The core clade of Gliomastix including the type species is well delimited with a 92 % bootstrap value even in the very conservative LSU analysis. Although Gams (1971) placed this genus into Acremonium, several authors have recognised Gliomastix. Most notably, Matsushima (1975) placed Acremonium masseei and A. polychromum into Gliomastix and Lechat et al. (2010) linked G. fusigera with Hydropisphaera bambusicola. As circumscribed in this paper, the phylogenetically supported Gliomastix differs from previous morphological concepts by excluding several distantly related species such as Acremonium cerealis and A. inflatum. The closely related A. persicinum clade may also be included as suggested by Supplemental fig. 6E in Schoch et al. (2009) and discussed above. At the moment, we recognise only four species from the present study in Gliomastix. An additional species, published while the present manuscript was in preparation, Acremonium tumulicola (Kiyuna et al. 2010), should also be included in this concept of Gliomastix.

The generic characters do not differ significantly from those summarised in the generic diagnosis of Dickinson (1968).

1. Type species. Gliomastix murorum (Corda) S. Hughes, Canad. J. Bot. 36: 769. 1958. Basionym: Torula murorum Corda, Icon. Fung. 2: 9. 1838.

≡ Sagrahamala murorum (Corda) Subram., Curr. Sci. 41: 49. 1972.

For additional synonyms, see Gams (1971). The type species of Gliomastix, G. chartarum, is a synonym of G. murorum (Hughes 1958). The distinction between G. murorum var. murorum having conidia in chains and G. murorum var. felina having conidia in mucoid heads does not appear to be supported by phylogenetic analysis. Gliomastix murorum var. felina isolates originally described as Graphium malorum (ex-type CBS 154.25) and Torula cephalosporioides (ex-type CBS 378.36) are molecularly confirmed as synonyms of G. murorum (Fig. 2B). Recently, Kiyuna et al. (2010) neotypified Gliomastix felina (Marchal) Hammill, recombined as Acremonium felinum (Marchal) Kiyuna, An, Kigawa & Sugiy., with CBS 147.81. The sequences deposited in GenBank, e.g., AB540562, suggest that this isolate represents G. roseogrisea. The new combination is reduced to synonymy with that species below.

2. Gliomastix masseei (Sacc.) Matsush., Icon. microfung. Matsush. lect. (Kobe): 76. 1975. Basionym: Trichosporium masseei Sacc., Syll. Fung. 22: 1356. 1913

[= Trichosporium aterrimum Massee, Bull. Misc. Inform. 1899: 167 non (Corda) Sacc. 1886]

The name lacks an ex-type isolate. Although the isolate (CBS 794.69) sequenced is basal to the Gliomastix clade (Fig. 2B), it appears to be a suitable to serve as the basis for epitypification.

Holotype of Trichosporium masseei: India, Punjab, Changa Manga, on Morus indica, Jan. 1898, J. Gleadow, ex Herb. Massee, K; isotypes IMI 49,214 = IMI 87,346.

Epitype designated here: Italy, Turin, isolated from rabbit dung, A. Fontana, CBS H-8244, ex-epitype culture CBS 794.69.

3. Gliomastix polychroma (J.F.H. Beyma) Matsush., Icon. microfung. Matsush. lect. (Kobe): 77. 1975. Basionym: Oospora polychroma J.F.H. Beyma, Verh. K. Ned. Akad. Wetensch., Sect. 2, 26 (2): 5. 1928.

≡ Sagrahamala polychroma (J.F.H. Beyma) Subram., Curr. Sci. 41: 49. 1972.

Additional synonyms are given by Gams (1971). This clade includes the ex-type isolate of Oospora polychroma, basionym of G. polychroma, CBS 181.27 (Fig. 2B). Periconia tenuissima var. nigra is confirmed as a synonym via inclusion of its ex-type isolate CBS 151.26 (Fig. 2B). The status of the different isolate, CBS 617.94, from banana, requires further clarification. This isolate may be related to Acremonium musicola, a species not represented in CBS.

4. Gliomastix roseogrisea (S.B. Saksena) Summerbell, comb. nov. MycoBank MB519588. Basionym: Cephalosporium roseogriseum S.B. Saksena, Mycologia 47: 895. 1956 [1955].

≡ Acremonium roseogriseum (S.B. Saksena) W. Gams [as `roseogriseum'], Cephalosporium-artige Schimmelpilze (Stuttgart): 87. 1971.

Gliomastix roseogrisea, like G. murorum, has a variety of conidial forms including conidia in chains and conidia of various shapes in mucoid heads. This plasticity of form recalls the situation mentioned above for A. sclerotigenum and may represent a relatively common situation in acremonioid species. As another example Gams (1971) lists “Gliomastix murorum var. felina pro parte in Dickinson in Mycol Pap. 115: 16, 1968” as an additional synonym of this taxon.

As mentioned above in the discussion of the genus, Kiyuna et al. (2010) recently neotypified Gliomastix felina (basionym Periconia felina Marchal, Bull. Soc. R. Bot. Belg. 34:141. 1895) with CBS 147.81, an isolate collected by Hammill (1981). This isolate is a typical G. roseogrisea, a taxon not studied by Kiyuna et al. (2010).

5. Gliomastix tumulicola (Kiyuna, An, Kigawa & Sugiy.) Summerbell, comb. nov. MycoBank MB519599. Basionym: Acremonium tumulicola Kiyuna, An, Kigawa & Sugiy., Mycoscience 52: 13. 2010.

This newly described species is phylogenetically placed by its original authors (Kiyuna et al. 2010) in the Gliomastix clade and comparison of sequences confirms that placement. Although this information was received too late to include this species in our phylogenetic analyses, the species is placed in Gliomastix.

The genus Sarocladium was described for two pinkish coloured fungal pathogens causing sheath blast of rice (Gams & Hawksworth 1976). The drawings in that paper and the photographs in Bills et al. (2004) show structures that overlap with those produced by the phylogenetically related A. kiliense, A. strictum, and A. zeae. As in Fusarium, plant pathogenic fungi that sporulate on above-ground plant parts are likely to produce upright, branching sporulating structures with mucoid conidia suggesting dispersal by insects that fly from plant to plant. Species with habitats where water flux or microarthropod movement may be important in dispersal, e.g., various Acremonia occurring in soil or Fusarium domesticum growing on cheese, may have simplified conidiogenous structures. Bills et al. (2004) suggested that the generic placement of Acremonium kiliense and A. strictum should be re-examined in light of their close relationship with Sarocladium oryzae.

The genus Sarocladium is delineated here to include several species previously recognised in Acremonium, as seen in Figs 1 and 2. In Fig. 2, where phylogenetic signal is relatively low, Sarocladium tepidly (84 % bootstrap) links to the A. bacillisporum clade. In Fig. 1, it links with a 99 % bootstrap value. Phylogenetic clustering algorithms often insert the A. bacillisporum clade between A. strictum and A. kiliense due to certain apo- or plesiomorphies shared with one or the other of these two members of the A. strictum clade (data not shown). On the other hand, the next most closely related clade in Fig. 1, the A. breve/A. curvulum clade, has ITS sequences with substantial sections that are difficult to align with those of the A. bacillisporum and A. strictum clades, indicating considerable evolutionary distance.

The genus Sarocladium is emended here to include those species that belong to the A. strictum and A. bacillisporum clades. The generic name Sagrahamala is not a contender for this group because the type species is the unrelated Acremonium luzulae. In addition Acremonium luzulae is a species in need of epitypification, because, as shown in the present study, more than one phylogenetic species is encompassed under the name.

Sarocladium W. Gams & D. Hawksw., Kavaka 3: 57. 1976 [1975].

Colonies on 2 % malt extract agar slimy-glabrous to moderately floccose to deeply dusty, sometimes ropy; with, in Gams' terminology (Gams 1971), phalacrogenous, nematogenous, to plectonematogenous conidiation; growing 13–25 mm in 10 d at 20 °C, whitish to pinkish to salmonaceous or, when conidia are formed in chains, sometimes acquiring vivid conidial mass colouration such as ochraceous or greenish glaucous; reverse pale to pinkish orange to pale grey-brown, rarely greenish-blue. Conidiogenous apparatus ranging from adelophialides, solitary orthotropic phialides to conidiophore structures with one or a few branches, or with cymose branching or occasionally with one or two ranks of loosely structured verticils, sometimes with repeated branching extending to 90 μm long. Phialides subulate, aculeate to acerose, straight, slightly curved, or undulate, thin- and smooth-walled, 15–60(–75) μm long, tapering from a basal width of 1.2–2.5 μm, with minimal collarette; conidia borne in mucoid heads or dry chains, notably longer than broad, l/w mostly 2.2–7.0, cylindrical to fusiform to bacilliform, aseptate, smooth-walled, with rounded or tapered-truncate ends, 3.5–8(–14) × 0.5–2 μm. Chlamydospores present or absent, when present relatively thick-walled, smooth or slightly roughened, globose to ellipsoidal, intercalary or terminal, mostly solitary, occasionally in short chains, 4–8 μm. Internal transcribed spacer sequence mostly with distinctive CGGTCGCGCC motif in mid-ITS2 region.

Several species of Sarocladium are noted for melanogenesis yielding ochre-brown to dark grey-brown colony reverse colours on Sabouraud agar: S. glaucum, S. kiliense, and S. zeae (Gams 1971). In the case of S. kiliense, this melanogenesis has the result that most mycetoma cases feature black “grains” or sclerotium-like balls of compacted fungal hyphae (Summerbell 2003); melanogenesis is a well known pathogenicity factor in fungal diseases of humans and animals (Gómez & Nosanchuk 2003). As recognised here Sarocladium yields a remarkable unity of species with elongated conidia and phialides. Several species including S. kiliense, S. oryzae, and S. strictum form adelophialides prominently, at least in some isolates; acremonioid species outside Sarocladium usually lack this character.

The recognised species are given below. Acremonium implicatum may belong here, but the species lacks living ex-type or representative material. The “A. implicatum” isolate that grouped in Sarocladium, CBS 243.59, is noted by Gams (1971) as an authentic isolate of Fusidium terricola J.H. Mill., Giddens & A.A. Foster and this name could be used if A. implicatum sensu Gams is revealed as polyphyletic. The other “A. implicatum” isolate, CBS 397.70B, included in this study is not a Sarocladium; rather it is a member of the A. exiguum clade.

1. Type species. Sarocladium oryzae (Sawada) W. Gams & D. Hawksw., Kavaka 3: 58. 1976 [1975].

A description and synonymy are given by Gams & Hawksworth (1975). Bills et al. (2004) synonymised Sarocladium attenuatum with S. oryzae based on the reported identity of the ITS sequence of its ex-type isolate, CBS 399.73, with that of representative isolates of S. oryzae. We resequenced the ITS region of CBS 399.73 and obtained a sequence differing from Bills et al. (AY566995) by 6 base-pairs and 2 gaps. Some of the base pairs in our sequence appeared to be symplesiomorphies shared with A. kiliense or A. strictum but not S. oryzae, rather than random mutations or possible miscalls. Our resequencing of unequivocal S. oryzae isolates CBS 180.74 and CBS 361.75 yielded results consistent with those of Bills et al. (2004). The status of S. attenuatum thus requires further study.

2. Sarocladium bacillisporum (Onions & Barron) Summerbell, comb. nov. MycoBank MB519589. Basionym: Paecilomyces bacillisporus Onions & G.L. Barron, Mycol. Pap. 107: 11. 1967.

≡ Acremonium bacillisporum (Onions & G.L. Barron) W. Gams, Cephalosporium-artige Schimmelpilze (Stuttgart): 72. 1971.

This species was described by Gams (1971). It is easily confused with Verticillium leptobactrum, which can be relatively floccose and loosely structured although some isolates are very dense and slow-growing (Gams, 1971). In addition colonies of S. bacillisporum at maturity have a pinkish colouration.

3. Sarocladium bactrocephalum (W. Gams) Summerbell, comb. nov. MycoBank MB519590. Basionym: Acremonium bactrocephalum W. Gams, Cephalosporium-artige Schimmelpilze (Stuttgart): 44. 1971.

As indicated by Gams (1971) this uncommon species is closely related to S. strictum, but is distinguished morphologically by its long, narrow conidia. It is molecularly distinguishable by LSU sequences.

4. Sarocladium glaucum (W. Gams) Summerbell, comb. nov. MycoBank MB519591. Basionym: Acremonium glaucum W. Gams, Cephalosporium-artige Schimmelpilze (Stuttgart): 68. 1971.

This species was described by Gams (1971). The ex-type culture CBS 796.69 indicates that this species belongs in Sarocladium.

5. Sarocladium kiliense (Grütz) Summerbell comb. nov. MycoBank MB519592. Basionym: Acremonium kiliense Grütz, Dermatol. Wochenschr. 80: 774. 1925.

= Cephalosporium incoloratum Sukapure & Thirum., Sydowia 19: 171. 1966 [1965].

Additional synonyms and a description of S. kiliense are given by Gams (1971) and Domsch et al. (2007); the species is also extensively illustrated by de Hoog et al. (2000). The ITS sequence of the ex-type strain of Acremonium incoloratum, CBS 146.62, is identical to that of the ex-type of S. kiliense, CBS 122.29 (data not shown). Though isolate CBS 146.62 is unusual in colour and lacks well differentiated chlamydospores that generally occur in S. kiliense, there is no phenetic difference profound enough to suggest that additional genes must be examined to be certain of their synonymy.

The sequences deposited in GenBank by Novicki et al. (2003) for their “Acremonium strictum genogroup III” (ITS: AY138846; LSU: AY138484) are actually of S. kiliense.

6. Sarocladium ochraceum (Onions & Barron) Summerbell, comb. nov. MycoBank MB519593. Basionym: Paecilomyces ochraceus Onions & G.L. Barron, Mycol. Pap. 107: 15. 1967.

≡ Acremonium ochraceum (Onions & G.L. Barron) W. Gams, Cephalosporium-artige Schimmelpilze (Stuttgart): 67. 1971.

This species was described by Gams (1971). We analysed the ex-type culture, CBS 428.67.

7. Sarocladium strictum (W. Gams) Summerbell, comb. nov. MycoBank MB519594. Basionym: Acremonium strictum W. Gams, Cephalosporium-artige Schimmelpilze (Stuttgart): 42. 1971.

Descriptions of S. strictum are given by Gams (1971) and Domsch et al. (2007). The type isolate of S. strictum was confirmed in this genus (Fig. 2C). Of the three isolates illustrated by Gams (1971) under A. strictum, CBS 287.70 D, is confirmed by sequencing as S. strictum. The only isolate of Acremonium zonatum in this study, CBS 565.67, turned out to have an ITS sequence identical to that of S. strictum. This is one of three isolates examined by Gams (1971) as A. zonatum. He stated that another isolate, CBS 145.62, appeared to be A. kiliense, but that examination of herbarium material suggested that this species had been growing on the natural substrate mixed with the real A. zonatum and had been isolated accidentally. One herbarium specimen examined by Gams (1971) showed septate conidia, something not otherwise seen in Sarocladium, so there may indeed be a real A. zonatum. It is not clear if A. zonatum sensu Gams is a unified concept or a designation of various acremonioid fungi forming leaf spots on tropical plants. In any case, the known connection of the genus Sarocladium with phytopathogenesis and endophytism as in S. zeae makes it plausible that species such as S. strictum and S. kiliense may play a role in plant disease.

8. Sarocladium zeae (W. Gams & D.R. Sumner) Summerbell, comb. nov. MycoBank MB519595. Basionym: Acremonium zeae W. Gams & D.R. Sumner, in Gams, Cephalosporium-artige Schimmelpilze (Stuttgart): 121. 1971.

This economically important maize endophyte species fits the description given by Gams (1971) as a fungus with felty to shaggy colonies. Two S. zeae isolates with more flattened colonies were accessed in CBS as A. strictum. Both CBS 646.75 and 226.84 were from maize and found to be producers of pyrrocidine metabolites as well as dihydroresorcylide, characteristic of S. zeae (Wicklow et al. 2008). Pyrrocidines are antagonistic to Aspergillus flavus and Fusarium verticillioides in maize inflorescences and are thus important in the ecology and economic significance of S. zeae. An additional A. strictum isolate, CBS 310.85, is also S. zeae as evidenced by pyrrocidine production, but has not yet been sequenced (Wicklow et al. 2008).

A significant theme of the current volume is the pioneering of a new approach to dikaryomycete nomenclature: the unitary naming of genus-level clades based on the oldest valid generic name, whether originally anamorphic or teleomorphic in nature (see discussion in Gräfenhan et al. 2011). Because the first named fungi were often species prominently in contact with humans and their environs and because the first names usually were attached to the most frequently seen reproductive state, there is considerable wisdom to using the oldest name applied to either aspect of the holomorph in constructing a unitary nomenclature.

The genus Trichothecium makes an excellent example, since the system used here preserves the best known species name in the group. A unitary system giving teleomorphs primacy would replace the familiar “T. roseum” with a Leucosphaerina name. A system that retains primacy for morphology, which is the only reasonable basis for dual nomenclature in the molecular era, would divide the Trichothecium clade into four genera, as is the case today. One of those genera, Acremonium, would be quintessentially artificial and almost completely divorced from evolutionary biological relationships. With increased emphasis on genomes, proteomes, and metabolomes, a focus on polyphyletic elements of microscopic shape seems counterproductive. Every new system of nomenclatural change will entail both fortunate and infelicitous changes and will receive some resistance in scientific communities. A nomenclatural system based on phylogeny will be considerably more stable than any previous system. The interests of all would be best served if it bridged gracefully out of pre-phylogenetic taxonomy, preserving as many familiar elements as possible. Trichothecium roseum, a constant from 1809 to today, is one of those elements that is worthy of being preserved.

Fig. 3.

A. Trichothecium roseum CBS 113334 showing retrogressive conidiation. B-D. conidiogenesis in “Trichothecium indicum”/Leucosphaerina indica CBS 123.78 showing retrogressive development (B), phialidic development (B) and sympodial development (D).