Epitypification of Fusarium oxysporum – clearing the taxonomic chaos

Abstract

Fusarium oxysporum is the most economically important and commonly encountered species of Fusarium. This soil-borne fungus is known to harbour both pathogenic (plant, animal and human) and non-pathogenic strains. However, in its current concept F. oxysporum is a species complex consisting of numerous cryptic species. Identification and naming these cryptic species is complicated by multiple subspecific classification systems and the lack of living ex-type material to serve as basic reference point for phylogenetic inference. Therefore, to advance and stabilise the taxonomic position of F. oxysporum as a species and allow naming of the multiple cryptic species recognised in this species complex, an epitype is designated for F. oxysporum. Using multi-locus phylogenetic inference and subtle morphological differences with the newly established epitype of F. oxysporum as reference point, 15 cryptic taxa are resolved in this study and described as species.

INTRODUCTION

Fusarium oxysporum is the most economically important and commonly encountered species of Fusarium. This soil-borne asexual fungus is known to harbour both pathogenic (plant, animal and human) and non-pathogenic strains (Leslie & Summerell 2006) and is also ranked fifth on a list of top 10 fungal pathogens based on scientific and economic importance (Dean et al. 2012, Geiser et al. 2013). Historically, F. oxysporum has been defined by the asexual phenotype as no sexual morph has yet been discovered, even though several studies have indicated the possible presence of a cryptic sexual cycle (Arie et al. 2000, Yun et al. 2000, Aoki et al. 2014, Gordon 2017). This is further supported by phylogenetic studies that place F. oxysporum within the Gibberella Clade (Baayen et al. 2000, O’Donnell et al. 2009, 2013). These studies also showed that F. oxysporum displays a complicated phylogenetic substructure, indicative of multiple cryptic species within F. oxysporum (Gordon & Martyn 1997, Laurence et al. 2014). As with other Fusarium species complexes, the F. oxysporum species complex (FOSC) has suffered from multiple taxonomic/classification systems applied in the past.

Diederich F.L. von Schlechtendal first introduced F. oxysporum in 1824, isolated from a rotten potato tuber (Solanum tuberosum) collected in Berlin, Germany. Wollenweber (1913) placed F. oxysporum within the section Elegans along with eight other Fusarium species and numerous varieties and forms based on similarity of the micro- and macroconidial morphology and dimensions. Snyder & Hansen (1940) later consolidated and reduced all species within the section Elegans into F. oxysporum and designated 25 special forms (formae speciales) within this species. These special forms were further expanded on by Gordon (1965) to 66, most of which are still used in literature today.

The use of special forms or formae speciales as subspecific rank in F. oxysporum classification has become common practice due to the broad morphological delineation of this species (Leslie & Summerell 2006). This informal subspecific rank is defined based on the plant pathogenicity of the particular F. oxysporum strain and excludes both clinical and non-pathogenic strains (Armstrong & Armstrong 1981, Gordon & Martyn 1997, Kistler 1997, Baayen et al. 2000, Leslie & Summerell 2006). Therefore, F. oxysporum strains attacking the same plant host are generally considered to belong to the same special form. Although this homologous trait has led to erroneous assumptions considering a specific special form to be phylogenetically monophyletic, several studies (O’Donnell et al. 1998, 2004, 2009, O’Donnell & Cigelnik 1999, Baayen et al. 2000, Lievens et al. 2009b, Van Dam et al. 2016) have highlighted the para- and polyphyletic relationships within several F. oxysporum special forms, e.g., F. oxysporum f. sp. batatas, F. oxysporum f. sp. cubense and F. oxysporum f. sp. vasinfectum. Additionally, several F. oxysporum special forms are able to infect and cause disease in more than one (sometimes unrelated) plant hosts, whereas others are highly specialised to a specific plant host (Armstrong & Armstrong 1981, Gordon & Martyn 1997, Kistler 1997, Baayen et al. 2000, Leslie & Summerell 2006, Fourie et al. 2011).

Naming F. oxysporum special forms are not subject to the International Code of Nomenclature for algae, fungi, and plants (ICN; McNeill et al. 2012, Thurland et al. 2018), and therefore no diagnosis (in Latin and/or English), nor the deposit of type material in a recognised repository is required. This decision was made due to the difficulty in accepting special forms within the Code, even though these strains are of great importance to plant pathologists and breeders (Deighton et al. 1962, Gordon 1965, Armstrong & Armstrong 1981). Several studies on F. oxysporum indicate that between 70 to over 150 special forms are known in F. oxysporum (Booth 1971, Armstrong & Armstrong 1981, Kistler 1997, Baayen et al. 2000, Leslie & Summerell 2006, Lievens et al. 2008, O’Donnell et al. 2009, Fourie et al. 2011, Laurence et al. 2014, Gordon 2017). At present Index Fungorum (http://www.indexfungorum.org/) lists 124 special forms in F. oxysporum, whereas MycoBank (http://www.mycobank.org/) list 127 special forms. Further careful scrutiny of literature revealed that 144 special forms have been named until February 2018 (Table 1). Although the special forms concept of Snyder & Hansen (1940) is still applied today, additional subspecific classification systems for special forms of F. oxysporum have also been introduced, which include haplotypes, races and vegetative compatibility groups (VCGs).

Table 1.

List of known special forms of Fusarium oxysporum.

formae speciales	Description	Synonym(s)	Listed	Race(s)	VCG(s)	Molecular studies
adzukicola	Kitazawa & Yanagita 1984, 1989		Summerell et al. 2010		Katan & Di Primo 1999
aechmeae	Sauthoff & Gerlach 1957, 1958	Fusarium bulbigenum f. aechmeae Sauthoff & Gerlach, Gratenwelt 57: 390. 1957	Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010			Gherbawy 1999, O’Donnell et al. 2009
albedinis	Sergent & Beguet 1921, Killian & Maire 1930, Malençon 1934, Louvet & Toutain 1981	Cylindrophora albedinis Kill. & Maire, Bull. Soc. Hist. Nat. Afrique N. 21: 89–101. 1930 Fusarium albedinis (Kill. & Maire) Malençon, Compt. Rend. Acad. Sci. 198: 1259–1261. 1930 Fusarium oxysporum var. albedinis (Kill. & Maire) Malençon, Rev. Mycol. (Paris) 15: 45–60. 1950	Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010		Tantaoui et al. 1996, Kistler et al. 1998, Katan 1999	Tantaoui & Boisson 1991, Tantaoui & Fernandez 1993 Tantaoui et al. 1996, Fernandez et al. 1994, 1998, Skovgaard et al. 2001, Mbofung et al. 2007, Lievens et al. 2008, O’Donnell et al. 2009, Elliott et al. 2010, Mirtalebi & Banihashemi 2014
aleuritis	Suelong 1981		Suelong 1981
allii	Matuo et al. 1979				Yoo et al. 1993, Katan & Di Primo 1999	O’Donnell et al. 2009
amaranthi	Chen & Swart 2001		Summerell et al. 2010		Chen & Swart 2001	Chen & Swart 2001
anethi	Janson 1951, Gordon 1965		Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010
anoectochili	Huang et al. 2014		Huang et al. 2014	Huang et al. 2014		Huang et al. 2014
apii	Snyder & Hansen 1940	Fusarium apii P.E. Nelson & Sherb., Tech. Bull. Mich. Agric. Exp. Sta. 155: 42. 1937 Fusarium oxysporum f. apii (P.E. Nelson & Sherb.) W.C. Snyder & H.N. Hansen, Amer. J. Bot. 27: 66. 1940 Fusarium bulbigenum var. apii (P.E. Nelson & Sherb.) Raillo, Fungi of the genus Fusarium: 250. 1950 Fusarium apii var. pallidum P.E. Nelson & Sherb., Tech. Bull. Mich. Agric. Exp. Sta. 155: 42. 1937	Snyder & Hansen 1940, Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010	Schneider & Norelli 1981, Puhalla 1984a, b, Epstein et al. 2017	Puhalla 1984a, b, Correll et al. 1986, 1987, Toth & Lacy 1991, Kistler et al. 1998, Katan 1999	Wang et al. 2001, O’Donnell et al. 2009, Chakrabarti et al. 2011, Epstein et al. 2017
arctii	Matuo et al. 1975		Summerell et al. 2010			O’Donnell et al. 2009
asparagi	Cohen 1946		Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010		Blok & Bollen 1997, Elmer & Stephens 1989, Yoo et al. 1993, Kistler et al. 1998, Katan 1999, Katan & Di Primo 1999	Baayen et al. 2000, Mbofung et al. 2007, O’Donnell et al. 2009, Poli et al. 2012, Mirtalebi & Banihashemi 2014
basilica	Dzidzariya 1968, Armstrong & Armstrong 1981	Fusarium oxysporum var. basilicum Dzidzariya, Pishch. Prom. SSR: 129–140. 1968	Armstrong & Armstrong 1968, 1981, Summerell et al. 2010		Elmer et al. 1994, Kistler et al. 1998, Katan 1999, Katan & Di Primo 1999	Chiocchetti et al. 1999, 2001, Pasquali et al. 2006, Lievens et al. 2008, O’Donnell et al. 2009
batatas	Wollenweber 1914, 1931	Fusarium batatas Wollenw., J. Agric. Res. 2: 268. 1914 Fusarium bulbigenum var. batatas (Wollenw.) Wollenw., Z. Parasitenk. (Berlin) 3: 414. 1931 Fusarium oxysporum f. batatas (Wollenw.) W.C. Snyder & H.N. Hansen, Amer. J. Bot. 27: 66. 1940	Snyder & Hansen 1940, Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010	Armstrong & Armstrong 1958b, 1968, Booth 1971	Katan 1999, Katan & Di Primo 1999	O’ Donnell et al. 1998, Kim et al. 2001, Mbofung et al. 2007, Lievens et al. 2009b, O’Donnell et al. 2009, Pinaria et al. 2015
benincasae	Gerlagh & Ester 1985			Gerlagh & Blok 1988
betae	Stewart 1931	Fusarium conglutinans var. betae D. Stewart, Phytopathology 9: 59. 1931 Fusarium orthoceras var. betae (D. Stewart) Padwick, Indian J. Agric. Sci. 10: 282. 1940 Fusarium oxysporum f. betae (D. Stewart) W.C. Snyder & H.N. Hansen, Amer. J. Bot. 27: 66. 1940 Fusarium oxysporum var. orthoceras (Appel & Wollenw.) Bilaǐ, The Fusaria: 282. 1955	Snyder & Hansen 1940, Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010	Armstrong & Armstrong 1976	Harveson & Rush 1997, Kistler et al. 1998, Webb et al. 2013	Cramer et al. 2003, Nitschke et al. 2009, O’Donnell et al. 2009, Hill et al. 2011, Covey et al. 2014
bouvardiae	Marziano et al. 1987					O’Donnell et al. 2009
brassica	Williams et al. 2016					Williams et al. 2016
callistephi	Beach 1918	Fusarium conglutinans var. callistephi Beach, Rep. Michigan Acad. Sci. 29: 297. 1918 Fusarium orthoceras var. callistephi (Beach) Padwick, Indian J. Agric. Sci. 10: 283. 1940 Fusarium oxysporum f. callistephi (Beach) W.C. Snyder & H.N. Hansen, Amer. J. Bot. 27: 66. 1940 Fusarium conglutinans var. majus Wollenw., Fusaria Autographica Delineata 3: 981. 1930	Snyder & Hansen 1940, Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010	Armstrong & Armstrong 1971		Mbofung et al. 2007, O’Donnell et al. 2009, Poli et al. 2012
canariensis	Mercier & Louvet 1973, Feather et al. 1979		Summerell et al. 2010		Katan 1999, Pyler et al. 2000, Gunn & Summerell 2002	Pyler et al 2000, Gunn & Summerell 2002, Mbofung et al. 2007, Lievens et al. 2009b, Elliott et al. 2010, Laurence et al. 2015, Pinaria et al. 2015
cannabis	Noviello & Snyder 1962		Gordon 1965, Armstrong & Armstrong 1968, 1981 Booth 1971			O’Donnell et al. 2009
capsici	Black et al. 1993
carthami	Klisiewicz & Houston 1963		Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010	Klisiewicz & Thomas 1970a, b, Klisiewicz 1975		Shende et al. 2015
cassiae	Armstrong 1954, Gordon 1965		Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010			O’Donnell et al. 2009
cattleyae	Foster 1955		Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010		Baayen & Kleijn 1989	O’Donnell et al. 2009
cepae	Hanzawa 1914	Fusarium cepae Hanzawa, Mykol. Zentbl. 5: 5. 1914 Fusarium oxysporum f. cepae (Hanzawa) W.C. Snyder & H.N. Hansen, Amer. J. Bot. 27: 66. 1940 Fusarium oxysporum var. cepae (Hanzawa) Raillo, Fungi of the genus Fusarium: 253. 1950	Snyder & Hansen 1940, Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010		Molnár et al. 1990, Yoo et al. 1993, Katan & Di Primo 1999, Swift et al. 2002, Widodo et al. 2008, Bayraktar et al. 2010, Southwood et al. 2012	Gherbawy 1999, Mbofung et al. 2007, Galván et al. 2008, O’Donnell et al. 2009, Bayraktar et al. 2010, Lin et al. 2010, Southwood et al. 2012, Mirtalebi & Banihashemi 2014, Taylor et al. 2016
chrysanthemi	Armstrong et al. 1970		Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010	Huang et al. 1992, Troisi et al. 2013	Puhalla 1985, Correll et al. 1987, Kistler et al. 1998, Katan 1999, Pasquali et al. 2004c	Kim et al. 2001, Pasquali et al. 2003, 2004a, b, c, Bogale et al. 2007, Lievens et al. 2008, O’Donnell et al. 2009, Li et al. 2010, Lin et al. 2010, Troisi et al. 2010, 2013
ciceris	Padwick 1940, Erwin 1958, Matuo & Sato 1962	Fusarium orthoceras var. ciceri Padwick, Indian J. Agr. Sci. 10: 241–284. 1940 Fusarium lateritium f. ciceri (Padwick) Erwin, Phytopathology 48: 500. 1958	Armstrong & Armstrong 1968, 1981, Booth 1971	Haware & Nene 1982, Barve et al. 2001, Jiménez-Gasco et al. 2001, 2004a, b, Jiménez-Gasco & Jiménez-Díaz 2003, Sharma et al. 2004, Honnareddy & Dubey 2006, Gurjar et al. 2009, Dubey et al. 2012, Demers et al. 2014, Upasani et al. 2016	Kistler et al. 1998	Kelly et al. 1994, 1998, García-Pedrasjas et al. 1999, Barve et al. 2001, Jiménez-Gasco et al. 2001, 2002, 2004a, b, Jiménez-Gasco & Jiménez-Díaz 2003, Sharma et al. 2004, 2014, 2016, Honnareddy & Dubey 2006, Bayraktar et al. 2008, Dubey & Singh 2008, Gurjar et al. 2009, Dubey et al. 2012, Demers et al. 2014, Ghosh et al. 2015, Upasani et al. 2016, Williams et al. 2016
cichorii	Poli et al. 2012					Poli et al. 2012
citri	Timmer et al. 1979, Timmer 1982					Hannachi et al. 2015
coffeae	Alvarez 1945, Wellman 1954	Fusarium bulbigenum var. coffeae Álv. García, J. Agric. Univ. Puerto Rico 29: 8. 1945	Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010
colocasiae	Nishimura & Kudo 1994					Hirano & Arie 2009, Poli et al. 2013
conglutinans	Wollenweber 1913, Padwick 1940	Fusarium conglutinans Wollenw., Phytopathology 3 (1): 30. 1913 Fusarium orthoceras var. conglutinans (Wollenw.) Padwick, Indian J. Agric. Sci. 10: 282. 1940 Fusarium oxysporum f. conglutinans (Wollenw.) W.C. Snyder & H.N. Hansen, Amer. J.Bot. 27: 66. 1940	Snyder & Hansen 1940, Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010	Ramirez-Villupadua et al. 1985, Armstrong & Armstrong 1952, 1953, 1966	Puhalla 1985, Bosland & Williams 1987, Correll et al. 1987, Correll 1991, Kistler et al. 1998, Katan 1999, Katan & Di Primo 1999	Bosland & Williams 1987, Kistler et al. 1987, Kistler & Benny 1989, Crowhurst et al. 1995, Gherbawy 1999, Kim et al. 2001, Bogale et al. 2007, Hirano & Arie 2009, O’Donnell et al. 2009, Srinivasan et al. 2010, Poli et al. 2012, Covey et al. 2014, Zang et al. 2014, Hansen et al. 2015, Kashiwa et al. 2016, Li et al. 2015, 2016, Taylor et al. 2016, Van Dam & Rep 2017
coriandrii	Booth 1971, Armstrong & Armstrong 1981		Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010
crassulae	Ortu et al. 2013					Ortu et al. 2013
croci	Boerema & Hamers 1989			Roebroeck 2000	Roebroeck 2000	Roebroeck 2000, Palmero et al. 2014
crotalariae	Kulkarni 1934, Gupta 1974	Fusarium vasinfectum var. crotalariae Kulk., Indian J. Agric. Sci 4: 994. 1934 Fusarium udum f.sp. crotalariae (Kulk.) Subram., The genus Fusarium: 114. 1971	Armstrong & Armstrong 1968, 1981
cubense	Smith 1910, Brandes 1919	Fusarium cubense E.F. Sm., Science, N.S. 31: 755. 1910 Fusarium cubense var. inodoratum E.W. Brandes, Phytopathology 9: 374. 1919 Fusarium oxysporum var. cubense (E.F. Sm.) Wollenw., Die Fusarien, ihre Beschreibung, Schadwirkung und Bekämpfung: 119. 1935 Fusarium oxysporum f. cubense (E.F. Sm.) W.C. Snyder & H.N. Hansen, Amer. J. Bot. 27: 66. 1940	Snyder & Hansen 1940, Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010	See review by Fourie et al. 2011 and Ploetz 2015	See review by Fourie et al. 2011 and Ploetz 2015, Mostert et al. 2017	See review by Fourie et al. 2011, Ploetz 2015 and Lin & Shen 2017, Mostert et al. 2017, Aguayo et al. 2017, Van Dam & Rep 2017, Czislowski et al. 2017
cucumerinum	Owen 1956		Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010	Armstrong & Armstrong 1978b, Armstrong et al. 1978, Gerlagh & Blok 1988	Ahn et al. 1998, Kistler et al. 1998, Katan 1999, Katan & Di Primo 1999, Vakalounakis & Fragkiadakis 1999, Vakalounakis et al. 2004	Namiki et al. 1994, Vakalounakis & Fragkiadakis 1999, Kim et al. 2001, Skovgaard et al. 2001, Wang et al. 2001, Vakalounakis et al. 2004, Lievens et al. 2007, 2008, Hirano & Arie 2009, O’Donnell et al. 2009, Lin et al. 2010, Poli et al. 2013, Scarlett et al. 2013, Mirtalebi & Banihashemi 2014, Bertoldo et al. 2015
cucurbitacearum	Gerlagh & Blok 1988			Gerlagh & Blok 1988		Bogale et al. 2007, O’Donnell et al. 2009, Bennett et al. 2013
cumini	Patel et al. 1957		Summerell et al. 2010			Talaviya et al. 2014, Nawade et al. 2017
cyclaminis	Gerlach 1954		Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010		Woudt et al. 1995, Kistler et al. 1998, Katan 1999, Lori et al. 2012	Woudt et al. 1995, Gherbawy 1999, Kim et al. 2001, O’Donnell et al. 2009, Lecomte et al. 2016
dahliae	Summerell et al. 2010		Summerell et al. 2010
delphinii	Laskaris 1949		Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010			Kondo et al. 2013
dianthi	Snyder & Hansen 1940	Fusarium dianthi Prill. & Delacr., Compt. Rend. Acad. Sci.: 744–745. 1899 Fusarium oxysporum f. dianthi (Prill. & Delacr.) W.C. Snyder & H.N. Hansen, Amer. J. Bot. 27: 66. 1940 Fusarium oxysporum f. sp. barbati W.C. Snyder, Phytopathology 31: 1056. 1941 Fusarium oxysporum var. dianthi (Prill. & Delacr.) Raillo, Fungi of the genus Fusarium: 255. 1950	Snyder & Hansen 1940, Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010	Hood & Stewart 1957, Garibaldi 1975, 1977, 1983, Baayen et al. 1988, Aloi & Baayen 1993, Summerell et al. 2010	Puhalla 1985, Correll et al. 1987, Hadar et al. 1989, Molnár et al. 1990, Manicom et al. 1990, Aloi & Baayen 1993, Baayen et al. 1997, Kistler et al. 1998, Katan 1999, Katan & Di Primo 1999	Manicom et al. 1990, Manicom & Baayen 1993, Manulis et al. 1994, Crowhurst et al. 1995, Baayen et al. 1997, 2000, Gherbawy 1999, Kim et al. 2001, Skovgaard et al. 2001, Bogale et al. 2007, Lievens et al. 2008, Hirano & Arie 2009, O’Donnell et al. 2009, Poli et al. 2013, Bertoldo et al. 2015, Pinaria et al. 2015, Koyyappurath et al. 2016, Taylor et al. 2016
dioscoreae	Wellman 1972
echeveriae	Ortu et al. 2015a					Ortu et al. 2015a
elaeagni	Armstrong & Armstrong 1968	Fusarium oxysporum var. orthoceras (Appel & Wollenw.) Bilaǐ, The Fusaria: 282. 1955	Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010
elaeidis	Gordon 1965		Gordon 1965, Booth 1971, Armstrong & Armstrong 1981, Summerell et al. 2010		See Flood 2006 for prior publications	See Flood 2006 for prior publications; Bogale et al. 2007, O’Donnell et al. 2009, Elliott et al. 2010
erucae	Chatterjee & Rai 1974
erythroxyli	Sands et al. 1997		Summerell et al. 2010		Sands et al. 1997, Kistler et al. 1998, Katan 1999, Katan & Di Primo 1999	Sands et al. 1997, Lievens et al. 2009b, O’Donnell et al. 2009
eucalypti	Arya & Jain 1962		Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010
eustomae	Raabe 1985a					Bertoldo et al. 2015
fabae	Yu & Fang 1948		Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971			Mbofung et al. 2007, O’Donnell et al. 2009, Srinivasan et al. 2010, Mirtalebi & Banihashemi 2014
fatshederae	Triolo & Lorenzini 1983					O’Donnell et al. 2009
foli	see Hirooka et al. 2008					Hirooka et al. 2008
fragariae	Winks & Williams 1965		Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010		Katan & Di Primo 1999, Nagarajan et al. 2006	Kim et al. 2001, Nagarajan et al. 2004, 2006, Hirano & Arie 2009, O’Donnell et al. 2009, Chakrabarti et al. 2011, Fang et al. 2013, Poli et al. 2013, Suga et al. 2013, Bertoldo et al. 2015, Czislowski et al. 2017, Henry et al. 2017
freesia						Taylor et al. 2016
garlic	Matuo et al. 1986				Yoo et al. 1993, Katan & Di Primo 1999
gerberae	Von Arx 1952, Gordon 1965		Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010
gladioli	Massey 1926, Snyder & Hansen 1940, Buxton 1955	Fusarium oxysporum var. gladioli Massey, Phytopathology 16: 511. 1926 Fusarium oxysporum f. gladioli (Massey) W.C. Snyder & H.N. Hansen, Amer. J. Bot. 27: 66. 1940 Fusarium orthoceras var. gladioli L. McCulloch, Phytopathology 34: 280. 1944	Snyder & Hansen 1940, Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010	Roebroeck & Mes 1992, Mes et al. 1994, De Haan et al. 2000	Molnár et al. 1990, Mes et al. 1994, Kistler et al. 1998, Katan 1999, Katan & Di Primo 1999, Di Primo et al. 2002	Mes et al. 1994, Crowhurst et al. 1995, Baayen et al. 2000, De Haan et al. 2000, Kim et al. 2001, Bogale et al. 2007, O’Donnell et al. 2009, Elliott et al. 2010, Lin et al. 2010, Pinaria et al. 2015, Van Dam & Rep 2017
glycines	Armstrong & Armstrong 1965		Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010			Lievens et al. 2009b, O’Donnell et al. 2009, Pinaria et al. 2015, Koyyappurath et al. 2016
hebes	Raabe 1985b		Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010
heliconiae	Waite 1963 (see Ploetz 2006)
heliotropae	Netzer & Weintal 1987					Mbofung et al. 2007, O’Donnell et al. 2009
herbemontis	Gordon 1965	Fusarium oxysporum var. herbemontis Tochetto, Revta Agron., Porto Alegre: 82–89. 1954	Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010
iridiacearum	Roebroeck 2000			Roebroeck 2000	Roebroeck 2000	Roebroeck 2000
koae	Gardner 1980				Shiraishi et al. 2012	O’Donnell et al. 2009, Shiraishi et al. 2012
laciniati	Pandotra et al. 1971		Summerell et al. 2010
lactucae	Matuo & Motohashi 1967, Hubbard & Gerik 1993		Summerell et al. 2010	Fujinaga et al. 2001, 2003, 2005, 2014, Yamauchi et al. 2001, 2004, Ogiso et al. 2002, Shimazu et al. 2005, Pasquali et al. 2007, 2008, Lin et al. 2014, Gilardi et al. 2017	Kistler et al. 1998, Katan 1999, Ogiso et al. 2002, Yamauchi et al. 2004, Pasquali et al. 2005, 2008, Pintore et al. 2017	Fujinaga et al. 2005, 2014, Shimazu et al. 2005, Mbofung et al. 2007, Pasquali et al. 2007, 2008, Lievens et al. 2008, Hirano & Arie 2009, O’Donnell et al. 2009, Lin et al. 2010, 2014, Mbofung & Pryor 2010, Poli et al. 2012, 2013, Mirtalebi & Banihashemi 2014, Bertoldo et al. 2015, Gilardi et al. 2017
lagenariae	Matuo & Yamamoto 1967		Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010	Armstrong & Armstrong 1978b	Katan & Di Primo 1999	Okuda et al. 1998, Kim et al. 2001, Galván et al. 2008, Hirano & Arie 2009, O’Donnell et al. 2009, Poli et al. 2013
lathyri	Bhide & Uppal 1948	Fusarium oxysporum var. lathyri V.P. Bhide & Uppal, Phytopathology 38: 560–567. 1948	Gordon 1965,Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010
lentis	Vasudeva & Srinivasan 1952	Fusarium orthoceras var. lentis Vasudeva & Sriniv., Indian Phytopathol. 5: 28. 1953	Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010	Pouralibaba et al. 2016, 2017	Belabid & Fortas 2002	Belabid et al. 2004, O’Donnell et al. 2009, Taheri et al. 2010, Datta et al. 2011, Mohammadi et al. 2011, Rafique et al. 2015, Al-Husien et al. 2017, Nourollahi & Madahjalai 2017
lilii	Imle 1942		Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, 1981, Summerell et al. 2010		Löffler & Rumine 1991, Baayen et al. 1998, Kistler et al. 1998, Katan 1999, Katan & Di Primo 1999	Baayen et al. 1998, 2000, Kim et al. 2001, Skovgaard et al. 2001, Wang et al. 2001, O’Donnell et al. 2009, Lin et al. 2010, Baysal et al. 2013, Van Dam & Rep 2017
lini	Bolley 1901	Fusarium lini Bolley, Proc. Ann. Meeting Soc. Prom. Agr. Sci. 22: 42. 1901 Fusarium oxysporum f. lini (Bolley) W.C. Snyder & H.N. Hansen, Amer. J. Bot. 27: 66. 1940	Snyder & Hansen 1940, Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010		Katan & Di Primo 1999, Baayen et al. 2000	Baayen et al. 2000, Bogale et al. 2007, O’Donnell et al. 2009, Pinaria et al. 2015, Taylor et al. 2016
loti	Bergstrom & Kalb 1995				Wunsch et al. 2009	Galván et al. 2008, O’Donnell et al. 2009, Wunsch et al. 2009
luffae	Kawai et al. 1958		Summerell et al. 2010	Armstrong & Armstrong 1978b		Kim et al. 1993, Wang et al. 2001, Lin et al. 2010
lupini	Snyder & Hansen 1940		Snyder & Hansen 1940, Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010	Richter 1941, Armstrong & Armstrong 1964, Rataj-Guranowska et al. 1984	Kistler et al. 1998, Katan 1999, Katan & Di Primo 1999	Bogale et al. 2007, O’Donnell et al. 2009
lycopersici	Wollenweber 1913	Fusarium oxysporum subsp. lycopersici Sacc., Syll. Fung. 4: 705. 1886 Fusarium lycopersici Bruschi, Rc. Accad. Naz. Lincei: 298. 1912 Fusarium lycopersici (Sacc.) Wollenw., Phytopathology 3 (1): 29. 1913 Fusarium oxysporum f. lycopersici (Sacc.) W.C. Snyder & H.N. Hansen, Amer. J. Bot. 27: 66. 1940	Snyder & Hansen 1940, Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010	Alexander & Tucker 1945, Gerdemann & Finley 1951, Gabe 1975, Elias & Schneider 1992, Elias et al. 1993, Marlatt et al. 1996, Mes et al. 1998, Cai et al. 2003, Hirano & Arie 2006, Lievens et al. 2009a	Puhalla 1985, Correll et al. 1987, Hadar et al. 1989, Molnár et al. 1990, Correll 1991, Elias & Schneider 1991, 1992, Marlatt et al. 1996, Kistler et al. 1998, Mes et al. 1998, Katan 1999, Katan & Di Primo 1999, Cai et al. 2003	Elias & Schneider 1992; Elias et al. 1993, Crowhurst et al. 1995, Marlatt et al. 1996, Mes et al. 1998, Gherbawy 1999, Kim et al. 2001, Bao et al. 2002, Cai et al. 2003, Hirano & Arie 2006, 2009, Bogale et al. 2007, Mbofung et al. 2007, Lievens et al. 2009a, b, O’Donnell et al. 2009, Elliott et al. 2010, Inami et al. 2010, Ma et al. 2010, See review by Takken & Rep 2010, Chakrabarti et al. 2011, Poli et al. 2012, 2013, Thatcher et al. 2012, Baysal et al. 2013, Bennett et al. 2013, Covey et al. 2014, Gawehns et al. 2014, Mirtalebi & Banihashemi 2014, Bertoldo et al. 2015, Hansen et al. 2015, Nirmaladevi et al. 2016, Taylor et al. 2016, Williams et al. 2016, Bilju et al. 2017, Van Dam & Rep 2017, Jelinski et al. 2017
magnoliae	Lin & Chen 1994
matthiolae	Baker 1948		Booth 1971, Summerell et al. 2010		Correll 1991, Kistler et al. 1998, Katan 1999	Kistler et al. 1987, Mbofung et al. 2007, O’Donnell et al. 2009, Srinivasan et al. 2010, Poli et al. 2012
medicaginis	Weimer 1928	Fusarium oxysporum var. medicaginis Weimer, J. Agric. Res. 37: 425. 1928 Fusarium oxysporum f. medicaginis (Weimer) W.C. Snyder & H.N. Hansen, Amer. J. Bot. 27: 66. 1940	Snyder & Hansen 1940, Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010		Puhalla 1985, Correll et al. 1987, Molnár et al. 1990, Kistler et al. 1998, Katan 1999	Mbofung et al. 2007, O’Donnell et al. 2009, Srinivasan et al. 2010, Poli et al. 2012, Mirtalebi & Banihashemi 2014, Thatcher et al. 2016, Williams et al. 2016, Czislowski et al. 2017
melongenae	Matuo & Ishigami 1958		Gordon 1965, Armstrong & Armstrong 1968, Booth 1971, 1981, Summerell et al. 2010		Hadar et al. 1989, Kistler et al. 1998, Katan 1999, Katan & Di Primo 1999, Altinok & Can 2010, Altinok 2013, Altinok et al. 2013	Crowhurst et al. 1995, Kim et al. 2001, Hirano & Arie 2009, O’Donnell et al. 2009, Altinok & Can 2010, Baysal et al. 2010, Bennett et al. 2013, Poli et al. 2013, Bertoldo et al. 2015, Dong et al. 2017
melonis	Leach & Currence 1938, Snyder & Hansen 1940	Fusarium bulbigenum var. niveum Leach & Curr., Minnisota Agric. Exp. Sta. Tech. Bull. 129: 1–32. 1938	Snyder & Hansen 1940, Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010	Risser & Mas 1965, Risser et al. 1976, Armstrong & Armstrong 1978b, Gerlagh & Blok 1988, Katan et al. 1994, Luongo et al. 2014, Mirtalebi & Banihashemi 2014, Sebastiani et al. 2017	Correll et al. 1987, Jacobson & Gordon 1988, 1990a, Hadar et al. 1989, Correll 1991, Katan et al. 1994, Kistler et al. 1998, Katan 1999, Katan & Di Primo 1999, Mirtalebi & Banihashemi 2014	Jacobson & Gordon 1990b, Kim et al. 1993, 2001, Crowhurst et al. 1995, Namiki et al. 1998, 2001, Gherbawy 1999, Skovgaard et al. 2001, Mbofung et al. 2007, Hirano & Arie 2009, Lievens et al. 2009b, O’Donnell et al. 2009, Lin et al. 2010, Bennett et al. 2013, Poli et al. 2013, Covey et al. 2014, Gawehns et al. 2014, Luongo et al. 2014, Ma et al. 2014, Mirtalebi & Banihashemi 2014, Bertoldo et al. 2015, Hansen et al. 2015, Pinaria et al. 2015, Schmidt et al. 2016, Taylor et al. 2016, Williams et al. 2016, Van Dam & Rep 2017, Sebastiani et al. 2017
meniscoideum (var.)	Bugnicourt 1939		Gerlach & Nirenberg 1982			O’Donnell et al. 2009
momordicae	Sun & Huang 1983					Skovgaard et al. 2001, O’Donnell et al. 2009, Lin et al. 2010, Bennett et al. 2013, Chen et al. 2015
mori	Pastrana et al. 2017				Pastrana et al. 2017	Pastrana et al. 2017
narcissi	Wollenweber & Reinking 1935, Snyder & Hansen 1940		Snyder & Hansen 1940, Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010			Linfield 1993, Crowhurst et al. 1995, O’Donnell et al. 2009, Taylor et al. 2016, Van Dam & Rep 2017
nelumbicola	Gordon 1965	Fusarium bulbigenum var. nelumbicola Y. Nisik. & Kyoto Watan., Ber. Ohara Inst. Landw. Biol. Okayama Univ.: 3. 1953	Snyder & Hansen 1940, Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010
nicotianae	Johnson 1921	Fusarium oxysporum var. nicotianae J. Johnson, J. Agric. Res. 20: 525. 1921	Booth 1971, Summerell et al. 2010			Bogale et al. 2007, O’Donnell et al. 2009
niveum	Wollenweber & Reinking 1935	Fusarium niveum E.F. Sm., Bull. U.S.D.A. 1894 Fusarium bulbigenum var. niveum (E.F. Sm.) Wollenw., Die Fusarien: 117. 1935 Fusarium oxysporum f. niveum (E.F. Sm.) W.C. Snyder & H.N. Hansen, Amer. J. Bot. 27: 66. 1940	Snyder & Hansen 1940, Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010	Reid 1958, Crall 1963, Netzer 1976, Armstrong & Armstrong 1978b, Martyn 1987, Gerlagh & Blok 1988, Martyn & Bruton 1989, Larkin et al. 1990, Zhou et al. 2010	Puhalla 1985, Correll et al. 1987, Hadar et al. 1989, Larkin et al. 1988, 1990, Correll 1991, Kistler et al. 1998, Katan 1999, Katan & Di Primo 1999	Kim et al. 1993, 2001, Crowhurst et al. 1995, Zhang et al. 2005, Bogale et al. 2007, Hirano & Arie 2009, O’Donnell et al. 2009, Lin et al. 2010, Chakrabarti et al. 2011, Poli et al. 2013, Gawehns et al. 2014, Mirtalebi & Banihashemi 2014, Bertoldo et al. 2015, Ren et al. 2015, Van Dam & Rep 2017, Czislowski et al. 2017
opuntiarum	Gordon 1965	Fusarium oxysporum var. opuntiarum Pettinari, Annali Sper. Agr.: 1419. 1951	Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010		Katan & Di Primo 1999	Baayen et al. 2000, Mbofung et al. 2007, O’Donnell et al. 2009, Ortu et al. 2013, Pinaria et al. 2015, Koyyappurath et al. 2016, Bertetti et al. 2017
orthoceras	Bilaǐ 1955
oxysporum (var.)	Von Schlechtendahl 1824		Gerlach & Nirenberg 1982
palmarum	Elliott et al. 2010					O’Donnell et al. 2009, Elliott et al. 2010, 2017, Giesbrecht et al. 2013
papaveris	Ortu et al. 2015b		Summerell et al. 2010		Katan 1999	Bertetti et al. 2014, Ortu et al. 2015b
passiflorae	Gordon 1965		Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010			Gherbawy 1999, Bogale et al. 2007, Lievens et al. 2009b, O’Donnell et al. 2009, Chakrabarti et al. 2011, Dos Santos Silva et al. 2013, Gawehns et al. 2014, Pinaria et al. 2015, Koyyappurath et al. 2016, Czislowski et al. 2017
perillae	Kim et al. 2002
perniciosum	Toole 1941	Fusarium perniciosum Hepting, Circ. U.S.D.A.: 7. 1939 Fusarium oxysporum f. perniciosum (Hepting) Toole, Phytopathology 31: 599. 1941 Fusarium vasinfectum var. perniciosum (Hepting) Carrera, Monatsh. Landw.: 483. 1955	Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010	Toole 1952		Crowhurst et al. 1995, Bogale et al. 2007, Mbofung et al. 2007, Lievens et al. 2009b, O’Donnell et al. 2009, Elliott et al. 2010, Bennett et al. 2013, Pinaria et al. 2015
phaseoli	Kendrick & Snyder 1942b		Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010	Ribeiro 1977, Ribeiro & Hagedorn 1979, Salgado & Schwartz 1993, Woo et al. 1996, Alves-Santos et al. 2002a, Cramer et al. 2003, Henrique et al. 2015	Woo et al. 1996, Kistler et al. 1998, Katan 1999, Katan & Di Primo 1999, Alves-Santos et al. 2002a	Woo et al. 1996, Cramer et al. 2003, Zanotti et al. 2006, Alves-Santos et al. 2002b, Bogale et al. 2007, Mbofung et al. 2007, Hirano & Arie 2009, O’Donnell et al. 2009, De Vega-Bartol et al. 2011, Baysal et al. 2013, Poli et al. 2013, Mirtalebi & Banihashemi 2014, Da Silva et al. 2014, Bertoldo et al. 2015, De Sousa et al. 2015
phormii	Wager 1947		Gordon 1965, Armstrong & Arm strong 1968, 1981, Booth 1971, Summerell et al. 2010
pini	Hartig 1892, Snyder & Hansen 1940	Fusisporium aurantiacum Link, Mag. Ges. Naturf. Freunde Berlin 3: 19. 1809 Fusoma pini Hartig, Forstl.-Naturwiss. Z. 1: 432–436. 1892 Fusarium blasticola Rostr., Gartner-Tidende 1895: 122. 1895 Fusarium oxysporum f. pini (Hartig) W.C. Snyder & H.N. Hansen, Amer. J. Bot. 27: 66. 1940 Fusarium oxysporum f. sp. blasticola Bilaǐ, Fusarii: 281. 1955				O’Donnell et al. 2009
pisi	Van Hall 1903, Snyder & Hansen 1940	Fusarium vasinfectum var. pisi C.J.J. Hall, Ber. Deutsch. Bot. Ges. 21: 4. 1903 Fusarium orthoceras var. pisi Linford, Res. Bull. Agric. Exp. Stn Univ. Wis.: 11. 1928 Fusarium oxysporum f. 8 W.C. Snyder, Zentralbl. Bakteriol., 2. Abt.: 374. 1935 Fusarium oxysporum var. pisi (C.J.J. Hall) Raillo, Fungi of the genus Fusarium: 254. 1950 Fusarium oxysporum var. orthoceras (Appel & Wollenw.) Bilaǐ, Fusarii: 282. 1955	Snyder & Hansen 1940, Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010	Snyder & Walker 1935, Snyder & Hansen 1940, Schreuder 1951, Bolton et al. 1966, Armstrong & Armstrong 1974, Kraft & Haglund 1978, Haglund & Kraft 1979, Coddington et al. 1987, Whitehead et al. 1992, Grajal-Martin et al. 1993	Puhalla 1985, Correll et al. 1987, Correll 1991, Whitehead et al. 1992, Kistler et al. 1998, Katan 1999, Katan & Di Primo 1999,	Coddington et al. 1987, Kistler et al. 1991, Whitehead et al. 1992, Grajal-Martin et al. 1993, Gherbawy 1999, Skovgaard et al. 2001, O’Donnell et al. 2009, Chakrabarti et al. 2011, Covey et al. 2014, Mirtalebi & Banihashemi 2014, Hansen et al. 2015, Taylor et al. 2016, Williams et al. 2016, Van Dam & Rep 2017
psidii	Prasad et al. 1952		Gordon 1965, Armstrong & Arm strong 1968, 1981, Booth 1971, Summerell et al. 2010			Gupta 2012, Mishra et al. 2013a, b, c, 2014
pyracanthae	McRitchie 1973, Armstrong & Armstrong 1981		Armstrong & Armstrong 1968, 1981, Summerell et al. 2010
querci	Gordon 1965		Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010
quitoense	Ochoa et al. 2004
radicis-capsici	Lomas-Cano et al. 2014, 2016					Lomas-Cano et al. 2014
radicis-cucumerinum	Vakalounakis 1996		Summerell et al. 2010		Katan 1999, Katan & Di Primo 1999, Vakalounakis & Fragkiadakis 1999, Vakalounakis et al. 2004, 2005, Tok & Kurt 2010	Vakalounakis & Fragkiadakis 1999, Vakalounakis et al. 2004, 2005, Lievens et al. 2007, Van Dam & Rep 2017
radicis-lupini	Weimer 1944		Gordon 1965, Booth 1971, Summerell et al. 2010
radicis-lycopersici	Jarvis & Shoemaker 1978		Summerell et al. 2010		Puhalla 1985, Correll et al. 1987, Katan et al. 1991, Kistler et al. 1998, Katan 1999, Katan & Di Primo 1999, Rosewich et al. 1999, Di Primo et al. 2001, Balmas et al. 2005, Huang et al. 2013	Kim et al. 2001, Skovgaard et al. 2001, Balmas et al. 2005, Hirano & Arie 2006, 2009, Bogale et al. 2007, Hibar et al. 2007, O’Donnell et al. 2009, Huang et al. 2013, Poli et al. 2013, Covey et al. 2014, Mirtalebi & Banihashemi 2014, Bertoldo et al. 2015, Taylor et al. 2016
radicis-vanillae	Koyyappurath et al. 2016					Koyyappurath et al. 2016
ranunculi	Garibaldi & Gullino 1985
rapae	Enya et al. 2008				Enya et al. 2008	Enya et al. 2008
raphani	Kendrick & Snyder 1942a		Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010		Bosland & Williams 1987, Kistler et al. 1998, Katan 1999, Katan & Di Primo 1999	Kistler & Benny 1989, Kistler et al. 1991, Kim et al. 2001, Bogale et al. 2007, Hirano & Arie 2009, O’Donnell et al. 2009, Lin et al. 2010, Srinivasan et al. 2010, Poli et al. 2012, 2013, Covey et al. 2014, Bertoldo et al. 2015, Taylor et al. 2016, Van Dam & Rep 2017, Kim et al. 2017
rauvolfiae	Janardhanan et al. 1964		Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010			O’Donnell et al. 2009
rhois	Snyder et al. 1949		Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010			Mbofung et al. 2007
ricini	Gordon 1965	Fusarium orthoceras var. ricini Wollenw., Biologico 6: 148. 1940	Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010			Prasad et al. 2008, Reddy et al. 2012
samaneae	Wellman 1972
sansevieriae	Gupta et al. 1982
sedi	Raabe 1960		Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010
sesami	Gordon 1965, Booth 1971	Fusarium vasinfectum var. sesami Zaprom., Pflanzenschutz-Vers. Sta. Taschkent: 36 pp. 1926	Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010		Basirnia & Banihashemi 2005	O’Donnell et al. 2009, Li et al. 2012, Bennett et al. 2013
sesbaniae	Gordon 1965, Booth 1971		Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010
spinaciae	Hungerford 1923	Fusarium spinaciae Sherb., Phytopathology 13: 209. 1923 Fusarium oxysporum f. spinaciae (Sherb.) W.C. Snyder & H.N. Hansen, Amer. J. Bot. 27: 66. 1940 Fusarium redolens f. spinaciae (Sherb.) Subram., Hyphomycetes: an account of Indian species, except Cercosporae: 690. 1971	Snyder & Hansen 1940, Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010	Armstrong & Armstrong 1976	Kistler et al. 1998, Katan 1999, Katan & Di Primo 1999, Takehara et al. 2003	Baayen et al. 2000, Kim et al. 2001, Skovgaard et al. 2001, Kawabe et al. 2007, Mbofung et al. 2007, Hirano & Arie 2009, O’Donnell et al. 2009, Poli et al. 2012, 2013, Bennett et al. 2013, Okubara et al. 2013, Covey et al. 2014, Mirtalebi & Banihashemi 2014, Bertoldo et al. 2015
stachydis	Gordon 1965		Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010
strigae	Elzein & Kroschel 2006					Elzein et al. 2008, Zimmermann et al. 2015, 2016
tabernaemontanae	Pande & Rao 1990
tanaceti	Hirooka et al. 2008					Hirooka et al. 2008
tracheiphilum	Wollenweber 1931, Snyder & Hansen 1940	Fusarium tracheiphilum E.F. Sm. 1899 Fusarium bulbigenum var. tracheiphilum (E.F. Sm.) Wollenw., Z. Parasitenk. (Berlin) 3: 413. 1931 Fusarium oxysporum f. tracheiphilum (E.F. Sm.) W.C. Snyder & H.N. Hansen, Amer. J. Bot. 27: 66. 1940	Snyder & Hansen 1940, Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010	Armstrong & Armstrong 1950, 1980, Hare 1953, Swanson & Van Gundy 1985, Smith et al. 1999	Correll et al. 1987, Kistler et al. 1998, Katan 1999, Katan & Di Primo 1999, Bao et al. 2002	Gherbawy 1999, Bao et al. 2002, Hirano & Arie 2009, O’Donnell et al. 2009, Lin et al. 2010, Troisi et al. 2010, Bennett et al. 2013, Poli et al. 2013, Bertoldo et al. 2015, Koyyappurath et al. 2016
trifolii	Bilaǐ 1955	Fusarium trifolii Jacz., Jb. Pfl. krankh. Russl. VII-VIII, Abt. 6. 1917 Fusarium oxysporum var. trifolii (Jacz.) Raillo, Fungi of the genus Fusarium: 255. 1950	Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010
tuberosi	Snyder & Hansen 1940	Fusarium oxysporum var. solani Raillo, Fungi of the genus Fusarium: 254. 1950 Fusarium oxysporum var. solani (Raillo) Bilaǐ, Fusarii: 281. 1955	Snyder & Hansen 1940, Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010		Molnár et al. 1990, Venter et al. 1992, Kistler et al. 1998, Katan 1999	Gherbawy 1999, Lievens et al. 2009a, O’Donnell et al. 2009
tulipae	Snyder & Hansen 1940		Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010		Katan 1999, Katan & Di Primo 1999	Gherbawy 1999, Baayen et al. 2000, Kim et al. 2001, Skovgaard et al. 2001, Hirano & Arie 2009, O’Donnell et al. 2009, Poli et al. 2013, Mirtalebi & Banihashemi 2014, Bertoldo et al. 2015, Pinaria et al. 2015, Swett & Uchida 2015, Van Dam & Rep 2017
vanillae	Tucker 1927	Fusarium batatas var. vanillae Tucker, J. Agric. Res. 44: 1121. 1927	Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010		Katan & Di Primo 1999	O’Donnell et al. 2009, Chakrabarti et al. 2011, Adame-García et al. 2015, Pinaria et al. 2015, Koyyappurath et al. 2016
vasconcella	Ochoa et al. 2004
vasinfectum	Atkinson 1892	Fusarium vasinfectum G.F. Atk., Bulletin of the Alabama Agricultural Experiment Station: 28. 1892 Fusarium oxysporum f. vasinfectum (G.F. Atk.) W.C. Snyder & H.N. Hansen, Amer. J. Bot. 27: 66. 1940	Snyder & Hansen 1940, Gordon 1965, Armstrong & Armstrong 1968, 1981, Booth 1971, Summerell et al. 2010	Armstrong & Armstrong 1958a, 1960, 1978a, Ibrahim 1966, Kappelman 1983, Chen et al. 1985, Assigbetse et al. 1994, Fernandez et al. 1994, Nirenberg et al. 1994, Skovgaard et al. 2001, Kim et al. 2005, Holmes et al. 2009, Guo et al. 2015	Puhalla 1985, Correll et al. 1987, Katan & Katan 1988, Hadar et al. 1989, Correll 1991, Fernandez et al. 1994, Davis et al. 1996, Kistler et al. 1998, Katan 1999, Katan & Di Primo 1999, Abo et al. 2005, Wang et al. 2010	Assigbetse et al. 1994, Fernandez et al. 1994, Crowhurst et al. 1995, Moricca et al. 1998, Skovgaard et al. 2001, Smith et al. 2001, Abd-Elsalam et al. 2002, 2004, 2006, Abo et al. 2005, Kim et al. 2005, 2017, McFadden et al. 2006, Wang et al. 2006, 2010, Mbofung et al. 2007, Zambounis et al. 2007, Bennett et al. 2008, 2013, Holmes et al. 2009, O’Donnell et al. 2009, Elliot et al. 2010, Chakrabarti et al. 2011, Egamberdiev et al. 2013, 2014, Da Silva et al. 2014, Covey et al. 2014, Doan et al. 2014, Cianchetta et al. 2015, Guo et al. 2015, Pinaria et al. 2015, Crutcher et al. 2016, Taylor et al. 2016, Van Dam & Rep 2017, Ortiz et al. 2017
voandzeiae	Armstrong et al. 1975		Armstrong & Armstrong 1981			O’Donnell et al. 2009
zingiberi	Trujillo 1963			Pappalardo et al. 2009	Katan & Di Primo 1999	Crowhurst et al. 1995, O’Donnell et al. 2009, Pappalardo et al. 2009, Chakrabarti et al. 2011, Gupta et al. 2014, Czislowski et al. 2017

The haplotype subspecific classification system was introduced by Chang et al. (2006) and later expanded upon by O’Donnell et al. (2008, 2009) to include strains from both the FOSC and Neocosmospora (formerly the F. solani (FSSC) species complex). This classification system is based on unique multilocus genotypes within the species complex, aimed to resolve communication problems among public health and agricultural scientists (O’Donnell et al. 2008). Chang et al. (2006) proposed a standardised haplotype nomenclature system that depict the species complex, species and genotype. O’Donnell et al. (2009) was able to identify 256 unique two-locus haplotypes from 850 isolates representing 68 special forms of F. oxysporum as well as environmental and clinical strains. However, this classification system is not in common use as a reference, and a continuously updated database is required.

One of the most important subspecific ranks applied to special forms of F. oxysporum are physiological pathotypes or races. This classification system is of great importance to plant breeders, especially for resistance breeding. Traditionally, race demarcation is based on cultivar specificity linked to specific resistance genes of the plant host cultivar (Armstrong & Armstrong 1981, Kistler 1997, Baayen et al. 2000, Roebroeck 2000, Fourie et al. 2011, Epstein et al. 2017). However, race designation has been inconsistent in the past (Gerlagh & Blok 1988, Correll 1991, Kistler 1997, Fourie et al. 2011) with several different nomenclatural systems being applied (Gabe 1975, Risser et al. 1976, Armstrong & Armstrong 1981) to further cause confusion (Kistler 1997). With advances in molecular technology, identification of races has been simplified using sequence-characterised amplified region (SCAR) primers (Lievens et al 2008, Epstein et al. 2017, Gilardi et al. 2017). However, time consuming and laborious pathogenicity tests are still needed to identify new emerging races and to test whether newly developed plant cultivars are resistant to known races (Epstein et al. 2017, Gilardi et al. 2017).

The use of vegetative compatibility (also known as heterokaryon compatibility) has formed an integral part of subspecific classification of F. oxysporum special forms and non-pathogenic strains. Formation of a stable heterokaryon between two auxotrophic nutritional mutants is regulated by several vic or het incompatibility loci (Correll 1991, Leslie 1993) indicating that the strains are homogenic at these loci (Correll 1991) and considered to be part of the same VCG. Therefore, classification using vegetative compatibility is based on genetic similarity at specific loci and not pathogenicity, providing a crude marker for population genetic studies (Correll 1991, Gordon & Martyn 1997, Leslie 1993, Leslie & Summerell 2006). Puhalla (1985), utilizing nit mutants, was the first to identify VCGs in F. oxysporum and characterised 16 VCGs in a collection of 21 F. oxysporum strains. The numbering system applied by Puhalla (1985), which is still used today, consists of a three-digit numerical code indicating the special form followed by digit(s) indicating the VCG (Katan 1999, Katan & Di Primo 1999). Conventional VCG characterisation is a relatively objective, time consuming and laborious assay only indicating genetic similarity and not genetic difference (Kistler 1997). Therefore, several PCR-based detection methods have been developed to identify economically important VCGs as diagnostic tool (Fernandez et al. 1998, Pasquali et al. 2004a, c, Lievens et al. 2008), e.g., F. oxysporum f. sp. cubense TR4 VCG01213 (Dita et al. 2010).

Until recently, limited knowledge on the genetic premise for host specificity in F. oxysporum was available (Gordon & Martyn 1997, Kistler 1997, Baayen et al. 2000). However, the discovery of a lineage-specific chromosome (or transposable/effector/accessory chromosome) in F. oxysporum f. sp. lycopersici by Ma et al. (2010), in which the host specific virulence genes lie (Van der Does et al. 2008, Takken & Rep 2010, Ma et al. 2013), has provided a new view into the evolution of pathogenicity in F. oxysporum. In vitro transfer of these accessory chromosomes into non-pathogenic F. oxysporum strains has converted the latter strains into host-specific pathogens, providing evidence that host-specific pathogenicity could be acquired through horizontal transfer of accessory chromosomes (Takken & Rep 2010, Ma et al. 2010, 2013, Van Dam et al. 2016, Van Dam & Rep 2017). Therefore, the special form name can be linked to the accessory chromosome whereas race demarcation can be linked to the specific virulence genes carried on these accessory chromosomes.

The genetic and functional mechanisms of the infection process in plants of various special forms of F. oxysporum has been well documented (Di Pietro et al. 2003, Ma et al. 2013, Upasani et al. 2016, Gordon 2017). However, these same mechanisms are still poorly understood in human and animal infections (O’Donnell et al. 2004, Guarro 2013, Van Diepeningen et al. 2015). Fusarium oxysporum has been linked to fungal keratitis (Hemo et al. 1989, Chang et al. 2006) and dermatitis (Guarro & Gene 1995, Romano et al. 1998, Ninet et al. 2005, Cutuli et al. 2015, Van Diepeningen et al. 2015), and has been isolated from contaminated hospital water systems (Steinberg et al. 2015, Edel-Hermann et al. 2016) and medical equipment (Barton et al. 2016, Carlesse et al. 2017) posing a serious threat to immunocompromised patients. Several recent reports also indicate that F. oxysporum is able to infect immunocompetent patients (Jiang et al. 2016, Khetan et al. 2018). In general, fusariosis is difficult to treat as Fusarium species display a remarkable resistance to antifungal agents (Guarro 2013, Al-Hatmi et al. 2018). However, some antimycotics are known to be effective against F. oxysporum related fusariosis (Al-Hatmi et al. 2018). Recently, both mycotoxins beauvericin and fusaric acid, produced by F. oxysporum strains that can infect tomato, have been shown to be important virulence determinants to infect immunosuppressed mice (López-Berges et al. 2013, López-Díaz et al. 2018).

Strains of F. oxysporum are known to produce a cocktail of polyketide secondary metabolites, some with unknown function and toxicities (Marasas et al. 1984, Mirocha et al. 1989, Bell et al. 2003, Desjardins 2006, Manici et al. 2017). Some of the better-known toxins produced by F. oxysporum include beauvericin (Marasas et al. 1984, Logrieco et al. 1998, López-Berges et al. 2013), fusaric acid (Marasas et al. 1984, López-Díaz et al. 2018) and fumonisins (Rheeder et al. 2002) to name a few. Mycotoxicological studies on F. oxysporum has thus far only focused on a strain to strain basis and therefore no link has yet been established between special form and/or race and mycotoxin production capabilities.

In light of the complicated and sometimes confusing classification systems applied to F. oxysporum taxonomy and nomenclature, the question has risen whether F. oxysporum truly represent a species (Kistler 1997). Given that F. oxysporum is a common, widespread, soil-borne fungus, with a global distribution and high economic importance, this question requires urgent attention. Therefore, to advance and stabilize the taxonomic and nomenclatural position of F. oxysporum and allow naming of the multiple cryptic species recognised in this species complex, Fusarium isolates were collected from the type locality in Berlin, Germany, and the type substrate, Solanum tuberosum. Using molecular phylogenetic and morphological tools, an epitype is designated for F. oxysporum in the present study based on these collections.

MATERIALS AND METHODS

Isolates

Tubers of S. tuberosum (potato), displaying symptoms of dry rot, were collected from several vegetable gardens in Berlin, Germany. Potato tubers were placed individually in paper bags, stored at 4 °C until transported to the laboratory for further processing. After surface-sterilisation of the potato tubers using a 10 % (v/v) sodium hypochlorite solution, pieces of symptomatic tissue were removed from the leading edges of the rot lesions and plated onto 2 % (w/v) potato dextrose agar (PDA) amended with 100 μg/mL penicillin and 100 μg/mL streptomycin, and peptone pentachloronitrobenzene agar (PCNB; Nash & Snyder 1962) and incubated at 25 °C in the dark. Axenic cultures were prepared on PDA from characteristic Fusarium colonies. Additional strains, previously identified as F. oxysporum, were obtained from the culture collection (CBS) of the Westerdijk Fungal Biodiversity Institute (WFBI), Utrecht, the Netherlands, and the working collection of Pedro W. Crous (CPC) housed at WFBI (Table 2).

Table 2.

Details of Fusarium strains included in the phylogenetic analyses.

Species	Culture accession1	Host/substrate	Special form	Origin	GenBank accession
					cmdA	IGS	rpb2	tef1	tub2
Fusarium callistephi	CBS 187.53T	Callistephus chinensis	callistephi	The Netherlands	MH484693	MH484784	MH484875	MH484966	MH485057
	CBS 115423	Agathosma betulina		South Africa	MH484723	MH484814	MH484905	MH484996	MH485087
F. carminascens	CBS 144739 = CPC 25792	Zea mays		South Africa	MH484752	MH484843	MH484934	MH485025	MH485116
	CBS 144740 = CPC 25793	Z. mays		South Africa	MH484753	MH484844	MH484935	MH485026	MH485117
	CBS 144741 = CPC 25795	Z. mays		South Africa	MH484754	MH484845	MH484936	MH485027	MH485118
	CBS 144738 = CPC 25800T	Z. mays		South Africa	MH484755	MH484846	MH484937	MH485028	MH485119
F. contaminatum	CBS 111552	Pasteurized fruit juice		The Netherlands	MH484718	MH484809	MH484900	MH484991	MH485082
	CBS 114899T	Pasteurized chocolate milk		Germany	MH484719	MH484810	MH484901	MH484992	MH485083
	CBS 117461	Tetra pack with milky nutrition		The Netherlands	MH484729	MH484820	MH484911	MH485002	MH485093
F. cugenangense	CBS 620.72 = DSM 11271 = NRRL 36520	Crocus sp.	gladioli	Germany	MH484697	MH484788	MH484879	MH484970	MH485061
	CBS 130304 = BBA 69050 = NRRL 25433	Gossypium barbadense	vasinfectum	China	MH484739	MH484830	MH484921	MH485012	MH485103
	CBS 130308 = ATCC 26225 = NRRL 25387	Human toe nail		New Zealand	MH484738	MH484829	MH484920	MH485011	MH485102
	CBS 131393	Vicia faba		Australia	MH484746	MH484837	MH484928	MH485019	MH485110
F. curvatum	CBS 247.61 = BBA 8398 = DSM 62308 = NRRL 22545	Matthiola incana	matthiolae	Germany	MH484694	MH484785	MH484876	MH484967	MH485058
	CBS 238.94 = NRRL 26422 = PD 94/184T	Beaucarnia sp.	meniscoideum	The Netherlands	MH484711	MH484802	MH484893	MH484984	MH485075
	CBS 141.95 = NRRL 36251 = PD 94/1518	Hedera helix		The Netherlands	MH484712	MH484803	MH484894	MH484985	MH485076
F. duoseptatum	CBS 102026 = NRRL 36115	Musa sapientum cv. Pisang ambon	cubense	Malaysia	MH484714	MH484805	MH484896	MH484987	MH485078
F. elaeidis	CBS 217.49 = NRRL 36358	Elaeis sp.	elaeidis	Zaire	MH484688	MH484779	MH484870	MH484961	MH485052
	CBS 218.49 = NRRL 36359	Elaeis sp.	elaeidis	Zaire	MH484689	MH484780	MH484871	MH484962	MH485053
	CBS 255.52 = NRRL 36386	Elaeis guineensis	elaeidis	Unknown	MH484692	MH484783	MH484874	MH484965	MH485056
F. fabacearum	CBS 144742 = CPC 25801	Z. mays		South Africa	MH484756	MH484847	MH484938	MH485029	MH485120
	CBS 144743 = CPC 25802T	Glycine max		South Africa	MH484757	MH484848	MH484939	MH485030	MH485121
	CBS 144744 = CPC 25803	G. max		South Africa	MH484758	MH484849	MH484940	MH485031	MH485122
F. foetens	CBS 120665	Nicotiana tabacum		Iran	MH484736	MH484827	MH484918	MH485009	MH485100
F. glycines	CBS 176.33 = NRRL 36286	Linum usitatissium	lini	Unknown	MH484686	MH484777	MH484868	MH484959	MH485050
	CBS 214.49 = NRRL 36356	Unknown		Argentina	MH484687	MH484778	MH484869	MH484960	MH485051
	CBS 200.89	Ocimum basilicum	basilici	Italy	MH484706	MH484797	MH484888	MH484979	MH485070
	CBS 144745 = CPC 25804	G. max		South Africa	MH484759	MH484850	MH484941	MH485032	MH485123
	CBS 144746 = CPC 25808T	G. max		South Africa	MH484760	MH484851	MH484942	MH485033	MH485124
F. gossypinum	CBS 116611	Gossypium hirsutum	vasinfectum	Ivory Coast	MH484725	MH484816	MH484907	MH484998	MH485089
	CBS 116612	G. hirsutum	vasinfectum	Ivory Coast	MH484726	MH484817	MH484908	MH484999	MH485090
	CBS 116613T	G. hirsutum	vasinfectum	Ivory Coast	MH484727	MH484818	MH484909	MH485000	MH485091
F. hoodiae	CBS 132474T	Hoodia gordonii	hoodiae	South Africa	MH484747	MH484838	MH484929	MH485020	MH485111
	CBS 132476	H. gordonii	hoodiae	South Africa	MH484748	MH484839	MH484930	MH485021	MH485112
	CBS 132477	H. gordonii	hoodiae	South Africa	MH484749	MH484840	MH484931	MH485022	MH485113
F. languescens	CBS 645.78 = NRRL 36531T	Solanum lycopersicum	lycopersici	Morocco	MH484698	MH484789	MH484880	MH484971	MH485062
	CBS 646.78 = NRRL 36532	S. lycopersicum	lycopersici	Morocco	MH484699	MH484790	MH484881	MH484972	MH485063
	CBS 413.90 = ATCC 66046 = NRRL 36465	S. lycopersicum	lycopersici	Israel	MH484708	MH484799	MH484890	MH484981	MH485072
	CBS 300.91 = NRRL 36416	S. lycopersicum	lycopersici	The Netherlands	MH484709	MH484800	MH484891	MH484982	MH485073
	CBS 302.91 = NRRL 36419	S. lycopersicum	lycopersici	The Netherlands	MH484710	MH484801	MH484892	MH484983	MH485074
	CBS 872.95 = NRRL 36570	S. lycopersicum	radicis-lycopersici	Unknown	MH484713	MH484804	MH484895	MH484986	MH485077
	CBS 119796 = MRC 8437	Z. mays		South Africa	MH484735	MH484826	MH484917	MH485008	MH485099
F. libertatis	CBS 144748 = CPC 25782	Aspalathus sp.		South Africa	MH484750	MH484841	MH484932	MH485023	MH485114
	CBS 144747 = CPC 25788	Aspalathus sp.		South Africa	MH484751	MH484842	MH484933	MH485024	MH485115
	CBS 144749 = CPC 28465T	Rock surface		South Africa	MH484762	MH484853	MH484944	MH485035	MH485126
F. nirenbergiae	CBS 129.24	Secale cereale		Unknown	MH484682	MH484773	MH484864	MH484955	MH485046
	CBS 149.25 = NRRL 36261	Musa sp.	cubense	Unknown	MH484683	MH484774	MH484865	MH484956	MH485047
	CBS 181.32 = NRRL 36303	S. tuberosum		USA	MH484685	MH484776	MH484867	MH484958	MH485049
	CBS 758.68 = NRRL 36546	S. lycopersicum	lycopersici	The Netherlands	MH484695	MH484786	MH484877	MH484968	MH485059
	CBS 744.79 = BBA 62355 = NRRL 22549	Passiflora edulis	passiflorae	Brazil	MH484700	MH484791	MH484882	MH484973	MH485064
	CBS 127.81 = BBA 63924 = NRRL 36229	Chrysanthemum sp.	chrysanthemi	USA	MH484701	MH484792	MH484883	MH484974	MH485065
	CBS 129.81 = BBA 63926 = NRRL 22539	Chrysanthemum sp.	chrysanthemi	USA	MH484703	MH484794	MH484885	MH484976	MH485067
	CBS 196.87 = NRRL 26219	Bouvardia longiflora	bouvardiae	Italy	MH484704	MH484795	MH484886	MH484977	MH485068
	CBS 840.88T	Dianthus caryophyllus	dianthi	The Netherlands	MH484705	MH484796	MH484887	MH484978	MH485069
	CBS 115416 = CPC 5307	Agathosma betulina		South Africa	MH484720	MH484811	MH484902	MH484993	MH485084
	CBS 115417 = CPC 5306	A. betulina		South Africa	MH484721	MH484812	MH484903	MH484994	MH485085
	CBS 115419 = CPC 5308	A. betulina		South Africa	MH484722	MH484813	MH484904	MH484995	MH485086
	CBS 115424 = CPC 5312	A. betulina		South Africa	MH484724	MH484815	MH484906	MH484997	MH485088
	CBS 123062 = GJS 91-17	Tulip roots		USA	MH484737	MH484828	MH484919	MH485010	MH485101
	CBS 130300 = NRRL 26368	Amputated human toe		USA	MH484743	MH484834	MH484925	MH485016	MH485107
	CBS 130301 = NRRL 26374	Human leg ulcer		USA	MH484744	MH484835	MH484926	MH485017	MH485108
	CBS 130303	S. lycopersicum	radicis-lycopersici	USA	MH484741	MH484832	MH484923	MH485014	MH485105
	CPC 30807			South Africa	MH484768	MH484859	MH484950	MH485041	MH485132
F. odoratissimum	CBS 794.70 = BBA 11103 = NRRL 22550	Albizzia julibrissin	perniciosum	Iran	MH484696	MH484787	MH484878	MH484969	MH485060
	CBS 102030	M. sapientum cv. Pisang mas	cubense	Malaysia	MH484716	MH484807	MH484898	MH484989	MH485080
	CBS 130310 = NRRL 25603	Musa sp.	cubense	Australia	MH484740	MH484831	MH484922	MH485013	MH485104
F. oxysporum	CBS 221.49 = IHEM 4508 = NRRL 22546	Camellia sinensis	medicaginis	South East Asia	MH484690	MH484781	MH484872	MH484963	MH485054
	CBS 144134ET	S. tuberosum		Germany	MH484771	MH484862	MH484953	MH485044	MH485135
	CBS 144135	S. tuberosum		Germany	MH484772	MH484863	MH484954	MH485045	MH485136
	CPC 25822	Protea sp.		South Africa	MH484761	MH484852	MH484943	MH485034	MH485125
F. pharetrum	CBS 144750 = CPC 30822	Aliodendron dichotomum		South Africa	MH484769	MH484860	MH484951	MH485042	MH485133
	CBS 144751 = CPC 30824T	A. dichotomum		South Africa	MH484770	MH484861	MH484952	MH485043	MH485134
F. trachichlamydosporum	CBS 102028 = NRRL 36117	M. sapientum cv. Pisang awak legor	cubense	Malaysia	MH484715	MH484806	MH484897	MH484988	MH485079
F. triseptatum	CBS 258.50 = NRRL 36389T	Ipomoea batatas	batatas	USA	MH484691	MH484782	MH484873	MH484964	MH485055
	CBS 116619	G. hirsutum	vasinfectum	Ivory Coast	MH484728	MH484819	MH484910	MH485001	MH485092
	CBS 119665	Sago starch		Papua New Guinea	MH484734	MH484825	MH484916	MH485007	MH485098
	CBS 130302 = NRRL 26360 = FRC 755	Human eye		USA	MH484742	MH484833	MH484924	MH485015	MH485106
F. udum	CBS 177.31	Digitaria eriantha		South Africa	MH484684	MH484775	MH484866	MH484957	MH485048
F. veterinarium	CBS 109898 = NRRL 36153T	Shark peritoneum		The Netherlands	MH484717	MH484808	MH484899	MH484990	MH485081
	CBS 117787	Swab sample near filling apparatus		The Netherlands	MH484730	MH484821	MH484912	MH485003	MH485094
	CBS 117790	Swab sample near filling apparatus		The Netherlands	MH484731	MH484822	MH484913	MH485004	MH485095
	CBS 117791	Pasteurized milk-based product		The Netherlands	MH484732	MH484823	MH484914	MH485005	MH485096
	CBS 117792	Pasteurized milk-based product		The Netherlands	MH484733	MH484824	MH484915	MH485006	MH485097
	NRRL 54984	Mouse mucosa		USA	MH484763	MH484854	MH484945	MH485036	MH485127
	NRRL 54996	Little blue penguin foot		USA	MH484764	MH484855	MH484946	MH485037	MH485128
	NRRL 62542	Unknown animal faeces		USA	MH484765	MH484856	MH484947	MH485038	MH485129
	NRRL 62545	Endoscope of veterinary clinic		USA	MH484766	MH484857	MH484948	MH485039	MH485130
	NRRL 62547	Canine stomach		USA	MH484767	MH484858	MH484949	MH485040	MH485131
Fusarium sp.	CBS 128.81 = BBA 63925 = NRRL 36233	Chrysanthemum sp.	chrysanthemi	USA	MH484702	MH484793	MH484884	MH484975	MH485066
	CBS 680.89 = NRRL 26221	Cucumis sativus	cucurbitacearum	The Netherlands	MH484707	MH484798	MH484889	MH484980	MH485071
	CBS 130323	Human nail		Australia	MH484745	MH484836	MH484927	MH485018	MH485109

¹ATCC: American Type Culture Collection, USA; BBA: Biologische Bundesanstalt für Land-und Forstwirtschaft, Berlin-Dahlem, Germany; CBS: Westerdijk Fungal Biodiverity Institute (WIFB), Utrecht, The Netherlands; CPC: Collection of P.W. Crous; DSM: Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Braunschweig, Germany; FRC: Fusarium Research Center, Penn State University, Pennsylvania; GJS: Collection of Gary J. Samuels; IHEM: Institute of Hygiene and Epidemiology-Mycology Laboratory, Brussels, Belgium; MRC: National Research Institute for Nutritional Diseases, Tygerberg, South Africa; NRRL: Agricultural Research Service Culture Collection, USA; PD: Collection of the Dutch National Plant Protection Organization, Wageningen, The Netherlands. ^T Ex-type culture; ^ETEpitype.

DNA isolation, PCR and sequencing

Total genomic DNA was extracted from isolates grown for 7 d on PDA at 24 °C using a 12/12 h photoperiod using the Wizard® Genomic DNA purification Kit (Promega Corporation, Madison, WI, USA), according to the manufacturer’s instructions. Partial gene sequences were determined for the β-tubulin (tub2), calmodulin (cmdA), the intergenic spacer region of the rDNA (IGS), RNA polymerase II second largest subunit (rpb2) and translation elongation factor 1-alpha (tef1), using PCR protocols described elsewhere (O’Donnell et al. 1998, 2007, 2009, 2010, Lombard et al. 2015). Primer pairs T1/CYLTUB1R (O’Donnell & Cigelnik 1997, Crous et al. 2004) for tub2, Cal228F/CAL2Rd (Carbone & Kohn 1999, Groenewald et al. 2013) for cmdA, iNL11/iCNS1 and the internal sequencing primers NLa/CNSa (O’Donnell et al. 2009) for IGS, 5f2/7cr (Liu et al. 1999, Sung et al. 2007) for rpb2, and EF1/EF2 (O’Donnell et al. 1998) for tef1, were used for amplifications of the respective gene regions. Integrity of the sequences was ensured by sequencing the amplicons in both directions using the same primer pairs as were used for amplification. Consensus sequences for each locus were assembled in MEGA v. 7 (Kumar et al. 2016), with the exception of the IGS locus, which was assembled in Geneious R11 (Kearse et al. 2012). All sequences generated in this study were deposited in GenBank (Table 1).

Phylogenetic analyses

Sequences of the individual loci were aligned using MAFFT v. 7.110 (Katoh et al. 2017) and manually corrected where necessary. The individual gene datasets were assessed for incongruency prior to concatenation using a 70 % reciprocal bootstrap criterion (Mason-Gamer & Kellogg 1996). Three independent phylogenetic algorithms, Maximum Parsimony (MP), Maximum Likelihood (ML) and Bayesian inference (BI), were employed for phylogenetic analyses. Phylogenetic analyses were conducted for the individual loci and then as a multilocus sequence dataset that included the cmdA, rpb2, tef1 and tub2 sequences.

For BI and ML, the best evolutionary models for each locus were determined using MrModeltest (Nylander 2004) and incorporated into the analyses. MrBayes v. 3.2.1 (Ronquist & Huelsenbeck 2003) was used for BI to generate phylogenetic trees under optimal criteria for each locus. A Markov Chain Monte Carlo (MCMC) algorithm of four chains was initiated in parallel from a random tree topology with the heating parameter set at 0.3. The MCMC analysis lasted until the average standard deviation of split frequencies was below 0.01 with trees saved every 1000 generations. The first 25 % of saved trees were discarded as the ‘burn-in’ phase and posterior probabilities (PP) were determined from the remaining trees.

The ML analyses were performed using RAxML v. 8.2.9 (randomised accelerated (sic) maximum likelihood for high performance computing; Stamatakis 2014) through the CIPRES website (http://www.phylo.org) to obtain another measure of branch support. The robustness of the analysis was evaluated by bootstrap support (BS) with the number of bootstrap replicates automatically determined by the software. For MP, analyses were done using PAUP (Phylogenetic Analysis Using Parsimony, v. 4.0b10; Swofford 2003) with phylogenetic relationships estimated by heuristic searches with 1 000 random addition sequences. Tree-bisection-reconnection was used, with branch swapping option set on ‘best trees’ only. All characters were weighted equally and alignment gaps treated as fifth state. Measures calculated for parsimony included tree length (TL), consistency index (CI), retention index (RI) and rescaled consistence index (RC). Bootstrap (BS) analyses (Hillis & Bull 1993) were based on 1 000 replications. Alignments and phylogenetic trees derived from this study were uploaded to TreeBASE (www.treebase.org).

Genealogical concordance phylogenetic species recognition (GCPSR)

In order to establish the recombination levels between the newly proposed species in this study and their closest phylogenetic relatives, pairwise homoplasy index (PHI) analyses were done on the respective concatenated multilocus datasets (Bruen et al. 2006). The analyses were conducted as described by Quaedvlieg et al. (2014) using SplitsTree v. 4.14.4 (Huson & Bryant 2006). Therefore, a PHI value below 0.05 (ϕ_W < 0.05) would indicate the presence of significant recombination in the dataset. Split graphs were constructed for visualization of the relationships between closely related species.

Morphological characterisation

All isolates were characterised following the protocols described by Leslie & Summerell (2006) using potato dextrose agar (PDA; recipe in Crous et al. 2009), synthetic nutrient-poor agar (SNA; Nirenberg 1976) and carnation leaf agar (CLA; Fisher et al. 1982). Colony morphology, pigmentation, odour and growth rates were evaluated on PDA after 3 and 7 d at 24 °C with a 12/12 h cool fluorescent light/dark cycle as described by Sandoval-Denis et al. (2018) and using the colour charts of Rayner (1970). Micromorphological characters were examined using water as mounting medium on a Zeiss Axioskop 2 plus with Differential Interference Contrast (DIC) optics and a Nikon AZ100 stereomicroscope both fitted with Nikon DS-Ri2 high definition colour digital cameras to photo-document fungal structures. Measurements were taken using the Nikon software NIS-elements D v. 4.50 and the 95 % confidence levels were determined for the conidial measurements with extremes given in parentheses. For all other fungal structures examined, only the extremes are presented. To facilitate the comparison of relevant micro- and macroconidial features, composite photo plates were assembled from separate photographs using PhotoShop CSS.

RESULTS

Isolates

A total of 23 fusarium-like isolates were obtained from the symptomatic tissues of the potato tubers. Of these, six isolates displayed typical F. oxysporum-like phenotypes, of which two (CBS 144134 and CBS 144135) were selected for further study.

Phylogenetic analyses

Approximately 500–650 bases were determined for cmdA, tef1 and tub2, 880 bases for rpb2 and 2 650 bases for IGS. Sequence comparisons of the IGS, rpb2 and tef1 gene regions generated in this study, against those in the Fusarium-ID (http://isolate.fusariumdb.org/blast.php) and Fusarium-MLST (http://www.westerdijkinstitute.nl/fusarium/) databases revealed that all isolates included in this study belonged to the FOSC. The congruency analysis revealed no conflict between the cmdA, rpb2, tef1 and tub2 sequence datasets and were therefore combined. However, the IGS sequence dataset revealed major conflict with several included taxa resolving into single lineages due to the large number of ambiguous regions in this gene region. Therefore, the IGS sequences were excluded from further analyses.

For the BI and ML analyses, a K80 model for cmdA, an HKY+ G+I model for rpb2, an HKY+G for tef1 and SYM+I+G model for tub2 were selected and incorporated into the analyses. The ML tree topology confirmed the tree topologies obtained from the BI and MP analyses, and therefore, only the ML tree is presented.

The combined four loci sequence dataset included 89 ingroup taxa with F. foetens (CBS 120665) and F. udum (CBS 177.31) as outgroup taxa. The dataset consisted of 2 679 characters including gaps. Of these characters, 2 291 were constant, 211 parsimony-uninformative and 177 parsimony-informative. The BI lasted for 1.2 M generations, and the consensus tree and posterior probabilities (PP) were calculated from 8 814 trees left after 2 937 were discarded as the ‘burn-in’ phase. The MP analysis yielded 1 000 trees (TL = 574; CI = 0.747; RI = 0.858; RC = 0.641) and a single best ML tree with -InL = 7353.014512 (Fig. 1).

Fig. 1.

The ML consensus tree inferred from the combined cmdA, rpb2, tef1 and tub2 sequence alignment. Thickened branches indicate branches present in the ML, MP and Bayesian consensus trees. Support values (ML & MP bootstrap and posterior probability values) are indicated at the branches. The scale bar indicates 0.02 expected changes per site. Clade numbers are provided on the right of the tree and these are used for reference in the treatment of the species. The tree is rooted to F. foetens (CBS 120665) and F. udum (CBS 177.31). Epi- and ex-type strains are indicated in bold.

In the phylogenetic tree (Fig. 1) the ingroup taxa resolved into eight clades (I–VIII). Of these, Clades I, II, IV and VI represent single well- (ML & MP-BS ≥ 75–95 %; PP ≥ 0.95–0.98) to highly (ML & MP-BS ≥ 96 %; PP ≥ 0.99–1.0) supported clades, whereas Clades III, V, VII and VIII displayed substantial substructure. Clade III included eight well- to highly supported subclades as well as two single lineages. Sequence comparisons of the rpb2 and tef1 sequences with those generated by Maryani et al. (2019) revealed that both single lineages represented F. duoseptatum (CBS 102026) and F. tradichlamydosporum (CBS 102028), respectively. Similarly, the subclade that include isolates CBS 620.72, CBS 130304, CBS 130308 and CBS 131393 represent F. cugenangense. Both Clades V and VIII resolved two subclades in each, and Clade VII included three subclades. The phylogenetic relationships between Clades I–VIII and their underlying subclades are further discussed in the notes in the Taxonomy section.

The PHI tests revealed that no evidence of recombination (ϕ_W = 0.43; Fig. 2a) was detected between each Clade (I–VIII) and their underlining subclades. Similarly, the genealogical exclusivity of the subclades in Clades III (ϕ_W = 0.43; Fig. 2b) and VII (ϕ_W = 1.0; Fig. 2d), as well as between Clades IV–VIII (ϕ_W = 0.06; Fig. 2c) was also confirmed. The basal subclade in Clade VIII (ϕ_W = 0.031; Fig. 2c), however, showed significant evidence for recombination among all isolates included.

Fig. 2.

Splitgraphs showing the results of the pairwise homoplasy index (PHI) test of newly described taxa using both LogDet transformation and splits decomposition. PHI test results (ϕ_W) < 0.05 indicate significant recombination within the dataset. a. Representatives of all phylogenetic species resolved in this study; b. phylogenetic species in Clade III; c. phylogenetic species in Clades IV–VIII; d. phylogenetic species in Clade VII; e. isolates representing F. nirenbergiae.

Taxonomy

In this section we provide a new (emended) description of F. oxysporum and designate an epitype for this species. The following species are also recognised as new within the FOSC, based on phylogenetic inference and morphological comparisons. Isolates CBS 128.81, CBS 680.89 and CBS 130323 in Clade III are not treated further as these were sterile.

Fusarium callistephi L. Lombard & Crous, sp. nov. — MycoBank MB826833; Fig. 3

Fig. 3.

Fusarium callistephi (ex-type culture CBS 187.53). a–b. Colony on PDA; a. surface of colony on PDA after 7 d at 24 °C under continuous white light; b. reverse of colony on PDA; c. conidiophores on surface of carnation leaf; d. sporodochia on carnation leaves; e–i. conidiophores and phialides on aerial mycelium; j–k. sporodochia and sporodochial conidiophores; l. aerial conidia (microconidia); m. sporodochial conidia (macroconidia). — Scale bars: e–m = 10 μm.

Etymology. Name refers to the plant genus Callistephus from which this fungus was isolated.

Typus. Netherlands, Oostenbrink, from Callistephus chinensis, 28 Feb. 1953, collector unknown (holotype CBS H-23608 designated here, culture ex-type CBS 187.53).

Conidiophores carried on the aerial mycelium 60–110 μm tall, unbranched or sparingly branched, bearing terminal or intercalarily monophialides, often reduced to single phialides; aerial phialides subulate to subcylindrical, smooth- and thin-walled, 2–23 × 3–4 μm, periclinal thickening inconspicuous or absent; aerial conidia forming small false heads on the tips of the phialides, hyaline, ellipsoidal to falcate, smooth- and thin-walled, 0–1-septate; 0-septate conidia: (6–)7–11(–14) × 2–3 μm (av. 9 × 3 μm); 1-septate conidia: (13–)14–18(–20) × 2–4 μm (av. 16 × 3 μm). Sporodochia pale luteous to pale rosy vinaceous, formed abundantly on carnation leaves. Conidiophores in sporodochia verticillately branched and densely packed, consisting of a short, smooth- and thin-walled stipe, 4–7 × 2–4 μm, bearing apical whorls of 2–3 monophialides or rarely as single lateral monophialides; sporodochial phialides subulate to subcylindrical, 9–13 × 3–4 μm, smooth- and thin-walled, sometimes showing a reduced and flared collarette. Sporodochial conidia falcate, curved dorsiventrally with almost parallel sides tapering slightly towards both ends, with a blunt to papillate, curved apical cell and a blunt to foot-like basal cell, 3–4(–5)-septate, hyaline, smooth- and thin-walled; 3-septate conidia: (28–)33–39(–40) × 3–5 μm (av. 36 × 4 μm); 4-septate conidia: (30–)35–41(–42) × 3–5 μm (av. 38 × 4 μm); 5-septate conidia: 36–44(–47) × 4–5 μm (av. 40 × 5 μm). Chlamydospores not observed.

Culture characteristics — Colonies on PDA with an average radial growth rate of 2.9–4.2 mm/d at 24 °C. Colony surface white to pale vinaceous, floccose with abundant aerial mycelium; colony margins irregular, lobate, serrate or filiform. Odour absent. Reverse colourless, lacking diffusible pigment. On SNA, hyphae hyaline, smooth-walled, lacking chlamydospores, aerial mycelium sparse with moderate sporulation on the medium surface. On CLA, aerial mycelium sparse with abundant pale luteous to pale rosy vinaceous sporodochia forming on the carnation leaves.

Additional material examined. South Africa, Western Cape Province, Piketberg, from Agathosma betulina, 2001, K. Lubbe, CBS 115423 = CPC 5311.

Notes — Fusarium callistephi formed a highly-supported subclade in Clade III, closely related to F. cugenangense, F. elaeidis and the untreated Fusarium clade. This species (conidia 3–4(–5)-septate) can be distinguished from F. cugenangense (conidia 3–6-septate; Maryani et al. 2019) and F. elaeidis ((1–)3–5-septate) based on septation of their macroconidia. Additionally, F. cugenangense produces up to 3-septate microconidia, a feature not seen in either F. callistephi or F. elaeidis. Fusarium elaeidis readily formed polyphialidic conidiogenous cells on the aerial mycelium, not seen in F. callistephi.

Fusarium carminascens L. Lombard, Crous & Lampr., sp. nov. — MycoBank MB826835; Fig. 4

Fig. 4.

Fusarium carminascens (ex-type culture CBS 144738). a–b. Colony on PDA; a. surface of colony on PDA after 7 d at 24 °C under continuous white light; b. reverse of colony on PDA; c–d. conidiophores on surface of carnation leaf; e–f. sporodochia on carnation leaves; g–j. conidiophores and phialides on aerial mycelium; g–h. monophialides; i–j. polyphialides; k–l. chlamydospores; m–p. sporodochia and sporodochial conidiophores; o–p. phialides of sporodochial conidiophores; q. aerial conidia (microconidia); r. sporodochial conidia (macroconidia). — Scale bars: g–r = 10 μm.

Etymology. Name refers to the almost carmine exudates this fungus produces in its aerial mycelium when grown on PDA.

Typus. South Africa, KwaZulu-Natal Province, from Zea mays, 2008, S.C. Lamprecht (holotype CBS H-23609 designated here, culture ex-type CBS 144738 = CPC 25800).

Conidiophores carried on the aerial mycelium 35–55 μm tall, unbranched or sparingly branched, bearing terminal or intercalarily phialides, often reduced to single phialides; aerial phialides mono- and polyphialidic, subulate to subcylindrical, smooth- and thin-walled, 8–18 × 3–4 μm, periclinal thickening inconspicuous or absent; aerial conidia forming small false heads on the tips of the phialides, hyaline, ellipsoidal to falcate, smooth- and thin-walled, 0–1-septate; 0-septate conidia: (5–)7–11(–12) × 2–3(–4) μm (av. 9 × 3 μm); 1-septate conidia: (12–)13–15(–18) × 2–4 μm (av. 14 × 3 μm). Sporodochia bright orange, formed abundantly on carnation leaves. Conidiophores in sporodochia verticillately branched and densely packed, consisting of a short, smooth- and thin-walled stipe, 4–9 × 2–4 μm, bearing apical whorls of 2–3 monophialides or rarely as single lateral monophialides; sporodochial phialides subulate to subcylindrical, 5–13 × 2–4 μm, smooth- and thin-walled, sometimes showing a reduced and flared collarette. Sporodochial conidia falcate, curved dorsiventrally with almost parallel sides tapering slightly towards both ends, with a blunt to papillate, curved apical cell and a blunt to foot-like basal cell, (2–)3–4(–5)-septate, hyaline, smooth- and thin-walled; 2-septate conidia: 16–19 × 3–4 μm (av. 18 × 3 μm); 3-septate conidia: (21–)26–36(–40) × 3–5 μm (av. 31 × 4 μm); 4-septate conidia: (31–)33–43(–44) × 4–5 μm (av. 38 × 4 μm); 5-septate conidia: 45–51 × 4 μm (av. 48 × 4 μm). Chlamydospores globose to subglobose, formed terminally, 4–8 μm diam.

Culture characteristics — Colonies on PDA with an average radial growth rate of 3.1–4.0 mm/d at 24 °C. Colony surface vinaceous purple to livid purple, floccose with abundant aerial mycelium which produce an almost carmine exudate; colony margins irregular, lobate, serrate or filiform. Odour absent. Reverse dark livid to livid purple, lacking diffusible pigment. On SNA, hyphae hyaline, smooth-walled, with abundant chlamydospores, aerial mycelium sparse with abundant sporulation on the medium surface. On CLA, aerial mycelium sparse with abundant bright orange sporodochia forming on the carnation leaves.

Additional materials examined. South Africa, KwaZulu-Natal Province, from Zea mays, 2008, S.C. Lamprecht, CBS 144739 = CPC 25792, CBS 144740 = CPC 25793, CBS 144741 = CPC 25795.

Notes — Fusarium carminascens formed a well-supported subclade in Clade III, closely related to F. fabacearum and F. glycines. This species produced an almost carmine coloured exudate in its aerial mycelium, a feature not observed in any of the other strains studied here. Furthermore, F. carminascens produces polyphialidic conidiogenous cells on its aerial mycelium, not observed in F. fabacearum or F. glycines.

Fusarium contaminatum L. Lombard & Crous, sp. nov. — Myco-Bank MB826836; Fig. 5

Fig. 5.

Fusarium contaminatum (ex-type culture CBS 114899). a–b. Colony on PDA; a. Surface of colony on PDA after 7 d at 24 °C under continuous white light; b. reverse of colony on PDA; c–d. conidiophores on surface of carnation leaf; e–f. sporodochia on carnation leaves; g–k. conidiophores and phialides on aerial mycelium; l. false head carried on phialide on aerial mycelium; m–p. sporodochia and sporodochial conidiophores; q. aerial conidia (microconidia); r. sporodochial conidia (macroconidia). — Scale bars: g–l, q–r = 10 μm; m–p = 20 μm.

Etymology. Name refers to the fact that this fungus was isolated from contaminated food products.

Typus. Germany, Schluchtern, from pasteurized chocolate milk, Apr. 2004, J. Houbraken (holotype CBS H-23610 designated here, culture ex-type CBS 114899).

Conidiophores carried on the aerial mycelium 15–85 μm tall, unbranched or branched, bearing a single terminal or a whorl of 2–4 monophialides or intercalarily monophialides, often reduced to single phialides; aerial phialides subulate to subcylindrical, smooth- and thin-walled, 7–22 × 2–5 μm, periclinal thickening inconspicuous or absent; aerial conidia forming small false heads on the tips of the phialides, hyaline, ellipsoidal to falcate, smooth- and thin-walled, 0–1-septate; 0-septate conidia: 5–9(–11) × 2–4 μm (av. 7 × 3 μm); 1-septate conidia: (9–)10–14(–17) × 2–4 μm (av. 12 × 3 μm). Sporodochia bright orange, formed sparsely on carnation leaves. Conidiophores in sporodochia verticillately branched and densely packed, consisting of a short, smooth- and thin-walled stipe, 7–13 × 4 μm, bearing apical whorls of 2–3 monophialides or rarely as single lateral monophialides; sporodochial phialides subulate to subcylindrical, 4–9 × 2–3 μm, smooth- and thin-walled, sometimes showing a reduced and flared collarette. Sporodochial conidia falcate, curved dorsiventrally with almost parallel sides tapering slightly towards both ends, with a blunt to papillate, curved apical cell and a blunt to foot-like basal cell, (2–)3-septate, hyaline, smooth- and thin-walled; 2-septate conidia: (14–)15–17 × 3–4 μm (av. 16 × 3 μm); 3-septate conidia: (18–)20–26(–28) × 3–5 μm (av. 23 × 4 μm). Chlamydospores not observed.

Culture characteristics — Colonies on PDA with an average radial growth rate of 3.1–4.5 mm/d at 24 °C. Colony surface white to pale vinaceous, floccose with abundant aerial mycelium; colony margins irregular, lobate, serrate or filiform. Odour absent. Reverse rosy vinaceous, lacking diffusible pigment. On SNA, hyphae hyaline, smooth-walled, lacking chlamydospores, aerial mycelium sparse with abundant sporulation on the medium surface. On CLA, aerial mycelium sparse with abundant orange sporodochia forming on the carnation leaves.

Additional materials examined. Netherlands, from pasteurized fruit juice, date and collector unknown, CBS 111552; from tetra pack with milky nutrition, 2005, collector unknown, CBS 117461.

Notes — Fusarium contaminatum formed a highly-supported subclade in Clade VII, closely related to F. pharetrum and F. veterinarium. This species produces small, 2–3-septate macroconidia, whereas F. pharetrum produces much larger, 3(–4)-septate macroconidia and F. veterinarium produces slightly smaller, 1–(2–)3-septate macroconidia. None of these three species produced any chlamydospores on SNA.

Fusarium curvatum L. Lombard & Crous, sp. nov. — MycoBank MB826837; Fig. 6

Fig. 6.

Fusarium curvatum (ex-type culture CBS 238.94). a–b. Colony on PDA; a. surface of colony on PDA after 7 d at 24 °C under continuous white light; b. reverse of colony on PDA; c–d. conidiophores on surface of carnation leaf; e–f. sporodochia on carnation leaves; g–i. conidiophores, monophialides and polyphialides (arrows) on aerial mycelium; j. phialidic pegs on aerial mycelium; k–o. sporodochia and sporodochial conidiophores; p. aerial conidia (microconidia); q. sporodochial conidia (macroconidia). — Scale bars: g–i, n = 20 μm; j, o–q = 10 μm, k–m = 50 μm.

Etymology. Name refers to the strongly curved sporodochial conidia produced by this fungus.

Typus. Netherlands, from Beaucarnia sp., 1994, J.W. Veenbaas-Rijks (holo-type CBS H-23611 designated here, culture ex-type CBS 238.94 = NRRL 26422 = PD 94/184).

Conidiophores carried on the aerial mycelium 25–56 μm tall, unbranched or sparingly branched, bearing terminal or intercalarily phialides, often reduced to single phialides or as phialidic pegs; aerial phialides mono- and polyphialidic, subulate to subcylindrical, smooth- and thin-walled, 3–30 × 2–5 μm, periclinal thickening inconspicuous or absent; aerial conidia forming small false heads on the tips of the phialides, hyaline, ellipsoidal to falcate, smooth- and thin-walled, 0–1-septate; 0-septate conidia: (4–)5–9(–11) × 2–4 μm (av. 7 × 3 μm); 1-septate conidia: (10–)11–13 × 2–4 μm (av. 12 × 3 μm). Sporodochia orange, formed abundantly on carnation leaves. Conidiophores in sporodochia verticillately branched and densely packed, consisting of a short, smooth- and thin-walled stipe, 8–10 × 2–4 μm, bearing apical whorls of 2–3 monophialides or rarely as single lateral monophialides; sporodochial phialides subulate to subcylindrical, 8–22 × 2–4 μm, smooth- and thin-walled, sometimes showing a reduced and flared collarette. Sporodochial conidia falcate, strongly curved or curved dorsiventrally with almost parallel sides tapering slightly towards both ends, with a blunt to papillate, curved apical cell and a blunt to foot-like basal cell, (2–)3–5-septate, hyaline, smooth- and thin-walled; 2-septate conidia: (15–)16–22(–23) × 3–4 μm (av. 19 × 3 μm); 3-septate conidia: (18–)27–39(–41) × 3–5 μm (av. 33 × 4 μm); 4-septate conidia: (34–)37–43(–46) × 3–5 μm (av. 40 × 4 μm); 5-septate conidia: (30–)38–46(–51) × 3–5 μm (av. 42 × 4 μm). Chlamydospores not observed.

Culture characteristics — Colonies on PDA with an average radial growth rate of 3.1–4.5 mm/d at 24 °C. Colony surface pale vinaceous to rosy vinaceous, floccose with abundant aerial mycelium; colony margins irregular, lobate, serrate or filiform. Odour absent. Reverse pale vinaceous, lacking diffusible pigment. On SNA, hyphae hyaline, smooth-walled, lacking chlamydospores, aerial mycelium sparse with abundant sporulation on the medium surface. On CLA, aerial mycelium sparse with abundant orange sporodochia forming on the carnation leaves.

Additional materials examined. Germany, Berlin-Dahlem, from Matthiola incana, Feb. 1957, W. Gerlach, CBS 247.61 = BBA 8398 = DSM 62308 = NRRL 22545. – Netherlands, from Hedera helix, 1994, J.W. Veenbaas-Rijks, CBS 141.95 = NRRL 36251 = PD 94/1518.

Notes — Fusarium curvatum formed a highly-supported subclade in Clade VIII, closely related to F. nirenbergiae. This species produces strongly curved 3-septate macroconidia and aerial polyphialidic conidiogenous cells, distinguishing it from F. nirenbergiae. Additionally, F. curvatum failed to produce any chlamydospores on SNA, whereas F. nirenbergiae produced abundant chlamydospores.

Fusarium elaeidis L. Lombard & Crous, sp. nov. — MycoBank MB826838; Fig. 7

Fig. 7.

Fusarium elaeidis (ex-type culture CBS 217.49). a–b. Colony on PDA; a. surface of colony on PDA after 7 d at 24 °C under continuous white light; b. reverse of colony on PDA; c–d. conidiophores on surface of carnation leaf; e–f. sporodochia on carnation leaves; g. false head carried on a phialidic peg on aerial mycelium; h. phialidic peg; i–j. conidiophores and phialides on aerial mycelium; j. polyphialide; k–l. sporodochia and sporodochial conidiophores; m. aerial conidia (microconidia); n. sporodochial conidia (macroconidia). — Scale bars: g–n = 10 μm.

Etymology. Name refers to the host plant genus Elaeis, from which this fungus was first isolated.

Typus. Zaire, from Elaeis sp., 1949, T. Gogoi (holotype CBS H-23612 designated here, culture ex-type CBS 217.49 = NRRL 36358).

Conidiophores carried on the aerial mycelium 25–65 μm tall, unbranched or sparingly branched, bearing terminal or intercalarily phialides, often reduced to single phialides or as phialidic pegs; aerial phialides mono- and polyphialidic, subulate to subcylindrical, smooth- and thin-walled, 3–14 × 3–4 μm, periclinal thickening inconspicuous or absent; aerial conidia forming small false heads on the tips of the phialides, hyaline, ellipsoidal to falcate, smooth- and thin-walled, 0–1-septate; 0-septate conidia: 6–10(–13) × 2–3 μm (av. 8 × 3 μm); 1-septate conidia: (9–)11–15(–17) × 2–4(–5) μm (av. 13 × 3 μm). Sporodochia pale rosy vinaceous to orange, formed abundantly on carnation leaves. Conidiophores in sporodochia verticillately branched and densely packed, consisting of a short, smooth- and thin-walled stipe, 3–9 × 2–3 μm, bearing apical whorls of 2–3 monophialides or rarely as single lateral monophialides; sporodochial phialides subulate to subcylindrical, 8–12 × 2–4 μm, smooth- and thin-walled, sometimes showing a reduced and flared collarette. Sporodochial conidia falcate, curved dorsiventrally with almost parallel sides tapering slightly towards both ends, with a blunt to papillate, curved apical cell and a blunt to foot-like basal cell, (1–)3–5-septate, hyaline, smooth- and thin-walled; 1-septate conidia: (14–)15–25(–32) × 2–4 μm (av. 20 × 3 μm); 2-septate conidia: (17–)19–25 × 3–4 μm (av. 22 × 4 μm); 3-septate conidia: (22–)30–40(–46) × (2–)3–4 μm (av. 35 × 4 μm); 4-septate conidia: (34–)36–40(–43) × 3–5 μm (av. 38 × 4 μm); 5-septate conidia: (36–)37–43(–50) × 3–5 μm (av. 40 × 4 μm). Chlamydospores not observed.

Culture characteristics — Colonies on PDA with an average radial growth rate of 2.6–3.4 mm/d at 24 °C. Colony surface pale rosy vinaceous grey, floccose with abundant aerial mycelium; colony margins irregular, lobate, serrate or filiform. Odour absent. Reverse pale rosy vinaceous, lacking diffusible pigment. On SNA, hyphae hyaline, smooth-walled, lacking chlamydospores, aerial mycelium sparse with abundant sporulation on the medium surface. On CLA, aerial mycelium sparse with abundant pale rosy vinaceous to orange sporodochia forming on the carnation leaves.

Additional materials examined. Zaire, from Elaeis sp., 1949, T. Gogoi, CBS 218.49 = NRRL 36359. – Unknown locality, from Elaeis guineensis, 1952, J. Fraselle, CBS 255.52 = NRRL 36386.

Notes — Fusarium elaeidis formed a highly-supported subclade in Clade III, closely related to F. callistephi, F. cugenangense and the untreated Fusarium clade. See notes under F. callistephi for distinguishing morphological features.

Fusarium fabacearum L. Lombard, Crous & Lampr., sp. nov. — MycoBank MB826839; Fig. 8

Fig. 8.

Fusarium fabacearum (ex-type culture CBS 144743). a–b. Colony on PDA; a. surface of colony on PDA after 7 d at 24 °C under continuous white light; b. reverse of colony on PDA; c. conidiophores on surface of carnation leaf; d. sporodochia on carnation leaves; e. false head carried on a phialide on aerial mycelium; f–h. conidiophores and phialides on aerial mycelium; i–k. sporodochia and sporodochial conidiophores; l. chlamydospore; m. aerial conidia (microconidia); n. sporodochial conidia (macroconidia). — Scale bars: e–h, k–n = 10 μm; i–j = 50 μm.

Etymology. Name refers to the plant family, Fabaceae, which includes the plant host Glycine max from which this fungus was first isolated.

Typus. South Africa, North West Province, from Glycine max, 2010, S.C. Lamprecht (holotype CBS H-23613 designated here, culture ex-type CBS 144743 = CPC 25802).

Conidiophores carried on the aerial mycelium 25–50 μm tall, unbranched or sparingly branched, bearing terminal or intercalarily monophialides, often reduced to single phialides; aerial phialides subulate to subcylindrical, smooth- and thin-walled, 11–15 × 3–4 μm, periclinal thickening inconspicuous or absent; aerial conidia forming small false heads on the tips of the phialides, hyaline, ellipsoidal to falcate, smooth- and thin-walled, 0–1-septate; 0-septate conidia: (4–)5–9(–13) × 2–3 μm (av. 7 × 3 μm); 1-septate conidia: (12–)13–15(–16) × 3–4 μm (av. 14 × 3 μm). Sporodochia pale luteous to orange, formed abundantly on carnation leaves. Conidiophores in sporodochia verticillately branched and densely packed, consisting of a short, smooth- and thin-walled stipe, 4–7 × 3 μm, bearing apical whorls of 2–3 monophialides or rarely as single lateral monophialides; sporodochial phialides subulate to subcylindrical, 7–10 × 2–4 μm, smooth- and thin-walled, sometimes showing a reduced and flared collarette. Sporodochial conidia falcate, curved dorsiventrally with almost parallel sides tapering slightly towards both ends, with a blunt to papillate, curved apical cell and a blunt to foot-like basal cell, (1–)3–4(–5)-septate, hyaline, smooth- and thin-walled; 1-septate conidia: (15–)16–24(–25) × 3–4 μm (av. 20 × 3 μm); 3-septate conidia: (24–)27–33(–36) × (2–)3–5 μm (av. 30 × 4 μm); 4-septate conidia: (32–)33–37(–40) × 3–5 μm (av. 35 × 4 μm); 5-septate conidia: (35–)38–44 × 3–4 μm (av. 41 × 4 μm). Chlamydospores globose to subglobose, formed terminally, 5–8 μm diam.

Culture characteristics — Colonies on PDA with an average radial growth rate of 3.0–4.4 mm/d at 24 °C. Colony surface pale vinaceous grey to vinaceous grey, floccose with abundant aerial mycelium; colony margins irregular, lobate, serrate or filiform. Odour absent. Reverse pale vinaceous grey, lacking diffusible pigment. On SNA, hyphae hyaline, smooth-walled, with abundant chlamydospores, aerial mycelium sparse with abundant sporulation on the medium surface. On CLA, aerial mycelium sparse with abundant pale luteous to orange sporodochia forming on the carnation leaves.

Additional materials examined. South Africa, North West Province, from Glycine max, 2010, S.C. Lamprecht, CBS 144744 = CPC 25803; from Zea mays, 2008, C.M. Bezuidenhout, CBS 144742 = CPC 25801.

Notes — Fusarium fabacearum formed a highly-supported subclade in Clade III, closely related to F. carminascens and F. glycines. See notes under F. carminascens for distinguishing morphological features.

Fusarium glycines L. Lombard, Crous & Lampr., sp. nov. — MycoBank MB826840; Fig. 9

Fig. 9.

Fusarium glycines (ex-type culture CBS 144746). a–b. Colony on PDA; a. surface of colony on PDA after 7 d at 24 °C under continuous white light; b. reverse of colony on PDA; c–d. conidiophores on surface of carnation leaf; e–f. sporodochia on carnation leaves; g–i. conidiophores and phialides on aerial mycelium; j–k. sporodochia and sporodochial conidiophores; l. chlamydospore; m. aerial conidia (microconidia); n. sporodochial conidia (macroconidia). — Scale bars: g–i, l–n = 10 μm; j–k = 50 μm.

Etymology. Name refers to the plant genus Glycine from which this fungus was isolated.

Typus. South Africa, North West Province, from Glycine max, 2010, S.C. Lamprecht (holotype CBS H-23614 designated here, culture ex-type CBS 144746 = CPC 25808).

Conidiophores carried on the aerial mycelium 5–45 μm tall, unbranched or sparingly branched, bearing terminal or intercalarily monophialides, often reduced to single phialides; aerial phialides subulate to subcylindrical, smooth- and thin-walled, 15–25 × 2–4 μm, periclinal thickening inconspicuous or absent; aerial conidia forming small false heads on the tips of the phialides, hyaline, ellipsoidal to falcate, smooth- and thin-walled, 0–1-septate; 0-septate conidia: 7–11(–13) × 3–4 μm (av. 9 × 3 μm); 1-septate conidia: (13–)14–16(–18) × 3–4 μm (av. 15 × 3 μm). Sporodochia bright orange, formed abundantly on carnation leaves. Conidiophores in sporodochia verticillately branched and densely packed, consisting of a short, smooth- and thinwalled stipe, 4–9 × 2–4 μm, bearing apical whorls of 2–3 monophialides or rarely as single lateral monophialides; sporodochial phialides subulate to subcylindrical, 12–14 × 2–5 μm, smooth- and thin-walled, sometimes showing a reduced and flared collarette. Sporodochial conidia falcate, curved dorsiventrally with almost parallel sides tapering slightly towards both ends, with a blunt to papillate, curved apical cell and a blunt to foot-like basal cell, (1–)3–5-septate, hyaline, smooth- and thin-walled; 1-septate conidia: 20–25 × 3–4 μm (av. 23 × 3 μm); 3-septate conidia: 37–43(–48) × 4–5 μm (av. 38 × 4 μm); 4-septate conidia: 44–46(–51) × 4–5 μm (av. 42 × 4 μm); 5-septate conidia: 43–49(–52) × 4–5 μm (av. 46 × 4 μm).

Chlamydospores globose to subglobose, formed terminally, 4–8 μm diam.

Culture characteristics — Colonies on PDA with an average radial growth rate of 3.0–4.4 mm/d at 24 °C. Colony surface vinaceous, floccose with abundant aerial mycelium; colony margins irregular, lobate, serrate or filiform. Odour absent. Reverse vinaceous, lacking diffusible pigment. On SNA, hyphae hyaline, smooth-walled, with abundant chlamydospores, aerial mycelium sparse with abundant sporulation on the medium surface. On CLA, aerial mycelium sparse with abundant bright orange sporodochia forming on the carnation leaves.

Additional materials examined. Argentina, substrate unknown, date unknown, C.J.M. Carrera, CBS 214.49 = NRRL 36356 = LCF F-245. – Italy, from Ocimum basilicum, 1989, G. Tamiette & A. Matta, CBS 200.89. – South Africa, North West Province, from Glycine max, 2010, S.C. Lamprecht, CBS 144745 = CPC 25804. – Unknown locality, from Linum usitatissium, 1933, E.C. Stakman, CBS 176.33 = NRRL 36286.

Notes — Fusarium glycines formed a highly-supported subclade in Clade III, closely related to F. carminascens and F. fabacearum. See notes under F. carminascens for distinguishing morphological features.

Fusarium gossypinum L. Lombard & Crous, sp. nov. — MycoBank MB826841; Fig. 10

Fig. 10.

Fusarium gossypinum (ex-type culture CBS 116613). a–b. Colony on PDA; a. surface of colony on PDA after 7 d at 24 °C under continuous white light; b. reverse of colony on PDA; c–d. conidiophores on surface of carnation leaf; e. false head carried on a phialide on aerial mycelium; f–h. conidiophores and phialides on aerial mycelium; i. aerial conidia (microconidia); j. sporodochial conidia (macroconidia). — Scale bars: e = 20 μm; f–j = 10 μm.

Etymology. Name refers to the plant genus Gossypium from which this fungus was isolated.

Typus. Ivory Coast, Bouaké, wilted Gossypium hirsutum, Sept. 1995, K. Abo (holotype CBS H-23615 designated here, culture ex-type CBS 116613).

Conidiophores carried on the aerial mycelium 35–75 μm tall, unbranched or sparingly branched, bearing terminal or intercalarily monophialides, often reduced to single phialides; aerial phialides subulate to subcylindrical, smooth- and thin-walled, 3–30 × 2–4 μm, periclinal thickening inconspicuous or absent. Microconidia forming small false heads on the tips of the phialides, hyaline, ellipsoidal to falcate, smooth- and thin-walled, 0–1-septate; 0-septate conidia: (5–)6–8(–11) × 2–4 μm (av. 7 × 3 μm); 1-septate conidia: (11–)12–14(–15) × 2–4 μm (av. 15 × 3 μm). Macroconidia also formed by phialides on aerial mycelium, falcate, curved dorsiventrally with almost parallel sides tapering slightly towards both ends, with a blunt to papillate, curved apical cell and a blunt to foot-like basal cell, (1–)3-septate, hyaline, smooth- and thin-walled; 1-septate conidia: 16–18 × 3 μm (av. 17 × 3 μm); 2-septate conidia: 21–23 × 3–4 μm (av. 22 × 3 μm); 3-septate conidia: (24–)27–35(–38) × 3–4 μm (av. 31 × 4 μm). Sporodochia absent. Chlamydospores not observed.

Culture characteristics — Colonies on PDA with an average radial growth rate of 1.6–2.8 mm/d at 24 °C. Colony surface white to pale rosy vinaceous, floccose with abundant aerial mycelium; colony margins irregular, lobate, serrate or filiform. Odour absent. Reverse pale rosy vinaceous, lacking diffusible pigment. On SNA, hyphae hyaline, smooth-walled, lacking chlamydospores, aerial mycelium sparse with abundant sporulation on the medium surface. On CLA, aerial mycelium sparse lacking sporodochia on the carnation leaves.

Additional materials examined. Ivory Coast, Bouaké, wilted Gossypium hirsutum, Sept. 1995, K. Abo, CBS 116611 and CBS 116612.

Notes — Fusarium gossypinum formed a unique highly-supported subclade in Clade III. This species failed to produce any sporodochia on the carnation leaf pieces, but still produced abundant 3-septate macroconidia on the aerial mycelium. Other species included in Clade III, all readily produced sporodochia on carnation leaves.

Fusarium hoodiae L. Lombard, Crous & Lampr., sp. nov. — MycoBank MB826842; Fig. 11

Fig. 11.

Fusarium hoodiae (ex-type culture CBS 132474). a–b. Colony on PDA; a. surface of colony on PDA after 7 d at 24 °C under continuous white light; b. reverse of colony on PDA; c–d. conidiophores on surface of carnation leaf; e–f. sporodochia on carnation leaves; g–h. conidiophores and phialides on aerial mycelium; i–k. sporodochia and sporodochial conidiophores; l. chlamydospore; m. aerial conidia (microconidia); n. sporodochial conidia (macroconidia). — Scale bars: g–h, l–n = 10 μm; i = 50 μm; j–k = 20 μm.

Etymology. Name refers to the plant genus Hoodia from which this fungus was isolated.

Typus. South Africa, Northern Cape Province, Prieska, root of Hoodia gordonii, 2002, O.A. Philippou (holotype CBS H-23616 designated here, culture ex-type CBS 132474).

Conidiophores carried on the aerial mycelium 40–60 μm tall, unbranched or sparingly branched, bearing terminal or intercalarily monophialides, often reduced to single phialides; aerial phialides subulate to subcylindrical, smooth- and thin-walled, 15–24 × 2–3 μm, periclinal thickening inconspicuous or absent; aerial conidia forming small false heads on the tips of the phialides, hyaline, ellipsoidal to falcate, smooth- and thin-walled, 0–1-septate; 0-septate conidia: (5–)6–10(–16) × 2–4 μm (av. 8 × 3 μm); 1-septate conidia: (11–)12–16(–17) × 3–4 μm (av. 14 × 3 μm). Sporodochia pale vinaceous to light orange, formed abundantly on carnation leaves. Conidiophores in sporodochia verticillately branched and densely packed, consisting of a short, smooth- and thin-walled stipe, 7–11 × 3–5 μm, bearing apical whorls of 2–3 monophialides or rarely as single lateral monophialides; sporodochial phialides subulate to subcylindrical, 7–13 × 2–5 μm, smooth- and thin-walled, sometimes showing a reduced and flared collarette. Sporodochial conidia falcate, curved dorsiventrally with almost parallel sides tapering slightly towards both ends, with a blunt to papillate, curved apical cell and a blunt to foot-like basal cell, (1–)3(–4)-septate, hyaline, smooth- and thin-walled; 1-septate conidia: 20–33 × 3–5 μm (av. 25 × 4 μm); 3-septate conidia: (20–)27–39(–45) × 3–5 μm (av. 33 × 4 μm); 4-septate conidia: (35–)36–46(–51) × 4–5 μm (av. 41 × 5 μm). Chlamydospores globose to subglobose, formed terminally, 4–11 μm diam.

Culture characteristics — Colonies on PDA with an average radial growth rate of 3.1–4.5 mm/d at 24 °C. Colony surface pale vinaceous grey to livid vinaceous, floccose with abundant aerial mycelium; colony margins irregular, lobate, serrate or filiform. Odour absent. Reverse livid purple to pale vinaceous grey, lacking diffusible pigment. On SNA, hyphae hyaline, smooth-walled, with abundant chlamydospores, aerial mycelium sparse with abundant sporulation on the medium surface. On CLA, aerial mycelium sparse with abundant pale vinaceous to light orange sporodochia forming on the carnation leaves.

Additional materials examined. South Africa, Northern Cape Province, Prieska, root of Hoodia gordonii, 2002, O.A. Philippou, CBS 132476, CBS 132477.

Notes — Fusarium hoodiae formed a weakly supported clade constituting Clade IV in this phylogenetic study. All three isolates studied here, produced pale vinaceous to pale orange sporodochia on the carnation leaf pieces, unique for all the isolates studied.

Fusarium languescens L. Lombard & Crous, sp. nov. — MycoBank MB826843; Fig. 12

Fig. 12.

Fusarium languescens (ex-type culture CBS 645.78). a–b. Colony on PDA; a. surface of colony on PDA after 7 d at 24 °C under continuous white light; b. reverse of colony on PDA; c. conidiophores on surface of carnation leaf; d. sporodochia on carnation leaves; e–h. conidiophores and phialides on aerial mycelium; i–k. sporodochia and sporodochial conidiophores; l. chlamydospore; m. aerial conidia (microconidia); n. sporodochial conidia (macroconidia). — Scale bars: e–h, l–n = 10 μm; i–k = 20 μm.

Etymology. Name refers to the wilting symptoms associated with infections of this fungus.

Typus. Morocco, Solanum lycopersicum, date and collector unknown (holo-type CBS H-23617 designated here, culture ex-type CBS 645.78 = NRRL 36531).

Conidiophores carried on the aerial mycelium 25–30 μm tall, unbranched or sparingly branched, bearing terminal or intercalarily monophialides, often reduced to single phialides; aerial phialides subulate to subcylindrical, smooth- and thin-walled, 7–22 × 2–4 μm, periclinal thickening inconspicuous or absent; aerial conidia forming small false heads on the tips of the phialides, hyaline, ellipsoidal to falcate, smooth- and thin-walled, 0–1-septate; 0-septate conidia: (4–)5–9(–12) × 2–3 μm (av. 7 × 3 μm); 1-septate conidia: (9–)11–15 × 2–4 μm (av. 13 × 3 μm). Sporodochia light orange, formed abundantly on carnation leaves. Conidiophores in sporodochia verticillately branched and densely packed, consisting of a short, smooth- and thin-walled stipe, 5–10 × 3–4 μm, bearing apical whorls of 2–3 monophialides or rarely as single lateral monophialides; sporodochial phialides subulate to subcylindrical, 10–14 × 2–4 μm, smooth- and thin-walled, sometimes showing a reduced and flared collarette. Sporodochial conidia falcate, curved dorsiventrally with almost parallel sides tapering slightly towards both ends, with a blunt to papillate, curved apical cell and a blunt to foot-like basal cell, 1–3(–5)-septate, hyaline, smooth- and thin-walled; 1-septate conidia: (15–)18–23(–30) × 3–4 μm (av. 20 × 3 μm); 2-septate conidia: (14–)16–22(–24) × 4 μm (av. 19 × 3 μm); 3-septate conidia: (22–)26–38(–47) × 3–5 μm (av. 32 × 4 μm); 5-septate conidia: 32–40 × 4–5 μm (av. 36 × 5 μm). Chlamydospores globose to subglobose, formed terminally, 6–9 μm diam.

Culture characteristics — Colonies on PDA with an average radial growth rate of 3.1–4.5 mm/d at 24 °C. Colony surface flesh to rosy vinaceous, floccose with abundant aerial mycelium; colony margins irregular, lobate, serrate or filiform. Odour absent. Reverse pale luteous, lacking diffusible pigment. On SNA, hyphae hyaline, smooth-walled, with abundant chlamydospores, aerial mycelium sparse with abundant sporulation on the medium surface. On CLA, aerial mycelium sparse with abundant light orange sporodochia forming on the carnation leaves.

Additional materials examined. Israel, Bet Dagan, Solanum lycopersicum, 1986, R. Cohn, CBS 413.90 = ATCC 66046 = NRRL 36465. – Morocco, Solanum lycopersicum, date and collector unknown, CBS 646.78 = NRRL 36532. – Netherlands, Solanum lycopersicum, 1991, D.H. Elgersma, CBS 300.91 = NRRL 36416, CBS 302.91 = NRRL 36419. – South Africa, Zea mays, date and collector unknown, CBS 119796 = MRC 8437. – Unknown locality, Solanum lycopersicum, date and collector unknown, CBS 872.95 = NRRL 36570.

Notes — Fusarium languescens forms the highly-supported Clade VI, which mostly includes strains associated with tomato wilt. This species displays morphological overlap with several species treated here. Therefore, phylogenetic inference is needed to accurately identify this species.

Fusarium libertatis L. Lombard, Crous, sp. nov. — MycoBank MB826844; Fig. 13

Fig. 13.

Fusarium libertatis (ex-type culture CBS 144749). a–b. Colony on PDA; a. surface of colony on PDA after 7 d at 24 °C under continuous white light; b. reverse of colony on PDA; c–e. conidiophores on surface of carnation leaf; g–k. conidiophores and phialides on aerial mycelium; g–h. monophialides; i–k. polyphialides; l–n. sporodochia and sporodochial conidiophores; n. phialides of sporodochial conidiophores; o–p. chlamydospores; q. aerial conidia (microconidia); r. sporodochial conidia (macroconidia). — Scale bars: c–r = 10 μm.

Etymology. Name refers to ‘freedom’. Fusarium libertatis was isolated from the rock surfaces in the stone quarry on Robben Island where the prisoners were forced to work. It is named in remembrance of all those who through the centuries were incarcerated on the Island for their different political beliefs.

Typus. South Africa, Western Cape Province, Robben Island, Van Riebeeck’s Quarry, from rock surfaces, May 2015, P.W. Crous (holotype CBS H-23618 designated here, culture ex-type CBS 144749 = CPC 28465).

Conidiophores carried on the aerial mycelium 2–30 μm tall, unbranched or sparingly branched, bearing terminal or intercalarily phialides, often reduced to single phialides; aerial phialides mono- and polyphialidic, subulate to subcylindrical, smooth- and thin-walled, 8–13 × 2–4 μm, sometimes proliferating percurrently, periclinal thickening inconspicuous or absent; aerial conidia forming small false heads on the tips of the phialides, hyaline, ellipsoidal to falcate, smooth- and thin-walled, 0–1-septate; 0-septate conidia: (6–)7–9(–11) × 2–4 μm (av. 8 × 3 μm); 1-septate conidia: (11–)12–14(–15) × 2–4 μm (av. 13 × 3 μm). Sporodochia bright orange, formed abundantly on carnation leaves. Conidiophores in sporodochia verticillately branched and densely packed, consisting of a short, smooth- and thin-walled stipe, 4–8 × 3–4 μm, bearing apical whorls of 2–3 monophialides or rarely as single lateral monophialides; sporodochial phialides subulate to subcylindrical, 6–12 × 2–4 μm, smooth- and thin-walled, sometimes showing a reduced and flared collarette. Sporodochial conidia falcate, curved dorsiventrally with almost parallel sides tapering slightly towards both ends, with a blunt to papillate, curved apical cell and a blunt to foot-like basal cell, 1–3-septate, hyaline, smooth- and thin-walled; 1-septate conidia: (15–)17–21(–23) × 2–4 μm (av. 19 × 3 μm); 2-septate conidia: (18–)20–24(–25) × 2–3(–4) μm (av. 22 × 4 μm); 3-septate conidia: (24–)30–38(–40) × (2–)3–5 μm (av. 34 × 4 μm). Chlamydospores globose to subglobose, formed terminally and intercalarily, carried singly, 5–9 μm diam.

Culture characteristics — Colonies on PDA with an average radial growth rate of 2.3–4.4 mm/d at 24 °C. Colony surface vinaceous, floccose with abundant aerial mycelium; colony margins irregular, lobate, serrate or filiform. Odour absent. Reverse vinaceous, lacking diffusible pigment. On SNA, hyphae hyaline, smooth-walled, with abundant chlamydospores, aerial mycelium sparse with abundant sporulation on the medium surface. On CLA, aerial mycelium sparse with abundant bright orange sporodochia forming on the carnation leaves.

Additional materials examined. South Africa, Western Cape Province, from Aspalathus sp., 2008, C.M. Bezuidenhout, CBS 144747 = CPC 25788, CBS 144748 = CPC 25782.

Notes — Fusarium libertatis formed a unique well-supported clade Clade (II). This species readily produced polyphialidic conidiogenous cells on its aerial mycelium and can be distinguished from the other species (F. carminascens, F. curvatum and F. elaeidis) found to produce polyphialides by only producing up to 3-septate macroconidia, whereas the other polyphialidic species produce up to 5-septate macroconidia.

Fusarium nirenbergiae L. Lombard & Crous, sp. nov. — MycoBank MB826845; Fig. 14

Fig. 14.

Fusarium nirenbergiae (ex-type culture CBS 840.88). a–b. Colony on PDA; a. surface of colony on PDA after 7 d at 24 °C under continuous white light; b. reverse of colony on PDA; c. conidiophores on surface of carnation leaf; d. sporodochia on carnation leaves; e. conidiophores and phialides on aerial mycelium; f–g. sporodochia and sporodochial conidiophores; h. chlamydospore; i. aerial conidia (microconidia); j. sporodochial conidia (macroconidia). — Scale bars: e, h–j = 10 μm; f–g = 50 μm.

Etymology. Named in honour of Prof. H.I. Nirenberg for her contribution to our understanding of Fusarium taxonomy.

Typus. Netherlands, Aalsmeer, from Dianthus caryophyllus, 1988, H. Rattink (holotype CBS H-23619 designated here, culture ex-type CBS 840.88).

Conidiophores carried on the aerial mycelium 18–50 μm tall, unbranched or sparingly branched, bearing terminal or intercalarily monophialides, often reduced to single phialides; aerial phialides subulate to subcylindrical, smooth- and thin-walled, 8–24 × 2–4 μm, periclinal thickening inconspicuous or absent; aerial conidia forming small false heads on the tips of the phialides, hyaline, ellipsoidal to falcate, smooth- and thin-walled, 0–1-septate; 0-septate conidia: (5–)6–10(–11) × 2–4 μm (av. 8 × 3 μm); 1-septate conidia: (9–)10–14(–15) × 2–4 μm (av. 12 × 3 μm). Sporodochia bright orange, formed abundantly on carnation leaves. Conidiophores in sporodochia verticillately branched and densely packed, consisting of a short, smooth- and thin-walled stipe, 6–14 × 3–5 μm, bearing apical whorls of 2–3 monophialides or rarely as single lateral monophialides; sporodochial phialides subulate to subcylindrical, 8–18 × 2–4 μm, smooth- and thin-walled, sometimes showing a reduced and flared collarette. Sporodochial conidia falcate, curved dorsiventrally with almost parallel sides tapering slightly towards both ends, with a blunt to papillate, curved apical cell and a blunt to foot-like basal cell, 1–5-septate, hyaline, smooth- and thin-walled; 1-septate conidia: 15–29(–34) × 3–4 μm (av. 22 × 4 μm); 2-septate conidia: (18–)19–31(–39) × 2–4(–5) μm (av. 25 × 3 μm); 3-septate conidia: (30–)32–40(–43) × 3–4 μm (av. 36 × 4 μm); 4-septate conidia: (34–)36–44(–48) × 3–5 μm (av. 40 × 4 μm); 5-septate conidia: (36–)43–59(–66) × 3–5 μm (av. 51 × 4 μm). Chlamydospores globose to subglobose, formed terminally, 4–6 μm diam.

Culture characteristics — Colonies on PDA with an average radial growth rate of 2.9–4.2 mm/d at 24 °C. Colony surface pale vinaceous to vinaceous, floccose with abundant aerial mycelium; colony margins irregular, lobate, serrate or filiform. Odour absent. Reverse pale vinaceous grey to greyish lilac, lacking diffusible pigment. On SNA, hyphae hyaline, smooth-walled, with abundant chlamydospores, aerial mycelium sparse with moderate sporulation on the medium surface. On CLA, aerial mycelium sparse with abundant bright orange sporodochia forming on the carnation leaves.

Additional materials examined. Brazil, from Passiflora edulis, 1968, W. Gerlach, CBS 744.79 = BBA 62355 = NRRL 22549. – Italy, Napoli, Castellammare di Stabia, from Bouvardia longiflora, July 1986, B. Aloj, CBS 196.87 = NRRL 26219. – Netherlands, Berkel, from Solanum lycopersicum, 16 May 1968, G. Weststeijn, CBS 758.68 = NRRL 36546. – South Africa, Western Cape Province, Riebeeck-Wes, from Agathosma betulina, 2001, K. Lubbe, CBS 115424 = CPC 5312; Stellenbosch, Elsenberg farm, from Agathosma betulina, 2001, K. Lubbe, CBS 115416 = CPC 5307, CBS 115417 = CPC 5306, CBS 115419 = CPC 5308. – USA, California, from amputated human toe, unknown date and collector, CBS 130300 = NRRL 26368; Florida, from Solanum tuberosum, 1923, H.W. Wollenweber, CBS 181.32 = NRRL 36303; from Chrysanthemum sp., date unknown, G.M. Armstrong & J.K. Armstrong, CBS 127.81 = BBA 63924 = NRRL 36229; Florida, from Chrysanthemum sp., date unknown, A.W. Engelhard, CBS 129.81 = BBA 63926 = NRRL 22539; Maryland, Beltsville, from tulip roots, 1991, R.L. Lumsden, CBS 123062 = GJS 91-17; Florida, Immokalee, from Solanum lycopersicum, date unknown, J. Swezey, CBS 130303; Texas, San Antonio, from human leg ulcer, date and collector unknown, CBS 130301 = NRRL 26374. – Unknown locality, from Secale cereale, date unknown, H.W. Wollenweber, CBS 129.24; from Musa sp., date unknown, E.W. Mason, CBS 149.25 = NRRL 36261.

Notes — Fusarium nirenbergiae formed a well-supported subclade in Clade VIII, closely related to F. curvatum. See notes under F. curvatum for distinguishing morphological features.

Fusarium oxysporum Schltdl., Fl. Berol. 2: 139. 1824 — Fig. 15

Fig. 15.

Fusarium oxysporum (ex-epitype culture CBS 144134). a–b. Colony on PDA; a. surface of colony on PDA after 7 d at 24 °C under continuous white light; b. reverse of colony on PDA; c–d. conidiophores on surface of carnation leaf; e–f. sporodochia on carnation leaves; g–j. conidiophores and phialides on aerial mycelium; k–n. sporodochia and sporodochial conidiophores; o–p. chlamydospores; q. aerial conidia (microconidia); r. sporodochial conidia (macroconidia). — Scale bars: g–h, m–r = 10 μm; i–l = 50 μm.

Synonyms. Fusarium bulbigenum Cooke & Massee, Grevillea 16: 49. 1887.

Fusarium vasinfectum G.F.Atk., Bull. Alabama Agric. Exper. Station 41: 19. 1892.

Fusarium dianthi Prill. & Delacr., Compt. Rend. Acad. Sci. 129: 744. 1899.

Fusarium lini Bolley, Proc. Ann. Meeting Soc. Prom. Agr. Sci. 21: 1–4. 1902.

Fusarium orthoceras Appel & Wollenw., Arb. Kaiserl. Biol. Anst. Ld.- u. Forstw. 8: 152. 1910.

Fusarium citrinum Wollenw., Maine Agric. Exp. Sta. Bull. 219: 256. 1913.

Fusarium angustum Sherb., Cornell Univ. Agric. Exp. Sta. Mem. 6: 203. 1915.

Fusarium lutulatum Sherb., Cornell Univ. Agric. Exp. Sta. Mem. 6: 209. 1915.

Fusarium bostrycoides Wollenw. & Reinking, Phytopathology 15: 166. 1925.

Diplosporium vaginae Nann., Atti Reale Accad. Fisiocrit. Siena sér. 4, 17: 491. 1926.

For additional synonyms see Index Fungorum and MycoBank.

Typification. Germany, Berlin, from rotten tuber of Solanum tuberosum, 1824, D.L.F. von Schlechtendal, HAL 1612 F, holotype in HAL; (epitype designated here: Germany, Berlin, from rotten tuber of Solanum tuberosum, 17 Oct. 2017, L. Lombard, epitype CBS H-23620, MBT382397, culture ex-epitype CBS 144134).

Conidiophores carried on the aerial mycelium 15–75 μm tall, unbranched or sparingly branched, bearing terminal or intercalarily monophialides, often reduced to single phialides; aerial phialides subulate to subcylindrical, smooth- and thin-walled, 11–40 × 2–4 μm, periclinal thickening inconspicuous or absent; aerial conidia forming small false heads on the tips of the phialides, hyaline, ellipsoidal to falcate, smooth- and thin-walled, 0–1-septate; 0-septate conidia: (4–)6–10(–11) × 2–4 μm (av. 8 × 3 μm); 1-septate conidia: 13–15(–16) × 2–4 μm (av. 14 × 3 μm). Sporodochia bright orange, formed abundantly on carnation leaves. Conidiophores in sporodochia verticillately branched and densely packed, consisting of a short, smooth- and thin-walled stipe, 4–10 × 4–5 μm, bearing apical whorls of 2–3 monophialides or rarely as single lateral monophialides; sporodochial phialides subulate to subcylindrical, 8–13 × 3–5 μm, smooth- and thin-walled, sometimes showing a reduced and flared collarette. Sporodochial conidia falcate, curved dorsiventrally with almost parallel sides tapering slightly towards both ends, with a blunt to papillate, curved apical cell and a blunt to foot-like basal cell, (1–)3(–5)-septate, hyaline, smooth- and thin-walled; 1-septate conidia: (21–)22–26 × 4–5 μm (av. 24 × 4 μm); 2-septate conidia: 20–26(–27) × 4–5 μm (av. 23 × 4 μm); 3-septate conidia: (22–)25–29(–31) × 4–5 μm (av. 27 × 4 μm); 4-septate conidia: (30–)31–35 × 4–5 μm (av. 33 × 5 μm); 5-septate conidia: 35–38 × 5–6 μm (av. 37 × 5 μm). Chlamydospores globose to subglobose, formed intercalarily or terminally, 5–10 μm diam.

Culture characteristics — Colonies on PDA with an average radial growth rate of 3.0–4.0 mm/d at 24 °C. Colony surface pale vinaceous, floccose with abundant aerial mycelium; colony margins irregular, lobate, serrate or filiform. Odour absent. Reverse vinaceous to rosy vinaceous, lacking diffusible pigment. On SNA, hyphae hyaline, smooth-walled, producing abundant chlamydospores, aerial mycelium sparse with abundant sporulation on the medium surface. On CLA, aerial mycelium sparse with abundant bright orange sporodochia forming on the carnation leaves.

Additional materials examined. Germany, from rotten tuber of Solanum tuberosum, 17 Oct. 2017, L. Lombard, CBS 144135. – South Africa, Western Cape Province, from Protea sp., date unknown, C.M. Bezuidenhout, CPC 25822. – South East Asia, from Camellia sinensis, 1949, F. Bugnicourt, CBS 221.49 = IHEM 4508 = NRRL 22546.

Notes — Fusarium oxysporum formed a well-supported subclade in Clade V with F. triseptatum as closest relative. Both species in Clade V displayed some morphological overlap. However, the 1-septate ((21–)22–26 × 4–5 μm (av. 24 × 4 μm) and 2-septate (20–26(–27) × 4–5 μm (av. 23 × 4 μm) macroconidia of F. oxysporum are larger than those of F. triseptatum ((18–)19–23(–24) × 3–4 μm (av. 20 × 3 μm) and 17–25(–26) × 3 μm (av. 21 × 3 μm), respectively), whereas the 3-septate ((25–)27–39(–47) × 4–5 μm (av. 33 × 3 μm)), 4-septate ((31–)34–40(–41) × 4–5 μm (av. 37 × 4 μm)) and 5-septate ((33–48(–49) × 4–5 μm (av. 40 × 4 μm)) macroconidia of F. triseptatum are larger than those of F. oxysporum ((22–)25–29(–31) × 4–5 μm (av. 27 × 4 μm), (30–)31–35 × 4–5 μm (av. 33 × 5 μm) and 35–38 × 5–6 μm (av. 37 × 5 μm), respectively). Additionally, all isolates of F. oxysporum produced abundant bright orange sporodochia on carnation leaf pieces, not observed for any of the F. triseptatum isolates studied.

Fusarium pharetrum L. Lombard & Crous, sp. nov. — MycoBank MB826846; Fig. 16

Fig. 16.

Fusarium pharetum (ex-type culture CBS 144751). a–b. Colony on PDA; a. surface of colony on PDA after 7 d at 24 °C under continuous white light; b. reverse of colony on PDA; c–d. conidiophores on surface of carnation leaf; e–f. sporodochia on carnation leaves; g–h. false heads carried on a phialide on aerial mycelium; i–l. conidiophores and phialides on aerial mycelium; m–p. sporodochia and sporodochial conidiophores; q. aerial conidia (microconidia); r. sporodochial conidia (macroconidia). — Scale bars: g–l, q–r = 10 μm; m–p = 50 μm.

Etymology. Name refers to the practice of the Southern African indigenous San people of hollowing out the tubular branches of the host plant, Aloidendron dichotomum, to form quivers (Latin pharetra) for their arrows.

Typus. South Africa, from Aliodendron dichotomum, 2000, F. van der Walt & G.J. Marais (holotype CBS H-23621 designated here, culture ex-type CBS 144751 = CPC 30824).

Conidiophores carried on the aerial mycelium 20–75 μm tall, unbranched or sparingly branched, bearing terminal or intercalarily monophialides, often reduced to single phialides; aerial phialides subulate to subcylindrical, smooth- and thin-walled, 4–28 × 2–5 μm, periclinal thickening inconspicuous or absent; aerial conidia forming small false heads on the tips of the phialides, hyaline, ellipsoidal to falcate, smooth- and thin-walled, 0–1-septate; 0-septate conidia: 5–9(–13) × 2–3 μm (av. 7 × 3 μm); 1-septate conidia: (10–)12–16(–18) × 2–4 μm (av. 14 × 3 μm). Sporodochia rosy vinaceous to orange, formed abundantly on carnation leaves. Conidiophores in sporodochia verticillately branched and densely packed, consisting of a short, smooth- and thin-walled stipe, 5–10 × 3–5 μm, bearing apical whorls of 2–3 monophialides or rarely as single lateral monophialides; sporodochial phialides subulate to subcylindrical, 7–13 × 3–4 μm, smooth- and thin-walled, sometimes showing a reduced and flared collarette. Sporodochial conidia falcate, curved dorsiventrally with almost parallel sides tapering slightly towards both ends, with a blunt to papillate, curved apical cell and a blunt to foot-like basal cell, 3(–4)-septate, hyaline, smooth- and thin-walled; 3-septate conidia: (22–)27–35(–39) × 3–5 μm (av. 31 × 4 μm); 4-septate conidia: (34–)36–40(–41) × 3–5 μm (av. 36 × 5 μm). Chlamydospores not observed.

Culture characteristics — Colonies on PDA with an average radial growth rate of 3.1–4.5 mm/d at 24 °C. Colony surface rosy vinaceous, floccose with abundant aerial mycelium; colony margins irregular, lobate, serrate or filiform. Odour absent. Reverse rosy vinaceous, lacking diffusible pigment. On SNA, hyphae hyaline, smooth-walled, lacking chlamydospores, aerial mycelium sparse with abundant sporulation on the medium surface. On CLA, aerial mycelium sparse with abundant rosy vinaceous to orange sporodochia forming on the carnation leaves.

Additional material examined. South Africa, from Aliodendron dichotomum, 2000, F. van der Walt & G.J. Marais, CBS 144750 = CPC 30822.

Notes — Fusarium pharetrum formed a well-supported subclade in Clade VII, closely related to F. contaminatum and F. veterinarium. See notes under F. contaminatum for distinguishing morphological features.

Fusarium triseptatum L. Lombard & Crous, sp. nov. — MycoBank MB826847; Fig. 17

Fig. 17.

Fusarium triseptatum (ex-type culture CBS 258.50). a–b. Colony on PDA; a. surface of colony on PDA after 7 d at 24 °C under continuous white light; b. reverse of colony on PDA; c–d. conidiophores on surface of carnation leaf; e–f. false heads carried on a phialide on aerial mycelium; g–j. conidiophores and phialides on aerial mycelium; k–l. chlamydospores; m. microconidia; n. macroconidia. — Scale bars: e, g–n = 10 μm; f = 20 μm.

Etymology. Name refers to the abundant 3-septate macroconidia produced by this fungus.

Typus. USA, locality unknown, from Ipomoea batatas, 1950, T.T. McClure (holotype CBS H-23622 designated here, culture ex-type CBS 258.50 = NRRL 36389).

Conidiophores carried on the aerial mycelium 5–40 μm tall, unbranched or sparingly branched, bearing terminal or intercalarily monophialides, often reduced to single phialides; aerial phialides subulate to subcylindrical, smooth- and thin-walled, 6–22 × 2–4 μm, periclinal thickening inconspicuous or absent. Microconidia forming small false heads on the tips of the phialides, hyaline, ellipsoidal to falcate, smooth- and thin-walled, 0–1-septate; 0-septate conidia: (5–)6–10(–13) × 1–3 μm (av. 8 × 3 μm); 1-septate conidia: (12–)14–16(–18) × 2–4 μm (av. 15 × 3 μm). Macroconidia also formed by phialides on aerial mycelium, falcate, curved dorsiventrally with almost parallel sides tapering slightly towards both ends, with a blunt to papillate, curved apical cell and a blunt to foot-like basal cell, (1–)3(–5)-septate, hyaline, smooth- and thin-walled; 1-septate conidia: (18–)19–23(–24) × 3–4 μm (av. 20 × 3 μm); 2-septate conidia: 17–25(–26) × 3 μm (av. 21 × 3 μm); 3-septate conidia: (25–)27–39(–47) × 4–5 μm (av. 33 × 3 μm); 4-septate conidia: (31–)34–40(–41) × 4–5 μm (av. 37 × 4 μm); 5-septate conidia: 33–48(–49) × 4–5 μm (av. 40 × 4 μm). Sporodochia absent. Chlamydospores globose to subglobose, formed terminally, 5–12 μm diam.

Culture characteristics — Colonies on PDA with an average radial growth rate of 2.2–3.4 mm/d at 24 °C. Colony surface pale vinaceous grey to vinaceous grey, floccose with abundant aerial mycelium; colony margins irregular, lobate, serrate or filiform. Odour absent. Reverse pale vinaceous grey, lacking diffusible pigment. On SNA, hyphae hyaline, smooth-walled, with abundant chlamydospores, aerial mycelium sparse with abundant sporulation on the medium surface. On CLA, aerial mycelium sparse lacking sporodochia on the carnation leaves.

Additional materials examined. Ivory Coast, Béoumi, wilted Gossypium hirsutum, Oct. 1996, K. Abo, CBS 116619. – Papua New Guinea, Suki village, from sago starch, 2005, A. Greenhill, CBS 119665. – USA, Tennessee, from human eye, collector and date unknown, CBS 130302 = NRRL 26360 = FRC 755.

Notes — Fusarium triseptatum formed a highly-supported subclade in Clade V, closely related to F. oxysporum. See notes under F. oxysporum for distinguishing morphological features.

Fusarium veterinarium L. Lombard & Crous, sp. nov. — MycoBank MB826849; Fig. 18

Fig. 18.

Fusarium veterinarium (ex-type culture CBS 109898). a–b. Colony on PDA; a. surface of colony on PDA after 7 d at 24 °C under continuous white light; b. reverse of colony on PDA; c–d. conidiophores on surface of carnation leaf; e–f. sporodochia on carnation leaves; g–i. conidiophores and phialides on aerial mycelium; j–l. sporodochia and sporodochial conidiophores; m. aerial conidia (microconidia); n. sporodochial conidia (macroconidia). — Scale bars: g–n = 10 μm.

Etymology. Name refers to the fact that this fungus was isolated mostly from veterinary samples.

Typus. Netherlands, from shark peritoneum, date unknown, C. Hoek (holotype CBS H-23623 designated here, culture ex-type CBS 109898 = NRRL 36153).

Conidiophores carried on the aerial mycelium 12–90 μm tall, unbranched or sparingly branched, bearing terminal or intercalarily monophialides, often reduced to single phialides; aerial phialides subulate to subcylindrical, smooth- and thin-walled, 8–24 × 2–4 μm, periclinal thickening inconspicuous or absent; aerial conidia forming small false heads on the tips of the phialides, hyaline, ellipsoidal to falcate, smooth- and thin-walled, 0–1-septate; 0-septate conidia: (4–)6–8(–11) × 2–4 μm (av. 7 × 3 μm); 1-septate conidia: (9–)10–14(–15) × 2–4 μm (av. 12 × 3 μm). Sporodochia bright orange, formed abundantly on carnation leaves. Conidiophores in sporodochia verticillately branched and densely packed, consisting of a short, smooth- and thin-walled stipe, 8–13 × 3–4 μm, bearing apical whorls of 2–3 monophialides or rarely as single lateral monophialides; sporodochial phialides subulate to subcylindrical, 10–15 × 2–4 μm, smooth- and thin-walled, sometimes showing a reduced and flared collarette. Sporodochial conidia falcate, curved dorsiventrally with almost parallel sides tapering slightly towards both ends, with a blunt to papillate, curved apical cell and a blunt to foot-like basal cell, 1–(2–)3-septate, hyaline, smooth- and thin-walled; 1-septate conidia: (12–)15–19(–20) × 3–4 μm (av. 17 × 3 μm); 2-septate conidia: (16–)17–21(–24) × 3–4 μm (av. 19 × 3 μm); 3-septate conidia: (19–)20–24(–27) × 3–4 μm (av. 22 × 3 μm). Chlamydospores not observed.

Culture characteristics — Colonies on PDA with an average radial growth rate of 3.1–4.5 mm/d at 24 °C. Colony surface pale vinaceous grey, floccose with moderate aerial mycelium appearing wet; colony margins irregular, lobate, serrate or filiform. Odour absent. Reverse pale vinaceous, lacking diffusible pigment. On SNA, hyphae hyaline, smooth-walled, lacking chlamydospores, aerial mycelium sparse with abundant sporulation on the medium surface. On CLA, aerial mycelium sparse with abundant orange sporodochia forming on the carnation leaves.

Additional materials examined. Netherlands, from swab sample near filling apparatus, Apr. 2005, J. Houbraken, CBS 117787, CBS 117790; from pasteurized milk-based product, Apr. 2005, J. Houbraken, CBS 117791, CBS 117792. – USA, California, from endoscope of veterinary clinic, date and collector unknown, NRRL 62545; from canine stomach, date and collector unknown, NRRL 62547; Massachusetts, from mouse mucosa, date and collector unknown, NRRL 54984; from little blue penguin foot, date and collector unknown, NRRL 54996; Texas, from unknown animal faeces, date and collector unknown, NRRL 62542.

Notes — Fusarium veterinarium formed a highly-supported subclade in Clade VII, closely related to F. contaminatum and F. pharetrum. See notes under F. contaminatum for distinguishing morphological features.

DISCUSSION

Fusarium taxonomy and the underlying phylogenetic backbone on which it is based, is undergoing continuous revision. In modern day fungal taxonomy, phylogenetic inference plays a vital role to resolve the identity of cryptic species due to the paucity of morphological features. However, a key component of a robust phylogeny is the availability of living ex-type material to serve as basic reference point or ‘phylogenetic anchor’ on which comparative taxonomy can be based (Booth 1975). Epi- and/or neotypification provides a vital means where upon stability can be enforced into a chaotic classification system as being applied to F. oxysporum today.

Snyder & Hansen’s (1940) treatment of the section Elegans to represent only F. oxysporum, has resulted in a much too broad definition of this species. Based on this, the current morphological characters used to define F. oxysporum include aseptate microconidia forming false heads on short monophialides, commonly 3-septate macroconidia formed on monophialides or branched conidiophores in sporodochia, and chlamydospores that are either formed abundantly and quickly or slowly with some strains not forming them at all (Leslie & Summerell 2006, Fourie et al. 2011). In this study, all isolates were found to produce not only aseptate microconidia, but abundant 1-septate microconidia, all of which were carried on false heads. Several species were also found to form polyphialides (e.g., F. carminascens, F. curvatum, F. elaeidis and F. libertatis), a characteristic not associated with F. oxysporum morphology (Gerlach & Nirenberg 1982, Nelson et al. 1983, Leslie & Summerell 2006). Additionally, the majority of the species introduced here produced 4- to 5-septate macroconidia in the same abundance as the 3-septate macroconidia. Gerlach & Nirenberg (1982) also indicated the presence of 7-septate macroconidia, but these were not observed in this study given the media and growth conditions we employed. The ex-epitype strain of F. oxysporum designated here, agrees well with the morphological characteristics described by Wollenweber & Reinking (1935), Booth (1971), Gerlach & Nirenberg (1982) and Nelson et al. (1983). This strain produced abundant aseptate and 1-septate microconidia on monophialides only, abundant 3-septate macroconidia with much fewer 1-, 2-, 4- and 5-septate macroconidia on its sporodochia, and smooth-walled globose chlamydospores carried intercalarily and/or terminally. Although this strain was isolated from a potato tuber displaying symptoms of dry rot, the ability of this strain to induce these symptoms requires further investigation. Comparisons of the 15 novel Fusarium taxa introduced here, revealed subtle morphological distinctions between the species.

Fusarium carminascens, F. curvatum, F. elaeidis and F. libertatis readily formed polyphialides on the aerial mycelium, a feature not known for F. oxysporum (Wollenweber & Reinking 1935, Booth 1971, Gerlach & Nirenberg 1982, Nelson et al. 1983, Leslie & Summerell 2006). These four species are further distinguished from each other by the degree of septation and curvature of their macroconidia. Both F. carminascens and F. libertatis readily formed chlamydospores in culture, whereas no chlamydospores were observed for F. curvatum and F. elaeidis. Furthermore, all strains of F. carminascens produced an almost carmine red exudate on the aerial mycelium on PDA, not observed for any other strains studied here. The strong curvature of the macroconidia of F. curvatum is also a unique feature.

The remaining 11 novel species introduced here can be distinguished based on the degree of septation and dimensions of the macroconidia and the formation of chlamydospores in culture. Of these, F. contaminatum, F. gossypinum, F. hoodiae, F. languescens, F. pharetrum, F. triseptatum and F. veterinarium displayed some morphological overlap with the ex-epitype strain of F. oxysporum. However, F. contaminatum, F. gossypinum, F. pharetrum and F. veterinarium did not form chlamydospores in culture. These four species are easily distinguished based on macroconidial dimensions with F. contaminatum and F. veterinarium producing the smallest macroconidia. Fusarium hoodiae, F. languescens and F. triseptatum readily formed chlamydospores in culture and can be distinguished from each other and F. oxysporum based on their sporodochia. All strains of F. triseptatum failed to produce any sporodochia on the carnation leaf pieces, whereas F. hoodiae formed distinct pale vinaceous to pale orange sporodochia compared to the only pale orange sporodochia of F. languescens. Fusarium callistephi, F. fabacearum, F. glycines and F. nirenbergiae are easily distinguished from each other and F. oxysporum by the degree of macroconidial septation and dimensions. However, these subtle morphological differences need to be supported by phylogenetic inference to accurately discriminate between these novel species introduced in the FOSC in this study.

Individual analyses of the partial sequences of the four gene regions (cmdA, rpb2, tef1 and tub2) included in this study (results not shown) revealed that the tef1 gene region provided the best resolution to discriminate the novel species introduced here. The rpb2 gene region also provided good resolution, but with lower statistical support, whereas the cmdA and tub2 provided little to no support. However, the addition of the latter two gene regions to either or both the rpb2 and tef1 greatly increased the statistical support of each Clade (I–VIII) and their underlining subclades. Genealogical concordance phylogenetic species recognition analyses also indicated that there was no evidence of recombination detected between any of the Clades and subclades resolved in this study. Analysis of the IGS gene region (results not shown) provided contradictory tree topologies and support values, with several strains in Clades III, VII and VIII forming single lineages. Although O’Donnell et al. (2015) advocates the use of rpb1, rpb2 and tef1 for sequence-based identification of Fusarium species, attempts to generate rpb1 sequence data in this study failed for the majority of strains included in this study.

Previous studies of FOSC revealed a high phylogenetic diversity within this complex, resolving three (O’Donnell et al. 1998, Brankovics et al. 2017), four (O’Donnell et al. 2004) and five (Laurence et al. 2012) phylogenetic clades, respectively. Comparisons of all these clades with those resolved in this study, revealed that Clade I in this study correlates well with Clade 1 resolved by O’Donnell et al. (1998, 2004), Laurence et al. (2012) and Brankovics et al. (2017). Similarly, Clade VIII in this study matched with Clade 3 of each of these studies. Clade III correlated with Clade 2 resolved by O’Donnell et al. (2004) and Brankovics et al. (2017), and Clade V correlated with clades 4 and 5 of Laurence et al. (2012), and Clade 4 of O’Donnell et al. (2004). Clades II, IV, VI and VII resolved in this study did not match any of the clades resolved in these previous studies.

Comparisons of the origin of the strains studied here revealed some correlation within most of the Clades (and subclades). All veterinarian strains included in this study clustered together with some strains originating from equipment used in food processing in a highly-supported subclade representing F. veterinarium. Similarly, three strains collected from contaminated dairy products and fruit juice clustered together in the highly-supported (sub)clade representing F. contaminatum. The majority of the isolates collected from tomato (Solanum lycopersicum) also cluster together in a clade representing F. languescens, with a few clustering in the F. nirenbergiae (sub)clade. In contrast to these few highlighted examples, all medically related strains clustered in various well- to highly supported clades, representing F. cugenangense, F. nirenbergiae, F. triseptatum and the untreated Fusarium clade. The highest host/substrate diversity was found in the F. nirenbergiae (sub)clade which included several special forms in addition to the medically related strains.

The application of the special form and pathotype classification system can only be successfully applied if the species boundaries are well established (Woudenberg et al. 2015), which is clearly not the case within the FOSC. For the FOSC, special forms are defined by the accessory chromosome obtained via horizontal gene transfer, and the pathotype on the type of virulence genes carried by this chromosome and should not be confused with the species boundaries within the FOSC. Therefore, epitypification of F. oxysporum in this study has resulted in the recognition of 21 phylogenetic species of which 15 are provided with names here. Although this study includes only a small subset of strains belonging to the FOSC, the inclusion of more isolates will provide a much better perspective on the cryptic diversity within this important species complex, allowing additional species to be recognised. Furthermore, it is hoped that with the epitypification of F. oxysporum, the confusing and sometimes complicated subspecific classification systems that have been applied to the FOSC in the past will become obsolete and be replaced by a more stable and convenient species-level classification system. We believe that such a system will allow for better communication between Fusarium researchers in the medical, environmental and phytopathological fields.