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Defining a species in fungal plant pathology: beyond the species level

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Abstract

In plant pathology, the correct naming of a species is essential for determining the causal agents of disease. Species names not only serve the general purpose of concise communication, but also are critical for effective plant quarantine, preventing the introduction of new pathogens into a territory. Many phytopathogenic genera have multiple species and, in several genera, disagreements between the multiple prevailing species concept definitions result in numerous cryptic species. Some of these species were previously called by various names; forma speciales (specialised forms), subspecies, or pathotypes. However, based on new molecular evidence they are being assigned into new species. The frequent name changes and lack of consistent criteria to delineate cryptic species, species, subspecies, forms, and races create increasing confusion, often making communication among biologists arduous. Furthermore, such ambiguous information can convey misleading evolutionary concepts and species boundaries. The aim of this paper is to review these concepts, clarify their use, and evaluate them by referring to existing examples. We specifically address the question, “Do plant pathogens require a different ranking system?” We conclude that it is necessary to identify phytopathogens to species level based on data from multiple approaches. Furthermore, this identification must go beyond species level to clearly classify hitherto known subspecies, forms and races. In addition, when naming phytopathogenic genera, plant pathologists should provide more information about geographic locations and host ranges as well as host specificities for individual species, cryptic species, forms or races. When describing a new phytopathogen, we suggest that authors provide at least three representative strains together with pathogenicity test results. If Koch’s postulates cannot be fulfilled, it is necessary to provide complementary data such as associated disease severity on the host plant. Moreover, more sequenced collections of species causing diseases should be published in order to stabilise the boundaries of cryptic species, species, subspecies, forms, and races.

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References

  • Ashu EE, Xu J (2015) The roles of sexual and asexual reproduction in the origin and dissemination of strains causing fungal infectious disease outbreaks. Infect Genet Evol 36:199–209

    Article  PubMed  Google Scholar 

  • Avelino J, Cristancho M, Georgiou S, Imbach P, Aguilar L, Bornemann G, Läderach P, Anzueto F, Hruska AJ, Morales C (2015) The coffee rust crises in Colombia and Central America (2008–2013): impacts, plausible causes and proposed solutions. Food Secur 7:303–321

    Article  Google Scholar 

  • Bán R, Kovács A, Körösi K, Perczel M, Turóczi G (2014) First report on the occurrence of a new pathotype, 714, of Plasmopara halstedii (sunflower downy mildew) in Hungary. Plant Dise 98:1580–1580

    Article  Google Scholar 

  • Bickford D, Lohman DJ, Sodhi NS, Peter KLN, Meier R, Winker K, Krista K, Indraneil Das I (2007) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22:148–155

    Article  PubMed  Google Scholar 

  • Bordewich M, Deutschmann IM, Fischer M, Kasbohm E, Semple C, Steel M (2018) On the information content of discrete phylogenetic characters. J Math Biol 77:527–544

    Article  PubMed  Google Scholar 

  • Bruen TC, Philippe H, Bryant D (2006) A simple and robust statistical test for detecting the presence of recombination. Genetics 172:2665–2681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burgess LW, Nelson PE, Toussoun TA, Forbes GA (1988) Distribution of Fusarium species in sections Roseum, Arthrosporiella, Gibbosum and Discolor recovered from grassland, pasture and pine nursery soils of Eastern Australia. Mycologia 80:815–824

    Article  Google Scholar 

  • Cai L, Hyde KD, Taylor PWJ, Weir BS, Waller JM, Abang MM, Zhang JZ, Yang YL, Phoulivong S, Liu ZY, Prihastuti H, Shivas RG, McKenzie EHC, Johnston PR (2009) A polyphasic approach for studying Colletotrichum. Fungal Divers 39:183–204

    Google Scholar 

  • Cannon PF, Damm U, Johnston PR, Weir BS (2012) Colletotrichum: current status and future directions. Stud Mycol 73:181–213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cantino DP, Bryant HN, Queiroz KD, Donoghue MJ, Eriksson T, Hillis DM, Michael S, Lee Y (1999) Species names in phylogenetic nomenclature. Syst Biol 48:790–807

    Article  CAS  PubMed  Google Scholar 

  • Chenuil A, Cahill AE, Délémontey N, Salliant Du, du Luc E, Fanton H (2019) Problems and questions posed by cryptic species. A Framework to Guide Future Studies 24:77–106

    Google Scholar 

  • Crespo A, Lumbsch HT (2010) Cryptic species in lichen-forming fungi. IMA Fungus 1:167–170

    Article  PubMed  PubMed Central  Google Scholar 

  • Crouch JA (2014) Colletotrichum caudatum is a species complex. IMA Fungus 5:17–30

    Article  PubMed  PubMed Central  Google Scholar 

  • Crous PW, Groenewald JZ (2005) Hosts, species and genotypes: opinions versus data. Australas Plant Pathol 34:463–470

    Article  Google Scholar 

  • Czembor E, Stępień Ł, Waśkiewicz A (2014) Fusarium temperatum as new species causing ear rot on maize in Poland. Plant Dis 98:1001

    Article  CAS  PubMed  Google Scholar 

  • Dvořák P, Poulíčková A, Hašler P, Belli M, Casamatta DA, Papini A (2015) Species concepts and speciation factors in cyanobacteria, with connection to the problems of diversity and classification. Biodivers Conserv 24:739–757

    Article  Google Scholar 

  • Edel-Hermann V, Lecomte C (2019a) Current status of Fusarium oxysporum formae speciales and races. Phytopathol 109:512–530

    Article  CAS  Google Scholar 

  • Dayarathne MC, Boonmee S, Braun U, Crous PW, Daranagama DA, Dissanayake AJ, Ekanayaka H, Jayawardena R, Jones EBG, Maharachchikumbura SSN, Perera RH, Phillips AJL, Stadler M, Thambugala KM, Wanasinghe DN, Zhao Q, Hyde KD, Jeewon R (2016) Taxonomic utility of old names in current fungal classification and nomenclature: Conflicts, confusion & clarifications. Mycosphere 7:1622–1648

    Article  Google Scholar 

  • de Labrouhe DT, Walser P, Jolivot D, Roche S, Serre F, Leguillon M, Delmotte F, Bordat A, Godiard L, Vincourt P, Vear F (2012) Proposal for improvement of sunflower downy mildew race nomenclature. In: Proceedings of the 18th International Sunflower Conference, Mar del Plata pp. 322 –327.

  • De Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56:879–886

    Article  PubMed  Google Scholar 

  • Dettman JR, Jacobson DJ, Taylor JW (2003) a multilocus genealogical approach to phylogenetic species recognition in the model eukaryote neurospora. Evolution (NY) 57:2703

    Google Scholar 

  • Dugan FM, Everhart S (2016) Cryptic species: a leitmotif of contemporary mycology has challenges and benefits for plant pathologists. Plant Heal Prog 17:250–253

    Article  Google Scholar 

  • Dykhuizen DE, Green L (1991) Recombination in Escherichia coli and the definition of biological species. J Bacteriol 173:7257–7268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edel-Hermann V, Lecomte C (2019b) Current status of Fusarium oxysporum Formae Speciales and races. Phytopathology 109:512–530

    Article  CAS  PubMed  Google Scholar 

  • Fan J, Urban M, Parker JE, Brewer HC, Kelly SL, Hammond-Kosack KE, Fraaije BA, Liu X, Cools HJ (2013) Characterization of the sterol 14α-demethylases of Fusarium graminearum identifies a novel genus-specific CYP51 function. New Phytol 198:821–835

    Article  CAS  PubMed  Google Scholar 

  • Fang X, Snell P, Barbetti MJ, Lanoiselet V (2017) Races of Magnaporthe oryzae in Australia and genes with resistance to these races revealed through host resistance screening in monogenic lines of Oryza sativa. Eur J Plant Pathol 148:647–656

    Article  Google Scholar 

  • Frisvad JC, Samson RA (2004) Polyphasic taxonomy of Penicillium subgenus Penicillium : a guide to identification of food and air-borne terverticillate penicillia and their mycotoxins. Stud Mycol 49:1–173

    Google Scholar 

  • Gao YH, Sun W, Su YY, Cai L (2014) Three new species of Phomopsis in Gutianshan nature reserve in China. Mycol Prog 13:111–121

    Article  Google Scholar 

  • Gao Y, Liu F, Duan W, Crous PW, Cai L (2017) IMA Fungus 8:153–187

    Article  PubMed  PubMed Central  Google Scholar 

  • Gascuel Q, Martinez Y, Boniface MC, Vear F, Pichon M, Godiard L (2015) The sunflower downy mildew pathogen Plasmopara halstedii. Mol Plant Pathol 16:109–122

    Article  PubMed  Google Scholar 

  • Geber J, Murphy E (2012) Scurvy in the great irish famine: evidence of vitamin c deficiency from a mid-19th century skeletal population. Am J Phys Anthropol 148:512–524

    Article  PubMed  PubMed Central  Google Scholar 

  • Geiser DM, Aoki T, Bacon CW, Baker SE, Bhattacharyya MK, Brandt ME, Brown DW, Burgess LW, Chulze S, Coleman JJ, Correll JC, Covert SF, Crous PW, Cuomo CA, De Hoog GS, Di Pietro A, Elmer WH, Epstein L, Frandsen RJ, Freeman S, Gagkaeva T, Glenn AE, Gordon TR, Gregory NF, Hammond-Kosack KE, Hanson LE, Jímenez-Gasco Mdel M, Kang S, Kistler HC, Kuldau GA, Leslie JF, Logrieco A, Lu G, Lysøe E, Ma LJ, McCormick SP, Migheli Q, Moretti A, Munaut F, O’Donnell K, Pfenning L, Ploetz RC, Proctor RH, Rehner SA, Robert VA, Rooney AP, Bin Salleh B, Scandiani MM, Scauflaire J, Short DP, Steenkamp E, Suga H, Summerell BA, Sutton DA, Thrane U, Trail F, Van Diepeningen A, Vanetten HD, Viljoen A, Waalwijk C, Ward TJ, Wingfield MJ, Xu JR, Yang XB, Yli-Mattila T, Zhang N (2013) One fungus, one name: defining the genus Fusarium in a scientifically robust way that preserves longstanding use. Phytopathol 103:400–408

    Article  Google Scholar 

  • Geiser DM, Al-Hatmi A, Aoki T, Arie T, Balmas V, Barnes I, Bergstrom GC, Bhattacharyya MKK, Blomquist CL, Bowden R, Brankovics B, Brown DW, Burgess LW, Bushley K, Busman M, Cano-Lira JF, Carrillo JD, Chang HX, Chen CY, Chen W, Chilvers MI, Chulze SN, Coleman JJ, Cuomo CA, de Beer ZW, de Hoog GS, Del Castillo-Múnera J, Del Ponte E, Diéguez-Uribeondo J, Di Pietro A, Edel-Hermann V, Elmer WH, Epstein L, Eskalen A, Esposto MC, Everts KL, Fernández-Pavía SP, da Silva GF, Foroud NA, Fourie G, Frandsen RJN, Freeman S, Freitag M, Frenkel O, Fuller KK, Gagkaeva T, Gardiner DM, Glenn AE, Gold S, Gordon T, Gregory NF, Gryzenhout M, Guarro J, Gugino B, Gutiérrez S, Hammond-Kosack K, Harris LJ, Homa M, Hong CF, Hornok L, Huang JW, Ilkit M, Jacobs A, Jacobs K, Jiang C, Jimenez-Gasco MDM, Kang S, Kasson MT, Kazan K, Kennell JC, Kim H, Kistler HC, Kuldau GA, Kulik T, Kurzai O, Laraba I, Laurence MH, Lee TY, Lee YW, Lee YH, Leslie JF, Liew ECY, Lofton LW, Logrieco A, Sánchez López-Berges M, Luque AG, Lysøe E, Ma LJ, Marra RE, Martin FN, May SR, McCormick S, McGee CT, Meis JF, Migheli Q, Mohamed Nor NMI, Monod M, Moretti A, Mostert D, Mulé G, Munaut F, Munkvold GP, Nicholson P, Nucci M, O'Donnell K, Pasquali M, Pfenning LH, Prigitano A, Proctor R, Ranque S, Rehner S, Rep M, Rodríguez-Alvarado G, Rose LJ, Roth MG, Ruiz-Roldán C, Saleh AA, Salleh B, Sang H, Scandiani M, Scauflaire J, Schmale D 3rd, Short DP, Šišić A, Smith J, Smyth CW, Son H, Spahr E, Stajich JE, Steenkamp E, Steinberg C, Subramaniam R, Suga H, Summerell BA, Susca A, Swett CL, Toomajian C, Torres-Cruz TJ, Tortorano AM, Urban M, Vaillancourt LJ, Vallad GE, van der Lee T, Vanderpool D, van Diepeningen AD, Vaughan M, Venter E, Vermeulen M, Verweij PE, Viljoen A, Waalwijk C, Wallace EC, Walther G, Wang J, Ward T, Wickes B, Wiederhold NP, Wingfield MJ, Wood AKM, Xu JR, Yang XB, Yli-Matilla T, Yun SH, Zakaria L, Zhang H, Zhang N, Zhang S, Zhang X (2020) Phylogenomic analysis of a 55.1 kb 19-gene dataset resolves a monophyletic Fusarium that includes the Fusarium solani Species Complex. Phytopathology doi: https://doi.org/10.1094/PHYTO-08-20-0330-LE.

    Article  Google Scholar 

  • Geiser DM, Jimenez-Gasco MDM, Kang S, Makalowska I, Veeraraghavan N, Ward TJ, Zhang N, Kuldau GA, O’Donnell K (2004) FUSARIUM-ID v. 1.0: A DNA sequence database for identifying Fusarium. Euro J Plant Pathol 110:473–479

    Article  CAS  Google Scholar 

  • Gilbert AS, Wheeler RT, May RC (2015) Fungal pathogens: survival and replication within macrophages. Cold Spring Harb Perspect Med 5:019661

    Article  CAS  Google Scholar 

  • Gladieux P, De Bellis F, Hann-Soden C, Svedberg J, Johannesson H, Taylor JW (2020) Neurospora from natural populations: Population genomics insights into the Life history of a model microbial Eukaryote. In: Statistical population genomics Humana, New York, NY pp. 313–336.

  • Groenewald JZ, Nakashima C, Nishikawa J, Shin HD, Park JH, Groenewald M, Braun U, Crous PW (2013) Species concepts in Cercospora: spotting the weeds among the roses. Stud Mycol 75:115–170

    Article  CAS  PubMed  Google Scholar 

  • Guarnaccia V, Groenewald JZ, Woodhall J, Armengol J, Cinelli T, Eichmeier A (2018) Diaporthe diversity and pathogenicity revealed from a broad survey of grapevine diseases in Europe. Persoonia 40, 135–153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guarro J, Gené J, Stchigel AM (1999) Developments in fungal taxonomy. Clin Microbiol Rev 12:454–500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hawksworth D (2011) A new dawn for the naming of fungi: impacts of decisions made in Melbourne in July 2011 on the future publication and regulation of fungal names. MycoKeys 1:7–20

    Article  Google Scholar 

  • Hennig W (1966) Phylogenetic systematics. University of Illinois Press, Urbana

    Google Scholar 

  • Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267

    Article  CAS  PubMed  Google Scholar 

  • Hyde KD, Chomnunti P, Crous PW, Groenewald JZ, Damm U, Ko TW, Shivas RG, Summerell BA, Tan YP (2010) A case for re-inventory of Australia’s plant pathogens. Persoonia 25:50–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hyde KD, Jeewon R, Chen YJ, Bhunjun CS, Calabon MS, Jiang HB, Lin CG, Norphanphoun C, Sysouphanthong P, Pem D, Tibpromma S, Zhang Q, Doilom M, Jayawardena RS, Liu JK, Maharachchikumbura SSN, Phukhamsakda C, Phookamsak R, Al-Sadi AM, Thongklang N, Wang Y, Gafforov Y, Jones EBG, Lumyong S (2020) The numbers of fungi: is the descriptive curve flattening? Fungal Divers 103:219–271

    Article  Google Scholar 

  • Hyde KD, Nilsson RH, Alias SA, et al. (2014). One stop shop: backbones trees for important phytopathogenic genera: I. Fungal Diversity 67: 21–125.

    Article  Google Scholar 

  • Jayawardena RS, Hyde KD, Chen YJ, Papp V, Palla B, Papp D, Bhunjun CS, Hurdeal VG, Senwanna C, Manawasinghe IS, Harischandra DL, Gautam AK, Avasthi S, Chuankid B, Goonasekara ID, Hongsanan S, Zeng XY, Liyanage KK, Liu NG, Karunarathna A, Hapuarachchi KK, Luangharn T, Raspé O, Brahmanage R, Doilom M, Lee HB, Mei L, Jeewon R, Huanraluek N, Chaiwan N, Stadler M, Wang Y (2020) One stop shop IV: taxonomic update with molecular phylogeny for important phytopathogenic genera: 76–100. Fungal Divers 103:87–218

    Article  Google Scholar 

  • Jones DR, Baker RHA (2007) Introductions of non-native plant pathogens into Great Britain. Plant Pathol 56:891–910

    Article  Google Scholar 

  • Judson OP, Normark BB (1996) Ancient asexual scandals. Trends Ecol Evol 11:41–46

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Filipski AJ, Battistuzzi FU, Pond SL, Tamura K (2012) Statistics and truth in phylogenomics. Mol Biol Evol 29:457–472

    Article  CAS  PubMed  Google Scholar 

  • Laurence MH, Summerell BA, Burgess LW, Liew EC (2014) Genealogical concordance phylogenetic species recognition in the Fusarium oxysporum species complex. Fungal Biol 118:374–384

    Article  PubMed  Google Scholar 

  • Leslie JF, Summerell BA (2006) The Fusarium laboratory manual. Blackwell Publishing, Ames

    Book  Google Scholar 

  • Liang LY, Jiang N, Chen WY, Liang YM, Tian CM (2019) Botryosphaeria qinlingensis sp. nov. causing oak frogeye leaf spot in China. Mycotaxon 134:463–473

    Article  Google Scholar 

  • Li F, Upadhyaya NM, Sperschneider J, Matny O, Nguyen-Phuc H, Mago R, Raley C, Miller ME, Silverstein KA, Henningsen E, Hirsch CD (2019) Emergence of the Ug99 lineage of the wheat stem rust pathogen through somatic hybridisation. Nat Commun 10:1–15

    Article  CAS  Google Scholar 

  • Liu F, Wang M, Damm U, Crous PW, Cai L (2016) Species boundaries in plant pathogenic fungi: a Colletotrichum case study. BMC Evol Biol 16:81. https://doi.org/10.1186/s12862-016-0649-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luchi N, Ioos R, Santini A (2020) Fast and reliable molecular methods to detect fungal pathogens in woody plants. Appl microbiol and biotechn 104:2453–2468

  • Lücking R, Aime MC, Robbertse B, Miller AN, Ariyawansa HA, Aoki T, Cardinali G, Crous PW, Druzhinina IS, Geiser DM, Hawksworth DL, Hyde KD, Irinyi L, Jeewon R, Johnston PR, Kirk PM, Malosso E, May TW, Meyer W, Öpik M, Robert V, Stadler M, Thines M, Vu D, Yurkov AM, Zhang N, Schoch CL (2020) Unambiguous identification of fungi: where do we stand and how accurate and precise is fungal DNA barcoding? IMA Fungus 11:14–46

    Article  PubMed  PubMed Central  Google Scholar 

  • Manawasinghe IS, Zhang W, Li X, Zhao W, Chethana KT, Xu J, Chen Z, Dissanayaka AJ, Mugnai L, Úrbez-Torres JR, Savocchia S (2018) Novel microsatellite markers reveal multiple origins of Botryosphaeria dothidea causing the Chinese grapevine trunk disease. Fungal Ecol 33, 134–142

    Article  Google Scholar 

  • McNeill J, Barrie FR, Buck R, Demoulin V, Greuter W, Hawksworth DL, Herendeen PS, Knapp S, Marhold K, Prado J, Prud'homme Van Reine WF, Smith GF, Wiersema JH (2012) International Code of Nomenclature for algae, fungi, and plants (Melbourne Code) Regnum Vegetabile 154. ISBN 978-3-87429-425-6 http://www.iapt-taxon.org/nomen/main.php

  • Maharachchikumbura SSN, Hyde KD, Groenewald JZ, Xu J, Crous PW (2014) Pestalotiopsis revisited. Stud Mycol 79:121–186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manawasinghe IS, Dissanayake A, Liu M, Wanasinghe D, Xu J, Zhao W, Wei Z, Zhou Y, Hyde KD, Brooks S, Yan J (2019) High genetic diversity and species complexity of Diaporthe associated with grapevine dieback in China. Front Microbiol 10:1936

    Article  PubMed  PubMed Central  Google Scholar 

  • Manawasinghe IS, Phillips AJL, Hyde KD, Chethana KWT, Zhang W, Zhao WS, Yan JY, Li XH (2016) Mycosphere Essays 14: assessing the aggressiveness of plant pathogenic Botryosphaeriaceae. Mycosphere 7:883–892

    Article  Google Scholar 

  • Mallet J (2007) Subspecies, semispecies, superspecies. Encyclopedia Biodivers 5:523–526

    Google Scholar 

  • Marcelino VR, Irinyi L, Eden JS, Meyer W, Holmes EC, Sorrell TC (2019) Metatranscriptomics as a tool to identify fungal species and subspecies in mixed communities–a proof of concept under laboratory conditions. IMA Fungus 10:1–10

    Article  Google Scholar 

  • McCook S (2006) Global rust belt: Hemileia vastatrix and the ecological integration of world coffee production since 1850. J Glob Hist 1:177–195

    Article  Google Scholar 

  • McCook S, Vandermeer J (2015) The Big Rust and the red queen: long-term perspectives on coffee rust research. Phytopathology 105:1164–1173

    Article  CAS  PubMed  Google Scholar 

  • McDonald B (2004) Population genetics of plant pathogens. The Plant Health Instructor. https://doi.org/10.1094/PHI-A-2004-0524-01

    Article  Google Scholar 

  • Mayr E (1942) Systematics and the origin of species. Columbia University Press, New York

    Google Scholar 

  • Mayr E (1982) Of what use are subspecies? Auk 99:593–595

    Google Scholar 

  • Milgroom MG (2017) . Population biology of plant pathogens: genetics, ecology, and evolution. The American Phytopathological Society.

    Book  Google Scholar 

  • Morse SS (2001) Factors in the emergence of infectious diseases. Plagues Politics 4:8–26

    Article  Google Scholar 

  • Nieuwenhuis BP, James TY (2016a) The frequency of sex in fungi. Philoso Trans R Soc B 371:20150540

    Article  CAS  Google Scholar 

  • Nguyen HGT, Jančič S, Meijer M, Tanney JB, Zalar P, Gunde-Cimerman N, Seifert KA (2015) Correction: application of the phylogenetic species concept to wallemia sebi from house dust and indoor air revealed by multi-locus genealogical concordance. PLoS ONE 10:e0129752

    Article  CAS  Google Scholar 

  • Nieuwenhuis BPS, James TY (2016b) The frequency of sex in fungi. Philos Trans R Soc B 371:20150540

    Article  CAS  Google Scholar 

  • O’Donnell K, Cigelnik E, Nirenberg HI (1998) Molecular systematics and phylogeography of the Gibberella fujikuroi species complex. Mycologia 90:465–493

    Article  Google Scholar 

  • O’Donnell K, Ward TJ, Aberra D, Kistler HC, Aoki T, Orwig N, Kimura M, Bjørnstad S, Klemsdal SS (2008) Multilocus genotyping and molecular phylogenetics resolve a novel head blight pathogen within the Fusarium graminearum species complex from Ethiopia. Fungal Genet Biol 45:1514–1522

    Article  CAS  PubMed  Google Scholar 

  • O’Donnell K, Ward TJ, Geiser DM, Kistler HC, Aoki T (2004) Genealogical concordance between the mating type locus and seven other nuclear genes supports formal recognition of nine phylogenetically distinct species within the Fusarium graminearum clade. Fungal Genet Biol 41:600–623

    Article  PubMed  CAS  Google Scholar 

  • O’Donnell K, Rooney AP, Proctor RH, Brown DW, McCormick SP, Ward TJ, Frandsen RJN, Lysøe E, Rehner SA, Aoki T, Robert VARG, Crous PW, Groenewald JZ, Kang S, Geiser DM (2013) RPB1 and RPB2 phylogeny supports an early Cretaceous origin and a strongly supported clade comprising all agriculturally and medically important fusaria. Fungal Genet Biol 52:20–31

    Article  CAS  PubMed  Google Scholar 

  • O’Donnell K, Ward TJ, Robert VARG, Crous PW, Geiser DM, Kang S (2015) DNA sequence-based identification of Fusarium: current status and future directions. Phytoparasitica 43:583–595

    Article  Google Scholar 

  • Oláh J, Andersen T, Beshkov S, Ciubuc C, Coppa G, Kovács T, Oláh J (2018) Unified phylogenetic species concept: taking subspecies and race out of science: postmodern theory applied to the Potamophylax cingulatus group (Trichoptera, Limnephilidae). Opuscula Zool (budapest) 49:33–70

    Article  Google Scholar 

  • Omotayo OP, Omotayo AO, Mwanza M, Babalola OO (2019) Prevalence of mycotoxins and their consequences on human health. Toxicol Res 35:1–7

    Article  CAS  PubMed  Google Scholar 

  • Paping R, Vanhaute E, O Grada C (eds) (2007) When the Potato Failed. Causes and Effects of the Last European Subsistence Crisis, 1845–1850. Brepols Publishers, Turnhout

  • Patten M (2009) Subspecies’ and “race” should not be used as synonyms. Nature 457:147

    Article  CAS  PubMed  Google Scholar 

  • Patten MA (2015) Subspecies and the philosophy of science. Auk 132:481–485

    Article  Google Scholar 

  • Phillips AJL, Alves A, Abdollahzadeh J, Slippers B, Wingfield MJ, JZ (2013) The Botryosphaeriaceae: genera and species known from culture. Stud Mycol 76:51–167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Proctor RH, McCormick SP, Alexander NJ, Desjardins AE (2009) Evidence that a secondary metabolite gene cluster has grown by gene relocation during evolution of the filamentous fungus Fusarium. Mol Microbiol 74:1128–1142

    Article  CAS  PubMed  Google Scholar 

  • Quaedvlieg W, Binder M, Groenewald JZ, Summerell BA, Carnegie AJ, Burgess TI, Crous PW (2014) Introducing the consolidated species concept to resolve species in the Teratosphaeriaceae. Persoonia Mol Phylogeny Evol Fungi 33:1–40

    Article  CAS  Google Scholar 

  • Rouxel M, Mestre P, Comont G, Lehman BL, Schilder A, Delmotte F (2013) Phylogenetic and experimental evidence for host-specialized cryptic species in a biotrophic oomycete. New Phytol 197:251–263

    Article  PubMed  Google Scholar 

  • Safran RJ, Nosil P (2012) Speciation: the origin of new species. Nat Educ Knowl 3:17

    Google Scholar 

  • Scauflaire J, Gourgue M, Munaut F (2011) Fusarium temperatum sp.nov. from maize, an emergent species closely related to Fusarium subglutinans. Mycologia 103:586–597

    Article  PubMed  Google Scholar 

  • Scholthof KBG (2007) The disease triangle: pathogens, the environment and society. Nat Rev Microbiol 5:152–156

    Article  CAS  PubMed  Google Scholar 

  • Shang Y, Xiao G, Zheng P, Cen K, Zhan S, Wang S (2016) Divergent and convergent evolution of fungal pathogenicity. Genome Biol Evol 8:1374–1387

    Article  PubMed  PubMed Central  Google Scholar 

  • Sharma M, Kulshrestha S (2015) Colletotrichum gloeosporioides: an anthracnose causing pathogen of fruits and vegetables. Biosci Biotechnol Res Asia 12(2):1233–1246

    Article  Google Scholar 

  • Singh RP, Hodson DP, Jin Y, Lagudah ES, Ayliffe MA, Bhavani S, Rouse MN, Pretorius ZA, Szabo LJ, Huerta-Espino J, Basnet BR (2015) Emergence and spread of new races of wheat stem rust fungus: continued threat to food security and prospects of genetic control. Phytopathol 105:872–884

    Article  Google Scholar 

  • Solarte F, Muñoz CG, Maharachchikumbura SSN, Álvarez E (2018) Diversity of Neopestalotiopsis and Pestalotiopsis spp., causal agents of guava scab in Colombia. Plant Dis 102:49–59

    Article  PubMed  Google Scholar 

  • Spring O, Thines M (2010) Molecular techniques for classification and diagnosis of plant pathogenic oomycota. In: Molecular identification of fungi. Springer, Berlin pp. 35–50.

  • Stępień Ł (2014) The use of Fusarium secondary metabolite biosynthetic genes in chemotypic and phylogenetic studies. Crit Rev Microbiol 40:176–185

    Article  PubMed  CAS  Google Scholar 

  • Stępień Ł, Chełkowski J (2010) Fusarium head blight of wheat: pathogenic species and their mycotoxins. World Mycotox J 3:107–119

    Article  CAS  Google Scholar 

  • Stępień Ł, Gromadzka K, Chełkowski J, Basińska-Barczak A, Lalak-Kańczugowska J (2019) Diversity and mycotoxin production by Fusarium temperatum and Fusarium subglutinans as causal agents of pre-harvest Fusarium maize ear rot in Poland. J Appl Gen 60:113–121

    Article  CAS  Google Scholar 

  • Stępień Ł, Koczyk G, Waśkiewicz A (2011) FUM cluster divergence in fumonisins-producing Fusarium species. Fungal Biol 115:112–123

    Article  PubMed  CAS  Google Scholar 

  • Stępień Ł, Waśkiewicz A, Wilman K (2015) Host extract modulates metabolism and fumonisin biosynthesis by the plant-pathogenic fungus Fusarium proliferatum. Int J Food Microbiol 193:74–81

    Article  PubMed  CAS  Google Scholar 

  • Storfer A, Alfaro ME, Ridenhour BJ, Jancovich JK, Mech SG, Parris MJ, Collins JP (2007) Phylogenetic concordance analysis shows an emerging pathogen is novel and endemic. Ecol Lett 10:1075–1083

    Article  PubMed  Google Scholar 

  • Struck TH, Feder JL, Bendiksby M, Birkeland S, Cerca J, Gusarov VI, Kistenich S, Larsson KH, Liow LH, Nowak MD, Stedje B, Bachmann L, Dimitrov D (2018) Finding evolutionary processes hidden in cryptic species. Trends Ecol Evol 33:153–163

    Article  PubMed  Google Scholar 

  • Subramanian S, Kumar S (2003) Neutral substitutions occur at a faster rate in exons than in noncoding DNA in primate genomes. Genom Res 13:838–844

    Article  CAS  Google Scholar 

  • Talhinhas P, Batista D, Diniz I, Vieira A, Silva DN, Loureiro A, Tavares S, Pereira AP, Azinheira HG, Guerra-Guimarães L, Várzea V, do Céu Silva M, (2017) The coffee leaf rust pathogen Hemileia vastatrix : one and a half centuries around the tropics. Mol Plant Pathol 18:1039–1051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor JW (2015) Evolutionary perspectives on human fungal pathogens. Cold Spring Harb Perspect Med 5:e019588

    Article  CAS  Google Scholar 

  • Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, Hibbett DS, Fishera MC (2000) Phylogenetic species recognition and species concepts in fungi. Fungal Genet Biol 31:21–32

    Article  CAS  PubMed  Google Scholar 

  • Thines M (2019) An evolutionary framework for host shiftsjumping ships for survival. New Phytol 224:605–617

    Article  PubMed  Google Scholar 

  • Thirkell TJ, Charters MD, Elliott AJ, Sait SM, Field KJ (2017) Are mycorrhizal fungi our sustainable saviours? Considerations for achieving food security. J Ecol 105:921–929

    Article  CAS  Google Scholar 

  • Udayanga D, Castlebury LA, Rossman AY, Chukeatirote E, Hyde KD (2014) Insights into the genus Diaporthe: phylogenetic species delimitation in the D. eres species complex. Fungal Divers 67:203–229

    Article  Google Scholar 

  • Udayanga D, Castlebury LA, Rossman AY, Chukeatirote E, Hyde KD (2015) The Diaporthe sojae species complex: Phylogenetic re-assessment of pathogens associated with soybean, cucurbits and other field crops. Fungal Biol 119:383–407

    Article  PubMed  Google Scholar 

  • Vakalounakis DJ, Wang Z, Fragkiadakis GA, Skaracis GN, Li DB (2004). Characterization of Fusarium oxysporum isolates obtained from cucumber in China by pathogenicity, VCG, and RAPD. Plant Disease, 88:645–649

    Article  CAS  PubMed  Google Scholar 

  • van Valen L (1976) Ecological species, multispecies and oaks. Taxon 25:233–239

    Article  Google Scholar 

  • Vieira WA, Lima WG, Nascimento ES, Michereff SJ, Câmara MP, Doyle VP (2017) The impact of phenotypic and molecular data on the inference of Colletotrichum diversity associated with Musa. Mycologia 109:912–934

    Article  CAS  PubMed  Google Scholar 

  • Wanasinghe DN, Phukhamsakda C, Hyde KD, Jeewon R, Lee HB, Jones EBG, Tibpromma S, Dissanayake AJ, Tennakoon DS, Jayasiri SC, Gafforov Y, Camporesi E, Bulgakov TS, Ekanayake AH, Perera RH, Samarakoon MC, Goonasekara ID, Mapook A, Li WJ, Senanayake IC, Li J, Norphanphoun C, Doilom M, Bahkali AH, Xu J, Mortimer PE, Tibell L, Tibell S, Karunarathna SC, (2018) Fungal diversity notes 709–839: taxonomic and phylogenetic contributions to fungal taxa with an emphasis on fungi on Rosaceae. Fungal Divers 89:1–236

    Article  Google Scholar 

  • Watanabe M, Yonezawa T, Lee KI, Kumagai S, Sugita-Konishi Y, Goto K, Hara-Kudo Y (2011) Molecular phylogeny of the higher and lower taxonomy of the Fusarium genus and differences in the evolutionary histories of multiple genes. BMC Evol Biol 11:322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weir BS, Johnston PR, Damm U (2012) The Colletotrichum gloeosporioides species complex. Stud Mycol 73:115–180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • WHO (2021) Mycotoxins are naturally occurring toxins,can be found in food & The adverse health effects of as immune deficiency and cancer. Accessed 20 Jan 2021.

  • Wingfield MJ, Wilhelm De Beer Z, Slippers B, Wingfield BD, Groenewald JZ, Lombard L, Crous PW (2012) One fungus, one name promotes progressive plant pathology. Mol Plant Pathol 13:604–613

    Article  CAS  PubMed  Google Scholar 

  • Wróbel B (2008) Statistical measures of uncertainty for branches in phylogenetic trees inferred from molecular sequences by using model-based methods. J Appl Genet 49:49–67

    Article  PubMed  Google Scholar 

  • Xu J (2002) Estimating the spontaneous mutation rate of loss of sex in the human pathogenic fungus Cryptococcus neoformans. Genetics 162:1157–1167

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu J (2020) Fungal species concepts in the genomics era. Genome 63:459–468

    Article  PubMed  Google Scholar 

  • Xu J (2004) Genotype-environment interactions of spontaneous mutations for vegetative fitness in the human pathogenic fungus Cryptococcus neoformans. Genetics 168:1177–1188

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu J (2016) Fungal DNA barcoding. Genome 59:913–932

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Li H, Zhou GY, Liu JA (2016) When do we call genetically distinct strains different species? A cautionary case study of the Colletotrichum gloesporioides species complex. Fungal Genom Biol 06:1–5

    Article  Google Scholar 

  • Zain ME (2011) Impact of mycotoxins on humans and animals. J Saudi Chem Soc 15:129–144

    Article  CAS  Google Scholar 

  • Zhang H, Luo W, Pan Y, Xu J, Xu JS, Chen WQ, Feng J (2014) First report of Fusarium temperatum causing fusarium ear rot on Maize in Northern China. Plant Dis 98:1273

    PubMed  Google Scholar 

  • Zhang W, Groenewald JZ, Lombard L, Schumacher RK, Phillips AJ, Crous PW (2020) Evaluating species in Botryosphaeriales. Persoonia 46:63–115

    Google Scholar 

  • Zhang W, Manawasinghe IS, Zhao W, Xu J, Brooks S, Zhao X, Hyde KD, Chethana KWT, Liu J, Li XH, Yan JY (2017) Multiple gene genealogy reveals high genetic diversity and evidence for multiple origins of Chinese Plasmopara viticola population. Sci Rep 7:17304

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhou Y, Dou Z, He W, Zhang X, Zhang Y (2016) Botryosphaeria sinensia sp nov., a new species from China. Phytotaxa 245:43–50

    Article  Google Scholar 

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Acknowledgements

We would like to thank the Thailand Research Fund, Grant RDG6130001 entitled “Impact of climate change on fungal diversity and biogeography in the Greater Mekong Subregion”. Kevin D Hyde thanks Chiang Mai University for the award of a Visiting Professor. Ishara S Manawasinghe thank Prof Marco Thines for guiding the development of this paper by providing valuable ideas and comments. Alan JL Phillips acknowledges the support from UIDB/04046/2020 and UIDP/04046/2020 Centre grants from FCT, Portugal (to BioISI).

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ISM and KDH conceived the basic idea. ISM, AJLP and JX developed the outline. ISM, ŁS, DLH, AK, wrote the manuscript. JW created the graphics in the manuscript. AJLP, JX, AB, MT, ŁS, KDH, JY, RC, ZD, ML, JW revised the manuscript. All authors read and approved the final manuscript.

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Correspondence to Kevin D. Hyde.

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Manawasinghe, I.S., Phillips, A.J.L., Xu, J. et al. Defining a species in fungal plant pathology: beyond the species level. Fungal Diversity 109, 267–282 (2021). https://doi.org/10.1007/s13225-021-00481-x

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