, France

80. Mycology and Nematology Genetic Diversity and Biology Laboratory, USDA-ARS, Beltsville, MD 20705, U.S.A.

81. Swammerdam Institute for Life Science, University of Amsterdam, Amsterdam, The Netherlands

82. Department of Plant Pathology, University of Wisconsin, Madison, WI 53706, U.S.A.

83. Department of Plant Protection, College of Food and Agriculture Sciences, King Saud University, Riyadh 11451, Saudi Arabia

84. Department of Integrative Food, Bioscience and Biotechnology, Chonnam National University, Gwangju, Republic of Korea

85. Centre de Recherche et de Formation Agronomie, Haute Ecole Louvain en Hainaut, Montignies-sur-Sambre, Belgium

86. School of Plant and Environmental Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, U.S.A.

87. Amycel/Spawn Mate, San Juan Bautista, CA 95045, U.S.A.

88. Department of Ecological Plant Protection, University of Kassel, Witzenhausen, Germany

89. School of Forest Resources and Conservation, University of Florida, Gainesville, FL 32611, U.S.A.

90. Department of Biological Sciences, Binghamton University, State University of New York, Binghamton, NY 13902, U.S.A.

91. Department of Microbiology and Plant Pathology, University of California, Riverside, CA 92521, U.S.A.

92. Agroécologie, AgroSup Dijon, INRAE, University of Bourgogne Franche-Comté, Dijon, France

93. Life Science Research Center, Gifu University, Gifu, Japan

94. Department of Plant Pathology, University of Kentucky, Lexington, KY 40546, U.S.A.

95. Department of Biology, Indiana University, Bloomington, IN 47405, U.S.A.

96. Department of Botany and Plant Biotechnology, University of Johannesburg, Auckland Park, South Africa

97. Department of Microbial Biochemical and Food Biotechnology, University of the Free State, Bloemfontein, South Africa

98. DOE Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94702.

99. Department of Microbiology, Immunology and Molecular Genetics, University of Texas Health Science Center, San Antonio, TX 78229, U.S.A.

100. Department of Pathology, University of Texas Health Science Center, San Antonio, TX 78229, U.S.A.

101. Department of Biochemistry, University of Turku, Turku, Finland

102. Department of Medical Biotechnology, Soonchunhyang University, Asan, Republic of Korea

103. Department of Plant Biology, Rutgers University, New Brunswick, NJ 08901, U.S.A.

104. Department of Pathology, Johns Hopkins University, Baltimore, MD 21287, U.S.A.

Abstract

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.

Funder

U.S. Department of Agriculture Agricultural Research Service (USDA-ARS) National Program for Food Safety

National Science Foundation

Pennsylvania State Agricultural Experiment Station

Oak Ridge Institute for Science and Education

Publisher

Scientific Societies

Subject

Plant Science,Agronomy and Crop Science

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