Mycol. Res. 108 (5): 576–582 (May 2004). f The British Mycological Society 576 DOI: 10.1017/S0953756204009839 Printed in the United Kingdom. The type species of Verticillium is not congeneric with the plant-pathogenic species placed in Verticillium and it is not the anamorph of ‘ Nectria ’ inventa Rasoul ZARE1, Walter GAMS2* and Hans-Josef SCHROERS2 1 Department of Botany, Plant Pests and Diseases Research Institute, P.O. Box 1454, Tehran 19395, Iran. Centraalbureau voor Schimmelcultures, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. E-mail : gams@cbs.knaw.nl 2 Received 5 October 2003; accepted 20 January 2004. The monotype species of the genus Verticillium, Verticillium tenerum, is a synonym of the older name Sporotrichum luteo-album. Its purported teleomorph connection with ‘ Nectria’ inventa is refuted and the preserved specimens of that species are considered as probably identical with Stephanonectria keithii (Bionectriaceae). V. luteo-album takes a unique position in the Glomerella clade of ascomycetes, as sister of the Verticillium–Plectosphaerella clade, which comprises plant-pathogenic species. V. luteo-album is not closely related to V. dahliae and its relatives, which are also situated in this clade. Conservation of the name Verticillium with V. dahliae as conserved type will be necessary to retain this generic name for the plant-pathogenic Verticillium species. In anticipation of this conservation, the new combination Acrostalagmus luteo-albus (syn. Sporotrichum luteo-album) is made. INTRODUCTION Nees von Esenbeck (1816) introduced the genus Verticillium for a single saprotrophic species that he named V. tenerum. The generic name was given to express the verticillate arrangement of phialides (i.e. conidiogenous cells) on conidiophores (Latin verticillus, a whorl). Following many other authors, Gams (1971) characterized the genus by having usually 1-celled, hyaline conidia, verticillate conidiophores with aculeate phialides inserted in a mesotonous to acrotonous position, as distinct from the mostly basitonous ramification (if any) of Acremonium. For a long time, the genus has become a repository of some 190 described species. Verticillium is a vaguely delimited genus of anamorphic fungi, and verticillate, aculeate phialides are not sufficient for a natural generic classification. Verticillium species are found to be associated with different families and even orders of ascomycetes (e.g. Rehner & Samuels 1995) and the four sections distinguished by Gams & van Zaayen (1982) are still heterogeneous (Gams & Zare 2002). To understand their ecology and physiology, a finer subdivision and a more natural classification is required that reflects the affinities of the species. After most species of section Prostrata W. Gams 1971 have been excluded (Gams & Zare * Corresponding author. 2002, Zare & Gams 2004), the scope of this paper is to clarify the taxonomy of the type species. MATERIAL AND METHODS Numerous cultures of the anamorph were examined by us during the years. Teleomorph material was analysed in detail as follows : the only records of the species consist of the type material (IMI 051936), and three specimens of decaying stalks of Brassica sp., North Wootton, Norfolk, England, collected and identified by T. Petch in 1935, 1936 and 1942, respectively, kept in the Royal Botanic Gardens, Kew herbarium, K(M) 61837, K(M) 61835 and K(M) 61836. All these collections were also examined by Booth (1959). Perithecia were newly sectioned for our study using a freezing microtome. For a reconstruction of phylogenetic affinities, sequences of the ITS region of possibly related fungi available in GenBank (Table 1) were analysed, using Neighbour-joining and parsimony algorithms. Ambiguously aligned sections were omitted, leading to stretches of 510 characters that could be used in the analysis. Significance was assessed by bootstrap analyses based on 1000 resampled data sets. Newly generated sequences of Rhynchosporium alismatis were obtained from Wayne M. Pitt, and those of Acremonium furcatum (which falls outside the Hypocreales according to Rasoul Zare, Walter Gams and Hans-Josef Schroers 577 Table 1. Origin of strains/sequences used in this study. V.=Verticillium, P.=Plectosphaerella, R.=Rhynchosporium, A.=Acremonium, G.=Gliocladium, Gl.=Glomerella, C.=Colletotrichum, S.=Sordaria. Species GenBank no. Strain Source Country Host V. albo-atrum V. albo-atrum V. albo-atrum V. albo-atrum V. albo-atrum V. dahliae V. dahliae V. dahliae V. dahliae V. tricorpus V. tricorpus V. tricorpus V. nubilum V. nigrescens V. nigrescens V. luteo-album V. luteo-album V. luteo-album P. cucumerina P. cucumerina P. cucumerina P. cucumerina P. cucumerina P. cucumerina R. alismatis R. alismatis A. furcatum AF364015 AF364014 AF364008 Z29509 AF108476 Z29511 AF108478 AF364003 AF364004 AF364017 L28679 Z29524 AJ292463 AJ292440 AF108473 AF324878 AJ292421 AJ292420 AF132805 AF176952 U66732 AJ246154 L36640 AJ492873 AY258150 AY258151 AY378154 1201 Va1 KRS1 1776 (non-lucerne) UAMH 5393 2341 UAMH 5360 L1 MD80 1988 Collins & Barbara, unpubl. Collins & Barbara, unpubl. Collins & Barbara, unpubl. Morton et al. 1995 Bidochka et al. 1999 Morton et al. 1995 Bidochka et al. 1999 Collins & Barbara, unpubl. Collins & Barbara, unpubl. Collins & Barbara, unpubl. Moukhamedov et al. 1994 Morton et al. 1995 Zare et al. 2000 Zare et al. 2000 Bidochka et al. 1999 Collopy et al. 2001 Zare et al. 2000 Zare et al. 2000 Harrington et al. 2000 K. O’Donnell, unpubl. Chen et al. 1996 Carter et al. 1999 O’Donnell & Gray 1995 Atkins et al., unpubl. Pitt et al., unpubl. Pitt et al., unpubl. R. C. Summerbell, unpubl. Belgium Netherlands Canada Humulus lupulus Lycopersicon esculentum Medicago sativa Canada Medicago sativa Canada Russia Germany United Kingdom Solanum melongena Brassica napus ssp. oleifera Brassica napus ssp. oleifera Lycopersicon esculentum Scotland UK Mushroom compost Solanum tuberosum UK UK USA Polygonom seiboldii Dead butterfly Glycine max G. cibotii G. cibotii G. cibotii C. gloeosporioides C. musae Gl. acutata Gl. cingulata S. macrospora AF021264 AF048739 AF048738 AY266387 AY266401 AY266405 AY266404 AF246293 JCM 9206? JCM 9206? JCM 9203 ZE 0036 CMUBP1 G2 CMUBE1815 267 IMI 130213 IMI 044575 UAMH 6687 CBS 112.16 IMI 017438 IMI 182719 P8 NRRL 20430 ARC2 OOO17 380408 CBS 112535 CBS 112531 CBS 12242 (type strain) Glycine max Avena sp. UK Potato cyst nematode France Dune sand under Convolvulus soldanella Lee et al., unpubl. Shin & Lee, unpubl. Park et al., unpubl. Photita et al., unpubl. Photita et al., unpubl. Photita et al., unpubl. Photita et al., unpubl. Debuchy, R., unpubl. Glenn et al. 1996), from Richard C. Summerbell (Table 1). RESULTS Morphology Anamorph : Conidiophores : Main stipe erect, more or less straight, repeatedly branched, pale reddish brown or yellowish at the base, almost hyaline at the apex. Basal cell of the conidiophore occasionally slightly bulbous on the natural substratum, but not in culture. Full-grown conidiophore stipes 200–400 mm long, 4–5 mm wide at the base, tapering to 3 mm in the upper part. Main axis often branched several times. Phialides arising in whorls of 3–5 at several levels along the main stipe and its branches. Main conidiophore axis and its branches usually terminating into a longer phialide, around which three to five shorter phialides are grouped in a verticil. Conidiogenous cells : Phialides narrowly flask-shaped, only very slightly swollen at the base, tapering in the middle or upper part into a narrow neck which opens with an inconspicuous collarette; phialides subhyaline, measuring 10–25r2–4 mm in the widest part. Conidia forming rounded pale reddish brown slimy heads, oval, measuring 3.5–5r2–2.5 mm (Fig. 1b). Teleomorph : Perithecia seated on a small pseudoparenchymatous stroma developing in the outer tissues of the host ; globose to ovate, ostiolate, scarcely papillate, yellow to blackish brown, KOH–, 220–500 mm diam, 250–300 mm high ; in the upper half covered with some hyaline, rigid, septate, 5–6 mm wide hyphae, which distally narrow to a point (Fig. 1f), besides some more differentiated reddish conidiophores (Fig. 1d), some with intact phialides. Lateral perithecial wall 35–45 mm thick, composed of 7–9 layers of hexagonal to globose thin-walled cells measuring 6–10r4–6 mm, smaller and more compressed towards the inner layers. Asci cylindrical to clavate, 60–100r4–6 mm, containing eight ascospores in uniseriate or partly biseriate arrangement. Ascospores oblong to fusiform, hyaline to slightly Verticillium tenerum and ‘Nectria ’ inventa 578 Fig. 1. Verticillium luteo-album and Nectria inventa. (a) Conidiophore ; (b) conidia; (c) section through perithecium ; (d) conidiophores on the perithecial wall ; ( f ) section of perithecium with abortive conidiophores on the upper part ; (e) and (g) ascospores. (a) and (b) IMI 017438a ; (c–g) K(M) 61835. Bars a–b, d–e, and g=10 mm ; c and f=50 mm. brownish, showing faint longitudinal striations, (0–)1septate, 8–12r3–5 mm (Fig. 1e, g). Phylogeny ITS sequences show that within a monophyletic Glomerella clade (formerly classified in the Phyllachorales, but unrelated to the Phyllachoraceae ; Winka & Eriksson 2000), the darkening Verticillium species (sect. Nigrescentia W. Gams 1982), Plectosphaerella and its Plectosporium anamorphs, Acremonium furcatum, and V. luteo-album form a well-supported clade (100 % bootstrap support). Two subclades comprise : (1) most of the darkening Verticillium species (100 %) ; and (2) Plectosphaerella and the obviously congeneric Rhynchosporium alismatis (Pitt et al., unpubl.), V. nigrescens and Acremonium furcatum (66 %). Opposite to these subclusters, V. luteo-album (100 % bootstrap) and ‘Gliocladium ’ cibotii (also 100 %) take basal positions (Fig. 2). Species of Glomerella and their Colletotrichum anamorphs form another, well-defined clade (100 %), which is less related to the taxa discussed here. Together they form a monophyletic Glomerella clade, which is still of uncertain position in the Sordariomycetidae. A parsimony analysis yielded more than 2100 most parsimonious trees, which essentially had the same topology as the consensus tree (not shown). The definition and classification of species in Verticillium sect. Nigrescentia is not yet quite settled (Barbara & Clewes 2003) : strains of V. albo-atrum are heterogeneous. In contrast, V. dahliae is more homogeneous, and V. tricorpus and V. nubilum are closely related to the latter. These four species form a compact clade (100 %), while Verticillium nigrescens is more distant, near Acremonium furcatum, and may require reclassification. Verticillium luteo-album is thus clearly separated from all species of sect. Nigrescentia. Rasoul Zare, Walter Gams and Hans-Josef Schroers 579 AF364014 V. albo-atrum 70 AF364015 V. albo-atrum Z29509 V. albo-atrum 79 AF364008 V. albo-atrum 71 AF108476 V. albo-atrum AJ292463 V. nubilum 67 AF364003 V. dahliae AF364004 V. dahliae 99 100 Z29511 V. dahliae AF108478 V. dahliae 99 AF364017 V. tricorpus 89 L28679 V. tricorpus Z29425 V. tricorpus AF132805 P. cucumerina 66 AF176952 P. cucumerina U66732 P. cucumerina AJ246154 P. cucumerina 87 L36640 P. cucumerina AJ492873 P. cucumerina 98 91 100 AY258150 R. alismatis AY258151 R. alismatis 66 86 AJ292440 V. nigrescens AF108473 V. nigrescens 66 CBS122.42 A. furcatum 62 AF324878 V. luteo-album 100 AJ292421 V. luteo-album AJ292420 V. luteo-album AF021264 G. cibotii AF048739 G. cibotii 100 AF048738 G. cibotii 98 AY266387 C. gloeosporioides AY266401 C. gloeosporioides 55 100 AY266404 C. gloeosporioides AY266405 Gl. acutata AF246293 S. macrospora 0.01 substitutions/site Fig. 2. Neighbour-joining analysis of species of the Glomerella clade as evidenced by ITS sequences. Bootstrap values indicated at the nodes. V.=Verticillium, P.=Plectosphaerella, R.=Rhynchosporium, A.=Acremonium, G.=Gliocladium, Gl.=Glomerella, C.=Colletotrichum, S.=Sordaria. NOMENCLATOR Verticillium Nees, Syst. Pilze Schwämme : 57 (1816). Type : Verticillium tenerum Nees 1816 : Fr.=Verticillium luteo-album (Link : Fr.) Subram. 1971. Verticillium luteo-album (Link : Fr.) Subram., Hyphomycetes: 649 (1971). Sporotrichum luteo-album Link, Ges. Naturf. Freunde Berlin Mag. Neuesten Entdeck. Gesammten Naturk. 3 : 13 (1809) : Fries, Syst. mycol. 3 : 424 (1832), basionym (T in B). Botrytis aurantiaca Link, Ges. Naturf. Freunde Berlin Mag. Neuesten Entdeck. Gesammten Naturk. 3 : 14 (1809). Verticillium tenerum Nees, Syst. Pilze Schwämme : 57 (1816) : Fr. (?T in M). Botrytis tenera (Nees : Fr.) Pers., Mycol. Europ. 1 : 38 (1822) : Fries, Syst. mycol. 3 : 403 (1832). Sporotrichum mycophilum Link, Jahrb. Gewächsk. 1 : 179 (1818). Sporotrichum lateritium Ehrenb., Sylvae mycol. Berol. : 11, 22 (1818) : Fr. (T in B). Botrytis lateritia (Ehrenb. : Fr.) Fr., Syst. mycol. 3 : 402 (1832). Verticillium lateritium (Ehrenb. : Fr.) Rabenh., Deutschl. Kryptog.-Fl. 1 : 100 (1844). Botrytis lateritia Schwein., Trans. Am. philos. Soc. 2 : 281 (1832). Verticillium ochrorubrum Desm., Annls Sci. Nat., Bot., se´r. 2, 2 : 71 (1834). Verticillium affine Corda, Icones Fung. 1: 20 (1837). Acrostalagmus cinnabarinus Corda, Icones Fung. 2 : 15 (1838). Verticillium tenerum and ‘Nectria ’ inventa Stachylidium cinnabarinum (Corda) Bonord., Handb. allg. Mykol.: 110 (1851). Verticillium cinnabarinum (Corda) Reinke & Berth., Zersetz. Kartoff. : 63 (1879). Acrostalagmus parasitans Corda, Icones Fung. 3 : 11, 1839. Stachylidium parasitans (Corda) Bonord., Handb. allg. Mykol.: 110 (1851). Verticillium rufum Rabenh., Deutschl. Kryptog.-Fl. 1: 100 (1844). Verticillium ruberrimum Bonord., Handb. allg. Mykol. : 97 (1851). Acrostalagmus fulvus Berk. & Broome, J. Linn. Soc. 14 : 138 (1875). Verticillium cinnamomum Sousa da Câmara, Revta agron., Lisb. 20 : 62 (1932) (T in BPI) [non V. cinnamomeum Petch 1931]. Synonyms according to Hughes (1951, 1958), Booth (1959), Subramanian (1971), and Domsch et al. (1980). The cases where we examined type material ourselves are indicated by ‘T ’ with the respective herbarium acronym. Purported teleomorph: Nectria inventa Pethybr., Trans. Br. mycol. Soc. 6 : 107 (1919). DISCUSSION A very detailed description of Verticillium tenerum (as Nectria inventa) was given by Hughes (1951). Among the known synonyms of the type species, Sporotrichum luteo-album Link 1809 is the oldest name sanctioned by Fries (1832). Subramanian (1971) was the first to combine this epithet in Verticillium. Corda (1838) introduced the genus Acrostalagmus described as having verticillate conidiophores, with hyaline, egg-shaped conidia formed singly, but held together by slime. Acrostalagmus was distinguished from Verticillium for some decades by its stronger slime production (Lindau 1905), but later the two genera were generally accepted as synonymous (Pethybridge 1919, Isaac 1967). The type species of Acrostalagmus, A. cinnabarinus Corda, turned out to be identical with V. luteo-album (Hughes 1958, Subramanian 1971). Hughes (1951) reported that this fungus can sporulate on a great variety of plant substrata. In the compilation by Domsch et al. (1980), many kinds of soil, plant roots (without particular rhizosphere accumulation), litter and seeds, cotton fibres, and bird’s feathers and nests are documented as substrata. The species was also described as a mycoparasite on Daldinia concentrica (Hughes 1951), Alternaria brassicae (Tsuneda et al. 1976), and Cronartium comandrae (Powell 1971). Pethybridge (1919) discovered a number of red perithecia on a pile of old, diseased seed potatoes in very close association with conidiophores of ‘ V. cinnabarinum ’ and thought to have found its teleomorph, which he described as Nectria inventa. He emphasized that in some cases conidiophores of the anamorph were 580 present on the perithecial stroma and on the surfaces of the perithecia. In order to prove the anamorph– teleomorph connection, he transferred individual ascospores to agar films on the under side of cover glasses, observed their germination and obtained cultures with an anamorph matching V. cinnabarinum. He therefore regarded ‘ V. cinnabarinum ’ as the anamorph of Nectria inventa, but he did not succeed in reproducing the teleomorph from the anamorph. After him, no author has grown such ascospores and this connection could not be critically confirmed. The species was found again on decaying stalks of Brassica sp. by Petch in 1935, 1936 and 1942, and this material is preserved in K. Hughes (1951) and Gams & van Zaayen (1982) regarded the brick-red colour of all parts of the anamorph as very characteristic of the species. Consequently, Gams & van Zaayen (1982) retained this species as the only member of Verticillium sect. Verticillium, when they introduced several other sections of the genus. Such pigmentation is not known in any other verticillium-like species. V. luteo-album is, however, rather variable in its growth habit (intensity of sporulation, colony colour, and conidiophore ramification). This variation may account for a large number of synonyms. Cultures of Verticillium luteo-album are easily distinguished from the somewhat similar, plant-associated species of sect. Nigrescentia when examined on commonly used agar media. While the former is orangebrown in all its parts, the plant-associated species of sect. Nigrescentia show dark olivaceous-grey melanized pigmentation in some parts, vegetative hyphae, chlamydospores, microsclerotia or conidiophores, and usually less complex ramification of the conidiophores. By means of molecular methods, RFLP (Zare 2003) and sequencing (see Fig. 1), the species can also be sharply distinguished from each other. Sequences of 18S rDNA (Messner et al. 1996, Kerry O’Donnell, pers. comm.) have already indicated that species of the plant-associated Verticillium sect. Nigrescentia and V. luteo-album are close to Glomerella, which then was classified in the Phyllachorales; but no matching teleomorph genus could be found. Previous comparisons of sequences of the ITS region also suggested that V. luteo-album was related to sect. Nigrescentia (Zare 2000, 2003, Zare et al. 2000, Pitt et al. 2004). But, according to the present findings, its closest relatives are Acremonium furcatum and Plectosphaerella cucumerina. The latter shares 90–92 % sequence similarity with V. luteo-album, while V. alboatrum and V. dahliae are more distantly related to the type species and probably not congeneric with it. Glomerella is conventionally classified in the Phyllachorales (Silva-Hanlin & Hanlin 1998). But, according to Winka & Eriksson (2000), the Phyllachoraceae, and in particular Phyllachora, are only distantly related to the Glomerella clade as characterized here; also Spatafora & Blackwell (1994) found Glomerella clustering Rasoul Zare, Walter Gams and Hans-Josef Schroers close to the Microascales and suggested a classification in the Polystigmatales. But Polystigma is a member of the Phyllachoraceae s. str. (Cannon 1996) and therefore this order name cannot be accepted as distinct from the Phyllachorales. The family Glomerellaceae M. V. Locquin (1984 : 175) and even the order Glomerellales (cited as ‘ Chadefaud ex Locquin 1981 ’ in Locquin 1984) would probably be appropriate for them rather than the Phyllachoraceae. Unfortunately, the family and order names based on Glomerella are invalid (Art. 36 ; Hawksworth & David 1988), but in Kirk et al. (2001) the name Glomerellaceae is listed as if it were valid. Eriksson et al. (2003) list Glomerella as Sordariomycetidae (inc. sed.). In any case, V. luteo-album cannot be a member of the Nectriaceae or Bionectriaceae. Pethybridge (1919) found the anamorph in close association with perithecia of ‘Nectria ’ inventa, which obviously belongs to the Hypocreales because of its orange perithecia, cylindrical asci with 2-celled ascospores and absence of true paraphyses. The facts recorded here show that ‘N. ’ inventa cannot be the teleomorph of V. luteo-album as originally claimed. The close association of V. luteo-album with ‘N.’ inventa is to be explained by assuming that the former is a mycoparasite growing on the latter. The bulbous base of the conidiophores developed on this substratum (Fig. 1d) seems to facilitate penetration of its host. Pethybridge’s drawing of ‘ 2-celled ascospores ’ which are constricted at the septum may possibly have been conidia that developed a septum at germination. The type material of ‘ N. ’ inventa is in poor shape; that of the secondary collections is better, but no fresh collections of a comparable fungus are available and the anamorph is unknown. Our observations were found in close agreement with Pethybridge’s and Booth’s descriptions. In addition, they show that N. inventa is a member of the Bionectriaceae. In this family Schroers et al. (1999 : 116) established the genus Stephanonectria for Nectria keithii Berk. & Broome (Ann. Mag. nat. Hist., ser. 4, 27 : 144. 1876), characterized by superficial perithecia arising from a superficial to erumpent stroma on various dead plants, including stems of Brassica sp.; brown, KOH– perithecia, the ostioles surrounded by a crown-like structure ; ascospores 1-septate, covered with short striae ; anamorph sporodochial, myrothecium-like, with brownish orange conidial masses. We conclude with some confidence that N. inventa belongs to Stephanonectria. At least in the secondary collections perithecia are overall brown, and sitting superficially on the stroma; the outer perithecial wall cells are not easily recognizable as angular to globose, contrasting with the structure normally seen in Bionectria (Schroers 2001). The original description by Pethybridge mentions ‘cameo-brown ’ perithecia with short, stiff, multicellular hairs. An ornamentation of the ascospores is neither mentioned by him nor by Booth (1959). The interrupted striation of the ascospores, which is characteristic of S. keithii, could only occasionally be observed in ascospores of 581 the North Wootton material ; in the type material the structure could not be seen clearly at all. Nevertheless, we conclude that ‘ N.’ inventa is probably a synonym of S. keithii. That Stephanonectria is a member of the Bionectriaceae in the Hypocreales was also established by a sequence of the large subunit of rDNA (GenBank AF210671 ; Schroers 2000). The relationships of the families of the Hypocreales have been studied in detail by Rossman et al. (2001) and Zhang & Blackwell (2002). That they are unrelated to the Glomerella clade has also been demonstrated by Pitt et al. (unpubl.). Because of distinct morphology (particularly pigmentation), substrate relationships, and phylogenetic distance, a generic distinction between the former sections Verticillium and Nigrescentia is appropriate. In order to retain the name Verticillium for the plantrelated species, conservation of the genus name with a different type will be proposed. Anticipating such a conservation and because Acrostalagmus Corda will then be available based on the same type species, we introduce the new combination Acrostalagmus luteoalbus (Link : Fr.) Zare, W. Gams & Schroers, comb. nov. (basionym Sporotrichum luteo-album Link, Ges. TQ1 Naturf. Freunde Berlin Mag. Neuesten Entdeck. Gesammten Naturk. 3 : 13, 1809 : Fries, Syst. mycol. 3: 424, 1832). ACKNOWLEDGEMENTS We thank Wayne M. Pitt for pioneering cladograms of the Glomerella clade and contributing his sequences of Rhynchosporium alismatis. Richard C. Summerbell contributed ITS sequences of Acremonium furcatum and corrected our manuscript. The curators of the herbaria K and IMI are thanked for making the specimens in their keeping available. Two anonymous referees improved the clarity of the presentation. REFERENCES Barbara, D. J. & Clewes, E. 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