Abstract

INTRODUCTION

The modern concept of Penicillium (referred to in this paper as Penicillium sensu lato), was derived from the pioneering monographic revisions of Thom (1930), Raper & Thom (1949), and formalised by the recognition of four subgenera, Aspergilloides, Furcatum, Penicillium and Biverticillium by Pitt (1980). Over the past decade, the realisation has grown that Penicillium subgenus Biverticillium is phylogenetically distinct from other subgenera of Penicillium and that this distinctiveness should be reflected in its formal taxonomy. Because of their usually symmetrical, biverticillate conidiophores, the group has been recognised since Wehmer (1914) segregated them in an informal subdivision of Penicillium that he called “Verticillatae”. The delineation, species composition and taxonomic rank of this group were modified in subsequent monographs by Thom (1930), Raper & Thom (1949), Pitt (1980), and Ramírez (1982), culminating in the widespread recognition of subgenus Biverticillium and the use of this name in many taxonomic and phylogenetic studies. Malloch (1985), based on a consideration of morphological and ecological factors, and anamorph-teleomorph connections, may have been the first to speculate that subgenus Biverticillium should be removed from Penicillium as a separate genus.

The teleomorph genera historically associated with Penicillium sensu lato are Talaromyces and Eupenicillium (in single name nomenclature, the latter is now considered a synonym of Penicillium sensu stricto, see Houbraken & Samson 2011). The teleomorphs of these two groups produce distinctive ascomata. In Talaromyces, the soft ascomatal walls are comprised of multiple layers of interwoven hyphae and the ascomata mature quickly, usually within a few weeks in agar culture. In Penicillium sensu stricto, the sclerotium-like ascomata have rigid walls of thick-walled, isodiametric cells and the ascomatal maturity can take months and often ascospores do not form at all. Furthermore, in Talaromyces the ascus initials sometimes have morphologically distinguishable gametangia and the mature asci are produced in chains (Stolk & Samson 1972), while the ascomatal initials in Penicillium sensu stricto are irregularly interwoven, loosely branched hyphae masses (Emmons 1935), and the mature asci are single. Raper & Thom (1949) already recognised that there was considerable evidence that Penicillium subgenus Biverticillium constituted a natural and homogenous group. A comparison of the anamorphs of these two teleomorph types reveals a correlation with phialide shape, with anamorphs of Talaromyces (until now classified in Penicillium subgenus Biverticillium) having narrower phialides that are aculeate or lanceolate, and anamorphs in Penicillium sensu stricto having broader, ampulliform or flask-shaped phialides. One consequence of the differences in phialide shape is that the symmetrical nature of the conidiophores of species allied with Talaromyces tends to be emphasised, because in general the phialides are more densely packed. The colonies of subgenus Biverticillium can often be distinguished from those of Penicillium sensu stricto by the naked eye. They often have darker green conidia, more or less yellow pigmented and encrusted aerial hyphae, and colony reverses in yellow, orange or red to purplish red shades.

Once DNA-based studies of fungal phylogeny began, it quickly became apparent that the differences between Penicillium sensu stricto and Talaromyces were more than a matter of degree, and that there might be a significant problem with the generic concept of Penicillium sensu lato. Penicillium sensu stricto and Talaromyces occur as distinct clades within Trichocomaceae, which could be considered subfamilies (LoBuglio et al., 1993, LoBuglio & Taylor 1993). Using small subunit nuclear ribosomal DNA sequences (18S), Berbee et al. (1995) showed that Penicillium is polyphyletic if subgenus Biverticillium is included, a conclusion reconfirmed in one of the first reviews of the impact of molecular phylogenetics on Ascomycete taxonomy (Sugiyama 1998) using an analysis of 18S rDNA sequences. Removal of subgenus Biverticillium transforms Penicillium sensu stricto into a monophyletic group. This dichotomy between Penicillium sensu stricto and Talaromyces was shown repeatedly in studies employing nuclear ribosomal RNA genes, for example by Peterson (2000), who analysed a combination of the nuclear ribosomal internal transcribed spacer regions (ITS) and large subunit ribosomal DNA (28S) sequences (Ogawa et al. 1997, Ogawa & Sugiyama 2000), and by Wang & Zhuang (2007) in a phylogeny based on calmodulin sequences. The results of these analyses are all confirmed in the multigene phylogenetic analyses presented elsewhere in this volume by Houbraken & Samson (2011), using genes selected for their ability to accurately reflect molecular phylogeny. As indicated by Houbraken & Samson (2011), when other genera assigned to Trichocomaceae are included in phylogenetic analyses, the division between subgenus Biverticillium and Penicillium sensu stricto becomes even clearer. In that study, intervening genera include Aspergillus, Paecilomyces sensu stricto (with Byssochlamys as a synonym), and several small and less well-known genera such as Thermoascus, Penicilliopsis, Thermomyces and the recently described Rasamsonia (Houbraken et al. 2011).

In a molecularly defined, phylogenetically accurate taxonomic system, maintaining subgenus Biverticillium in Penicillium sensu stricto is untenable. However, almost every aspect of the biology, biochemistry, and physiology of these two groups emphasises their fundamental distinctiveness, although sometimes with limited taxon sampling. For example, Pitt (1980) emphasised the distinctiveness of subgenus Biverticillium by using a low water-activity medium, G25N (which includes 25 % glycerol) in his standard plating regime. Strains assigned to this subgenus grow slowly on this medium, less than 10 mm diam at 25 °C in 7 d, whereas species of the other subgenera are more xerophilic and grow faster. Cell-wall components seem to differ significantly. Leal & Bernabé (1998) reported on the complex glucomannogalactan components of the water soluble polysaccharide fraction of several species of Trichocomaceae, suggesting that a characteristic heteropolysaccharide composed of 4 galactose: 1 mannose: 1 glucose was unique to species of subgenus Biverticillium. Species of Penicillium sensu stricto species were characterised by the presence of a β-(1-5)(1-6)-galactofuran polysaccharide in the same fraction. Cell wall components as reflected by their exoantigens were screened in about 50 species of Penicillium sensu lato using an ELISA reaction to antibodies raised to P. digitatum (subgenus Penicillium). These antibodies reacted well with all the species of subgenera Furcatum, Penicillium and Aspergilloides, but did not react with the four species of subgenus Biverticillium tested (P. funiculosum, P. islandicum, P. rubrum, and P. tardum) (Notermans et al. 1998). Kuraishi et al. (1991) first noted that the pattern of ubiquinones in Penicillium sensu lato and showed a distinct pattern in subgenus Biverticillium. Paterson (1998) examined 335 strains and 118 species of Penicillium sensu lato and determined that the Q9 ubiqinone type was predominant in the species of Penicillium sensu stricto. In contrast, species of Talaromyces, Trichocoma and subgenus Biverticillium had different versions of the Q10 ubiquinone type. Exceptions to these patterns can be explained by the small number of species whose classification in, or elimination from, subgenus Biverticillium has been uncertain or controversial. Frisvad et al. (1990a) provided an overview of the extrolites of Talaromyces species, and demonstrated the occurrence of characteristic extrolites such as mitorubins, bisanthaquinones such as rugulosin and skyrin, vermicellin, vermistatin, vermiculine, duclauxin and glauconic acid. None of these compounds were found in cultures of Penicillium sensu stricto (Frisvad et al. 1990b).

The soon to be published International Code of Nomenclature for Algae, Fungi and Plants removes the primacy of teleomorph-over anamorph-typified names, leaving both kinds of names competing equally for priority (Norvell 2011). Because of these changes, we apply the principle of ‘one fungus - one name’ and in the nomenclatural revision, priority is given to the oldest genus and species name irrespective of whether they were originally described for teleomorphs or anamorphs (Hawksworth et al. 2011). In this respect, Penicillium returns to the single named, but pleomorphic, nomenclatural and taxonomic system used by many of the founders of its taxonomy, and actively promoted by the Peoria school (Thom 1930, Raper & Thom 1949). Talaromyces, now also defined as a pleomorphic genus, is adopted for the anamorphic species formerly included in Penicillium subgenus Biverticillium. In this study, the phylogenetic relationships of species of subgenus Biverticillium and other members of the Trichocomaceae were studied by sequencing a part of the RPB1 (RNA polymerase II largest subunit) gene. Furthermore, we discuss the taxonomy and nomenclature of species of this expanded concept of Talaromyces, based on phylogenetic, phenotypic and extrolite data. For detailed phylogenetic analysis below genus level, the ITS regions (including the 5.8S nrDNA) of ex-type strains and/or representatives were sequenced. As discussed below, this paper is not meant as a monographic treatment, because many complexes have not yet been studied comprehensively.

MATERIALS AND METHODS

RESULTS

Phylogenetic generic delimitation of Talaromyces and biverticillate anamorphic species

The phylogenetic relationships of Talaromyces and species of Penicillium subgenus Biverticillium among other related genera were studied using partial RPB1 sequences. One-hundred fifty-six strains were included in this analysis. The length of the alignment was 496 characters (exon data only, no introns observed) and 323 of those characters were variable. The proportion of gaps and completely undetermined characters in the alignment was 0.60 %. Figure 1 shows that members of the subgenus Biverticillium and Talaromyces are accommodated in a well-supported (97 % bs), monophyletic clade (= Talaromyces s. str.) and that species of the Penicillium subgenera Aspergilloides, Furcatum and Penicillium form an independent, well-supported clade (Penicillium s. str.). The majority of described Talaromyces species belong to Talaromyces s. str., but some species are dispersed in other clades, including Talaromyces ocotl, T. luteus, T. thermophilus, T. eburneus, T. emersonii, T. byssochlamydoides, T. spectabilis, T. brevicompactus, T. striatus and T. leycettanus. Talaromyces ocotl is in a well-supported clade with the type species of Sagenomella, S. diversispora, and other Sagenomella species. The former T. emersonii, T. eburneus and T. byssochlamydoides form a clade recently recognised and described as the genus Rasamsonia (Houbraken et al. 2011). Talaromyces thermophilus is also excluded from Talaromyces s. str. and is closely related to the type species of Thermomyces, Therm. lanuginosus. Basal to Therm. lanuginosus and T. thermophilus is Talaromyces luteus. This species is on a separate branch and no other closely related species were found in our analysis. The uniqueness of the species is supported by the production of large amounts of the prenylated diketopiperaziners talathermophilins A and B, not found in any other species (Chu et al. 2010). The phylogenetic position of T. leycettanus is not convincingly defined. This species is positioned near Warcupiella spinulosa and Hamigera striata (= Talaromyces striatus), but bootstrap support is lacking. Talaromyces brevistipitatus occurs on a well-supported branch with H. avellanea. Comparison of ITS and calmodulin sequences shows that this species is closely related to NRRL 2108, an undescribed, phylogenetically distinct Hamigera species (ITS 100 % bs, calmodulin 99 % bs) (Peterson et al. 2010). The majority of members of subgenus Biverticillium sensu Pitt (1980) are phylogenetically placed within Talaromyces s. str., with P. isariiforme as the only exception. This species belongs to Penicillium s. str. and is closely related to P. ochrosalmoneum. This relationship was also confirmed by extrolite data (see below).

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Fig. 1

. Best-scoring Maximum Likelihood tree calculated using RAxML, based on partial RPB1 sequences showing the relationships among members of Talaromyces and Penicillium subgenus Biverticillium and related genera. The bootstrap support percentages of the maximum likelihood (ML) analysis are presented at the nodes. Bootstrap support values less than 70 % are not shown and branches with bootstrap support values > 70 % are thickened. The bar indicates the number of substitutions per site. The tree is rooted with Coccidioides immitis (strain RS).

Figure 1 indicates that the following species phylogenetically belong in Talaromyces: Aphanoascus cinnabarinus (CBS 267.72), Sagenomella bohemica (CBS 545.86^T), Paecilomyces aerugineus (CBS 350.66^T), Geosmithia viridis (CBS 252.87^T) and Sagenoma viride (CBS 114.72^T). The former three strains are on a well-supported sister clade basal to Talaromyces muroii CBS 756.96.

Species delimitation and synonymies within Talaromyces

The ITS analysis (Fig. 2) was used in this study to provide a preliminary circumscription of the species belonging to the Talaromyces clade. Ninety-seven strains were included in the ITS analysis. The used primer pair V9G and LS266 also amplifies a part of the 18S and 28S rDNA; however, for analysis, only the span including the ITS regions and 5.8S rDNA was used. The length of the alignment was 483 characters and 221 characters were variable.

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Fig. 2

. Best-scoring Maximum Likelihood tree calculated using MEGA 5.0 based on ITS sequences showing the relationship among members of the Talaromyces and members of Penicillium subgenus Biverticillium. The bootstrap support percentages of the maximum likelihood (ML) analysis are presented at the nodes. Bootstrap support values less than 70 % are not shown and branches with bootstrap support values > 75 % are thickened. The bar indicates the number of substitutions per site. The tree is rooted with Trichocoma paradoxa (CBS 788.83). T. = Talaromyces; P. = Penicillium. Strains indicated with * are ITS sequencing obtained from GenBank.

Most bootstrap support values in the ITS analysis are low, less than 70 %. Only a few branches are supported with values higher than 70 %. The majority of Talaromyces species are on a branch with 96 % bootstrap support (clade 1, Fig. 2). This clade is also present in the RPB1 analysis (100 % bs). Another large clade was present in the ITS phylogram and this clade is supported with 96 % boostrap (clade 2). This clade can be divided in two subclades (2A and 2B), both present in the RPB1 analysis; however, the relationship among these subclades is not supported statistically. Talaromyces dendriticus, T. oblatus, and Paecilomyces pascuus are in the same lineage and the former two species share the same ITS sequence. Talaromyces assiutensis and T. gossypii also have similar ITS sequences and are phenotypically similar (Frisvad et al. 1990a).

Extrolite analysis

In general, Talaromyces species produce many biosynthetic families of polyketides and meroterpenoids, but rather few families of nonribosomal peptides and terpenes. By examining HPLC-DAD results from all described species of Penicillium, Aspergillus and their teleomorphs, and by searching the literature for families of exometabolites produced by these fungi, it is obvious that Talaromyces species have unique and specific extrolites (Table 2). Figure 3 shows the common exometabolite families in Talaromyces/Biverticillium, Penicillium, Aspergillus and other genera. Aspergillus and Penicillium share 91 biosynthetic families, but shares more of these with other fungal genera than with Talaromyces. A few exometabolites are shared among Talaromyces, Penicillium and Aspergillus including alternariols, asperphenamate, botryodiploidin, dehydrocarolic acid, emodins, geodins, gregatins, herqueinone, 3-hydroxyphtalic acid, italinic acid, lichexanthones, mellein, monordens, pinselin, rugulosuvines, rugulovasines, secalonic acids and zeorins. Most of these metabolites have relatively simple structures, and many occur in other genera less related phylogenetically to any of the penicilloid and aspergilloid genera. Considering the large number of shared exometabolite biosynthetic families in common between Penicillium and Aspergillus, Talaromyces is clearly different, which corresponds with all other data for these genera.

Table 2

Secondary metabolite (exometabolite) biosynthetic families known from Talaromyces and Penicillium subgenus Biverticillium. (P) means also found in Penicillium and its teleomorphic state Eupenicillium, (A) means also found in species of Aspergillus. (Others) means also found in other fungi outside Penicillium, Aspergillus, Talaromyces and related genera.

Secondary metabolite (exometabolite) biosynthetic families
AF-110	5-Hydroxymethylfurfural	Purpurogenones
Alternariols * (P and others)	Hydromethylmaltol	Rasfonin
Anthglutin	4-Hydroxy-4,5-dicarboxy pentadecanoic acid (T. spiculisporus)	Rubratoxins
Apiculides (incl. NG-011's * (others))	7-Hydroxy-2,5-dimethylchromane	Rugulosins (& flavoskyrin) * (others)
AS-186-G	3-Hydroxymethyl-6,8-dimethoxycoumarin	Rugulotrosins
Asperphenamates & asperglaucid * (A, P)	3-Hydroxyphthalic acid * (P)	Rugulosuvine * (P)
Atrovenetinon methyl acetal (P. verruculosum)	Islandic acids	Rugulovasines * (P)
Epi-Austdiols (7-epiaustdiol & 8-O-methylepiaustdiol) (the stereoisomer austdiol found in Aspergillus)	(+)-Isocitric acid + Decylcitric acid (T. spiculisporus)	Secalonic acids * (A, P, others)
Austins * (A, P)	Italinic acids * (P)	Speciferone* (others)
BE-24811	Juglones	Spiculisporic acids (= minioluteic acids)
BE-31405's	Lichexanthone * (others)	SQ 30957
Berkeleyamides	Luteusins	Stemphyperylenole
Botryodipoidin * (P & others)	Maculosin * (others)	Stipitatic acids
Chrodinanine A	Mellein * (A)	Talaperoxides
Cordyanhydrides	Methyl-4-carboxy-5-hydroxyphthalaldehydrate	Talaroconvolutins
Cyclochlorotines & islanditoxin	3-Methyl-6-hydroxy-8-methoxy-3,4-dihydroisocoumarins	Talaroderxine
Dehydrocarolic acids * (A, P)	Miniolutelides, berkeleydione, berkeleytriones, berkeleyacetals, dhilirolides	Talaroflavones
Diethylphthalate (Artefact?)	Mitorubrins & kasanosins & funicones	Talaromycins
5,6-Dihydro-3,5-dihydroxy-6-hydroxymethyl-2H-pyran-2-one	Monascins & monascorubramin	Talarotoxins
4,6-Dihydroxy-5-methylphthalide	Monordens * (A, others)	TAN-931
(2E,2E’,7S,7’E)-4,9-Dioxo-7-(4’,9’-dioxo-2’,7’decadienoyloxy)-2-decanoic acid	NG-061	Thailandolides
Diversonols	NK-374200	Trachyspermic acids
Duclauxins	OF-4949's	Trachyspic acid
Emodins * (A, P, others)	Penicilliopsin * (others)	Triacetic lactone
Erythroskyrins	Penisimplicins	(-)-2,3,4-Trihydroxy-butanamide
Flavomannin	Penisimplicissins	Vermicellins
Funiculosic acids	Penitrinic acid & penitricins	Vermiculins
Funiculosin	Pevalic acid	Vermilutins
Geodins * (A, P)	PF-1092A	Vermistatins & penicidones
Glauconic acids	Pinselic acid	Vertoskyrin
Gregatins and penicilliols * (A, P)	Pinselin * (A, others)	Wortmannilactones
Helicusins	Purpactins (= penicillides = vermixocins)	Wortmannins * (others)
Herqueinones* (P)	Purpuride	Xanthoradones
		Zeorins * (A, others)

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Fig. 3

. Common exometabolite families in Talaromyces/Biverticillium, Penicillium, Aspergillus and other genera.

Among the few extrolites shared by Penicillum, Aspergillus and Talaromyces are the ergochromes, secalonic acid D & F. These anthraquinone derived metabolites are found in P. isariiforme, P. chrysogenum, Aspergillus aculeatinus, P. dendriticum and P. pseudostromaticum (Samson et al. 1989, Frisvad & Samson 2004, Houbraken et al. 2011). It is also possible that there are optical antipodes of these compounds produced in these genera, as was found in Aspergillus versicolor ((+) versicolamide)) and A. sclerotiorum ((-)-versicolamide) (Williams 2011). If this is so, it may indicate that the extrolites of Talaromyces and Penicillium / Aspergillus may also differ in stereochemical aspects. Another example of shared yet different extrolites is the azaphilones, which are common in species of Talaromyces and related biverticillate anamorphic species (Frisvad et al. 1990a, Nicoletti et al. 2009, Osmanova et al. 2010), but could not be found in Aspergillus and Penicillium sensu stricto. When similar compounds were found in Talaromyces, stereoisomers of the compounds were found in Aspergillus and Penicillium. For example, while sclerotiorins occur in P. sclerotiorum, the epimers are found in Talaromyces helicus and T. luteus (Yoshida et al. 1995, 1996a, b). Austdiol was isolated from Aspergillus pseudoustus (Vleggaar et al. 1974, Samson et al. 2011), but 7-epi-austdiol from a Talaromyces species (Liu et al. 2010).

Misidentifications of strains can make these comparisons difficult, but the overwhelming majority of extrolites found in Talaromyces are not found in Aspergillus or Penicillium. Although vermistatins, penisimplisins, penisimplicissins were reported from Penicillium simplicissimum (Komai et al. 2005), the producing strain was misidentified and actually represents a species of Talaromyces. The opposite has also happened, and metabolites attributed to a species of subgenus Biverticillium are later found to be produced by species of Penicillium sensu stricto. Penicillium verruculosum was reported to produce verruculogen, hence the name (Cole et al. 1972, Cole & Kirksey 1973), but the strain was later reidentified as P. brasilianum (Frisvad 1989).

Penicillium isariiforme (Samson et al. 1989) and P. ochrosalmoneum (Wicklow & Cole 1984) both produce large amounts of citreoviridin, supporting their close relationship indicated by the phylogenetic analyses, as noted above (Fig. 1).

DISCUSSION

The symmetrical, biverticillate penicillus was used as a defining character by Wehmer (1914), and Thom (1915a, b). Wehmer (1914) proposed to call this group the Verticillata, while Thom (1915a) referred to it as the Penicillium luteum-purpurogenum group. Biourge (1923) was the first who named this group as the subgenus Biverticillium, but included species such as P. citrinum (as P. aurifluum), P. atramentosum etc., which are no longer regarded as members of this subgenus (Houbraken et al. 2010). The characteristic lanceolate or acerose phialides was used as a more definitive morphological character of subgenus Biverticillium and related Talaromyces anamorphs (Raper & Thom 1949), because biverticillate branched conidiophores with flask-shaped phialides are mainly found in unrelated species such as P. citrinum. Although the lanceolate phialides occur in most species of subgenus Biverticillium, some species, e.g. P. rugulosum, have phialides that are not slender and have an apical portion tapering into a long acuminate point.

Thom (1930) treated some of the Penicillia in his Biverticillate-Symmetrica group and distinguished four sections: Ascogena, Coremigena, Luteo-virida (Funiculosa and Luteo-purpurogena) and Miscellanea. Later, Raper & Thom (1949) subdivided the group into the P. luteum series, P. duclauxii series, P. funiculosum series, P. purpurogenum series, P. rugulosum series and P. herquei series. This grouping is inconsistent with our phylogenetic analysis of the biverticillate group. The classification proposed by Pitt (1980) is more in concordance with the phylogenetic and taxonomic treatment proposed here, although he included a few species in Penicillium subgenus Biverticillium, namely P. isariiforme, P. clavigerum and P. vulpinum (as P. claviforme) that are now classified in Penicillium sensu stricto. The same conclusion was shown by the early molecular results of LoBuglio & Taylor (1993), and subsequently supported by the physiological, morphological and extrolite characters reviewed in the Introduction, and generated during this study.

In general, Penicillium sensu stricto and Aspergillus share many more features with each other than they do with Talaromyces. This includes micro- and macro-morphology, good growth on low water activity media, and the many shared exometabolite families. Talaromyces produces a series of metabolites that are apparently unique to this genus (J.C. Frisvad unpubl. data). The characteristic yellow and red colony and mycelial colours in Talaromyces are often caused by accumulation of mitorubrins and other azaphilones and unique anthraquinones and mitorubrins that are not found in Aspergillus and Penicillium. Some azaphilones are found in Penicillium sclerotiorum and Penicillium hirayamae, but only their optical antipodes are found in Talaromyces.

TAXONOMY

Penicillium itself has a long list of generic synonyms (see Seifert et al. 2011) that must be considered for the species formerly included in subgenus Biverticillium. These synonyms of Penicillium are discussed in the Appendix to this paper. As it turns out, none of these are appropriate for subgenus Biverticillium, leaving the comparatively young Talaromyces as the oldest well-known generic name as the new home for the anamorphic species of subgenus Biverticillium.

Yaguchi et al. (1994a) introduced Erythrogymnotheca for the single species E. paucispora. No specimens of E. paucispora were studied; however, examination of the available ITS data on GenBank and the original description shows that this species belongs in Talaromyces. As a consequence, Erythrogymnotheca is synonymised with Talaromyces. Comparison of an ITS sequence of E. paucispora (AB176603) shows that it is related to P. korosum, P. pinophilum and P. liani in Talaromyces (Fig. 2). The original description suggests that Talaromyces and Erythrogymnotheca differ in ascus characteristics and ascospore morphology. However, these genera also share characters. The ascomatal initials of E. paucispora approximate those of Talaromyces flavus and other species of Talaromyces. Furthermore, E. paucispora produces a loose hyphaI yellow- or red-pigmented ascomata similar to those of other Talaromyces species and the main ubiquinone systems are Q-10 and Q-10 (H₂), also indicating a relationship with Talaromyces (Paterson 1998, Yaguchi et al. 1994a).

Matsushima (2001) described Paratalaromyces from soil collected in Taiwan, distinguishing it by a distinct textura epidermoidea layer in the ascomatal wall, and the presence of spinulose marginal hyphae. We have not seen the type but the description of Paratalaromyces lenticularis is similar to that of Talaromyces unicus (Tzean et al. 1992). We consider the genus a synonym here.

Visagie & Seifert (unpubl. data) report on the generic name Lasioderma Mont., typified by L. flavo-virens Durieu & Mont., which is conspecific with Penicillium aureocephalum Munt.-Cvetk., Hoyo & Gómez-Bolea. The name Lasioderma is widely used as an insect genus, and a formal proposal for the conservation of Talaromyces against this older name is being prepared.

Talaromyces C.R. Benj., Mycologia 47: 681. 1955.

• = Penicillium Link subgenus Biverticillium Dierckx apud Biourge Cellule 33: 31. 1923.

• = Penicillium subg. Biverticillata-Symmetrica Thom, The Penicillia: 158. 1930.

• = Sagenoma Stolk & G.F. Orr, Mycologia 66: 676. 1974.

• = Erythrogymnotheca Yaguchi & Udagawa, Mycoscience 35: 219. 1994.

• = Paratalaromyces Matsush., Matsush. Mycol. Mem. 10: 111 (2003) [2001].

Ascomata cleistothecial, usually with a distinctly hyphal exterior wall, often yellow, occasionally white, creamish, pinkish or reddish. Asci 8-spored, globose to ellipsoidal, ascus initials sometimes with morphologically distinguishable gametangia, mature asci produced in chains. Ascospores one-celled, rarely smooth-walled, but often with surface ornamentation and wings, hyaline to yellow, in strains producing abundant red pigment occasionally red. Conidiophores comprising smooth or rough-walled elements, with long hyaline stipes, generally terminating in a single whorl of 3–10 metulae, appearing symmetrical in face view (in some species with a single subterminal lateral branch that afterwards repeats the branching pattern of the main axis, but then with the whole conidiophore appearing asymmetrical), each metula with a terminal whorl of phialides. Conidiogenous cells phialidic, aculeate or acerose, rarely ampulliform, periclinal thickening usually visible in the conidiogenous aperture, with or without a cylindrical collarette. Conidia aseptate, green in mass, in basipetal connected chains, usually ellipsoidal to fusiform.

Type species: Talaromyces vermiculatus (P.A. Dang.) C.R. Benj., Mycologia 47: 684. 1955.

The name Talaromyces was introduced by Benjamin (1955), and the type species is T. vermiculatus (P.A. Dang.) C.R. Benj. One of the authors (RAS) personally visited several herbaria in Paris to locate holotype or other original material of Penicillium vermiculatum P.A. Dang. Dangeard (1907) described and illustrated both the anamorph and teleomorph under this name, but his material could not be located. To repair the shortcoming of the typification of Talaromyces, the lectotype for P. vermiculatum is here designated as Plate XVIII in Dangeard (1907, available at the Biodiversity Heritage Library, www.biodiversitylibrary.org). It was selected from among the plates XVI—XX because it includes the most detailed drawings of the anamorph, but also includes elements of the teleomorph. Herb. IMI 197477 is here designated as the epitype of Penicillium vermiculatum P.A. Dang. This specimen, which is also the holotype of Penicillium dangeardii J. Pitt, the seldom-used name for the anamorph of T. flavus, is derived from the equivalent cultures CBS 310.38, IMI 19447, and NRRL 2098. The latter strain was considered typical of P. vermiculatum by Raper & Thom (1949), the last major treatment to use this Penicillium name as a distinct species.

ACCEPTED SPECIES IN TALAROMYCES

Talaromyces aculeatus (Raper & Fennell) Samson, Yilmaz, Frisvad & Seifert, comb. nov. MycoBank MB560639.

Basionym: Penicillium aculeatum Raper & Fennell, Mycologia 40: 535. 1948.

Talaromyces albobiverticillius (H.-M. Hsieh, Y.-M. Ju & S.-Y. Hsieh) Samson, Yilmaz, Frisvad & Seifert, comb. nov. MycoBank MB560683.

Basionym: Penicillium albobiverticillium H.-M. Hsieh, Y.-M. Ju & S.-Y. Hsieh, Fung. Sci. 25: 26. 2010.

Talaromyces allahabadensis (B.S. Mehrotra & D. Kumar) Samson, Yilmaz & Frisvad, comb. nov. MycoBank MB560640.

Basionym: Penicillium allahabadense B.S. Mehrotra & D. Kumar, Canad. J. Bot. 40: 1399. 1962.

Talaromyces apiculatus Samson, Yilmaz & Frisvad, sp. nov. MycoBank MB560641.

• = Penicillium aculeatum var. apiculatum Abe, S., 1956, J. Gen. Appl. Microbiol., Tokyo 2: 124. 1956 (nom. inval., Art. 36).

Penicillio aculeato simile, sed conidiis apiculatis distinguitur.

Typus: Japan from soil (CBS H-20755 – Holotype, culture ex-type CBS 312.59)

Note: Species similar to Penicillium aculeatum but differing by apiculate conidia.

Talaromyces assiutensis Samson & Abdel-Fattah, Persoonia 9: 501. 1978.

Anamorphic synonym: Penicillium assiutense Samson & Abdel Fattah (simultaneously published, identical holotype).

Talaromyces aurantiacus (J.H. Mill., Giddens & A.A. Foster) Samson, Yilmaz, & Frisvad, comb. nov. MycoBank MB560642.

Basionym: Penicillium aurantiacum J.H. Mill., Giddens & A.A. Foster, Mycologia 49: 797. 1957.

Talaromyces austrocalifornicus Yaguchi & Udagawa Trans. Mycol. Soc. Japan 34: 245. 1993.

Anamorphic synonym: Penicillium austrocalifornicum Yaguchi & Udagawa (simultaneously published, identical holotype).

Talaromyces bacillisporus (Swift) C. R. Benj., Mycologia 47: 682. 1955.

• ≡ Penicillium bacillisporum Swift, Bull. Torrey Bot. Club 59: 221, 1932.

Talaromyces boninensis (Yaguchi & Udagawa) Samson, Yilmaz, & Frisvad, comb. nov. MycoBank MB560643.

Basionym: Talaromyces helicus var. boninensis Yaguchi & Udagawa, Transactions Mycological Society Japan 33: 511. 1992.

Talaromyces brunneus (Udagawa) Samson, Yilmaz & Frisvad, comb. nov. MycoBank MB560644.

Basionym: Penicillium brunneum Udagawa, J. Agric. Sci. (Tokyo) Nogyo Daigaku 5: 16. 1959.

Talaromyces calidicanius (J.L. Chen) Samson, Yilmaz & Frisvad, comb. nov. MycoBank MB560645.

Basionym: Penicillium calidicanium J.L. Chen, Mycologia 94(5): 870. 2002.

Talaromyces cecidicola (Seifert, Hoekstra & Frisvad) Samson, Yilmaz, Frisvad & Seifert, comb. nov. MycoBank MB560646.

Basionym: Penicillium cecidicola Seifert, Hoekstra & Frisvad, Stud. Mycol. 50: 520. 2004.

Talaromyces coalescens (Quintan.) Samson, Yilmaz & Frisvad, comb. nov. MycoBank MB560647.

Basionym: Penicillium coalescens Quintan., Mycopathol. 84: 115. 1984.

Talaromyces convolutus Udawaga, Mycotaxon 48: 141. 1993.

Anamorphic synonym: Penicillium convolutum Udagawa (simultaneously published, identical holotype).

Talaromyces dendriticus (Pitt) Samson, Yilmaz, Frisvad & Seifert, comb. nov. MycoBank MB560648.

Basionym: Penicillium dendriticum Pitt, The Genus Penicillium: 413. 1980.

Talaromyces derxii Takada & Udagawa, Mycotaxon 31: 418. 1988.

Anamorphic synonym: Penicillium derxii Takata & Udagawa (simultaneously published, identical holotype).

Talaromyces diversus (Raper & Fennell) Samson, Yilmaz & Frisvad, comb. nov. MycoBank MB560649.

Basionym: Penicillium diversum Raper & Fennell, Mycologia 40: 539. 1948.

Talaromyces duclauxii (Delacr.) Samson, Yilmaz, Frisvad & Seifert, comb. nov. MycoBank MB560650.

Basionym: Penicillium duclauxii Delacr., Bull. Soc. Mycol. France 7: 107. 1891.

Talaromyces echinosporus (Nehira) Samson, Yilmaz & Frisvad, comb. nov. MycoBank MB560651.

Basionym: Penicillium echinosporum Nehira, J. Ferment. Technol., Osaka 11: 861. 1933.

Note: Penicillium asperosporum G. Smith, Trans. Brit. Mycol. Soc. 48: 275. 1965. (= Penicillium echinosporum G. Sm., Trans. Brit. Mycol. Soc. 45: 387. 1962, non Nehira in J. Ferment. Technol. 11: 849. 1933) belongs in Penicillium section Aspergilloides (Houbraken & Samson 2011).

Talaromyces emodensis Udagawa, Mycotaxon 48: 146. 1993. Anamorphic synonym: Penicillium emodense Udagawa (simultaneously published, identical holotype).

Talaromyces erythromellis (A.D. Hocking) Samson, Yilmaz, Frisvad & Seifert, comb. nov. MycoBank MB560652.

Basionym: Penicillium erythromellis A.D. Hocking apud Pitt, The Genus Penicillium: 459. 1980.

Talaromyces euchlorocarpius Yaguchi, Someya & Udagawa, Mycoscience 40: 133. 1999.

Anamorphic synonym: Penicillium euchlorocarpium Yaguchi, Someya & Udagawa (simultaneously published, identical holotype).

Note: We have not seen the type, but the description and the ITS sequences available in GenBank (AB176617) show that this is a distinct species of Talaromyces.

Talaromyces flavo-virens (Durieu & Mont.) Visagie, Llimona & Seifert, ined.

Note: A manuscript on this species and its relationship to Penicillium aureocephalum Munt.-Cvetk., Hoyo & Gómez-Bolea is being prepared for publication in Mycotaxon.

Talaromyces flavus (Klöcker) Stolk & Samson, Stud. Mycol. 2: 10. 1972.

Anamorphic synonym: Penicillium dangeardii Pitt, The Genus Penicillium: 472. 1980.

Talaromyces funiculosus (Thom) Samson, Yilmaz, Frisvad & Seifert, comb. nov. MycoBank MB560653.

Basionym: Penicillium funiculosum Thom, Bull. Bur. Anim. Ind. U.S. Dep. Agric. 118: 69. 1910.

Talaromyces galapagensis Samson & Mahoney, Trans. Brit. Mycol. Soc. 69: 158. 1977.

Anamorphic synonym: Penicillium galapagense Samson & Mahoney (simultaneously published, identical holotype).

Talaromyces hachijoensis Yaguchi, Someya & Udagawa, Mycoscience 37: 157. 1996.

Note: We have not seen the type but the description and the ITS sequences available in GenBank (AB176620) show that this is a distinct species of Talaromyces. It is unusual in the genus for its apparent lack of an anamorph.

Talaromyces helicus (Raper & Fennell) C.R. Benj., Mycologia 47: 684. 1955.

• ≡ Penicillium helicum Raper & Fennell, Mycologia 40: 515. 1948.

Talaromyces indigoticus Takada & Udagawa, Mycotaxon 46: 129. 1993.

Anamorphic synonym: Penicillium indigoticum Takada & Udagawa (simultaneously published, identical holotype).

Talaromyces intermedius (Apinis) Stolk & Samson, Stud. Mycol. 2: 21. 1972.

Anamorphic synonym: Penicillium intermedium Stolk & Samson, Stud. Mycol. 2: 21. 1972.

Talaromyces islandicus (Sopp) Samson, Yilmaz, Frisvad & Seifert, comb. nov. MycoBank MB560654.

Basionym: Penicillium islandicum Sopp, Skr. Vidensk.-Selsk. Christiania, Math.-Naturvidensk. Kl. 11: 161. 1912.

Talaromyces loliensis (Pitt) Samson, Yilmaz & Frisvad, comb. nov. MycoBank MB560655.

Basionym: Penicillium loliense Pitt, The Genus Penicillium: 450. 1980

Talaromyces macrosporus (Stolk & Samson) Frisvad, Samson & Stolk, Ant. van Leeuwenhoek 57: 186. 1990.

Anamorphic synonym: Penicillium macrosporum Frisvad, Filt., Samson & Stolk. nom. illegit. Art. 53 (non P. macrosporum Berk. & Broome 1882).

Talaromyces marneffei (Segretain, Capponi & Sureau) Samson, Yilmaz, Frisvad & Seifert, comb. nov. MycoBank MB560656.

Basionym: Penicillium marneffei Segretain, Capponi & Sureau apud Segretain, Bull. Soc. Mycol. France 75: 416. 1959 [1960].

Talaromyces mimosinus A.D. Hocking apud Pitt, The Genus Penicillium: 507. 1980.

Anamorphic synonym: Penicillium mimosinum A. D. Hocking (simultaneously published, identical holotype).

Talaromyces minioluteus (Dierckx) Samson, Yilmaz, Frisvad & Seifert, comb. nov. MycoBank MB560657.

Basionym: Penicillium minioluteum Dierckx, Ann. Soc. Sci. Bruxelles 25: 87. 1901.

Talaromyces muroii Yaguchi, Someya & Udagawa, Mycoscience 35: 252. 1994.

Note: This species is unusual in Talaromyces because of its lack of a known anamorph.

Talaromyces palmae (Samson, Stolk & Frisvad) Samson, Yilmaz, Frisvad & Seifert, comb. nov. MycoBank MB560658.

Basionym: Penicillium palmae Samson, Stolk & Frisvad, Stud. Mycol. 31: 135. 1989.

Talaromyces panamensis (Samson, Stolk & Frisvad) Samson, Yilmaz, Frisvad & Seifert, comb. nov. MycoBank MB560659.

Basionym: Penicillium panamense Samson, Stolk & Frisvad, Stud. Mycol. 31: 136. 1989.

Talaromyces paucisporus (Yaguchi, Someya & Udagawa) Samson & Houbraken, comb.nov. MycoBank MB560684.

Basionym: Erythrogymnotheca paucispora Yaguchi, Someya & Udagawa, Mycoscience 35: 219. 1994.

Talaromyces phialosporus (Udagawa) Samson, Yilmaz & Frisvad, comb. nov. MycoBank MB560660.

Basionym: Penicillium phialosporum Udagawa, J. Agric. Sci. (Tokyo) Nogyo Daigaku 5: 11. 1959.

Talaromyces piceus (Raper & Fennell) Samson, Yilmaz, Frisvad & Seifert, comb. nov. MycoBank MB560661.

Basionym: Penicillium piceum Raper & Fennell, Mycologia 40: 533. 1948.

Talaromyces pinophilus (Hedgcock) Samson, Yilmaz, Frisvad & Seifert, comb. nov. MycoBank MB560662.

Basionym: Penicillium pinophilum Hedgcock apud Thom, Bull. Bur. Anim. Ind. US Dept. Agric. 118: 37. 1910.

Talaromyces pittii (Quintan.) Samson, Yilmaz, Frisvad & Seifert, comb. nov. MycoBank MB560663.

Basionym: Penicillium pittii Quintan., Mycopathol. 91: 69. 1985.

Talaromyces primulinus (Pitt) Samson, Yilmaz & Frisvad, comb. nov. MycoBank MB560664.

Basionym: Penicillium primulinum Pitt, The Genus Penicillium: 455. 1980.

Talaromyces proteolyticus (Kamyschko) Samson, Yilmaz & Frisvad, comb. nov. MycoBank MB560665.

Basionym: Penicillium proteolyticum Kamyschko, Not. Syst. Crypt. Inst. Bot. Acad. Sci. USSR 14: 228. 1961.

Talaromyces pseudostromaticus (Hodges, G.M. Warner, Rogerson) Samson, Yilmaz, Frisvad & Seifert, comb. nov. MycoBank MB560666.

Basionym: Penicillium pseudostromaticum Hodges, G.M. Warner & Rogerson, Mycologia 62: 1106. 1970.

Talaromyces purpureus (E. Müll. & Pacha-Aue) Stolk & Samson, Stud. Mycol. 2: 57. 1972.

Anamorphic synonym: Penicillium purpureum Stolk & Samson, Stud. Mycol. 2: 57. 1972.

Talaromyces purpurogenus (Stoll) Samson, Yilmaz, Frisvad & Seifert, comb. nov. MycoBank MB560667.

Basionym: Penicillium purpurogenum Stoll, Beitr. Charakt. Penicillium-Arten: 32. 1904.

Talaromyces rademirici (Quintan.) Samson, Yilmaz & Frisvad, comb. nov. MycoBank MB560668.

Basionym: Penicillium rademirici Quintan., Mycopathol. 91: 69. 1985.

Talaromyces radicus (A.D. Hocking & Whitelaw) Samson, Yilmaz, Frisvad & Seifert, comb. nov. MycoBank MB560669.

Basionym: Penicillium radicum A.D. Hocking & Whitelaw, Mycol. Res. 102: 802. 1998.

Talaromyces ramulosus (Visagie & K. Jacobs) Samson, Yilmaz, Frisvad & Seifert, comb. nov. MycoBank MB560670.

Basionym: Penicillium ramulosum Visagie & K. Jacobs, Mycologia 101: 890. 2009.

Talaromyces rotundus (Raper & Fennell) C.R. Benj., Mycologia 47: 683. 1955.

• ≡ Penicillium rotundum Raper & Fennell, Mycologia 40: 518. 1948.

Talaromyces ryukyuensis (S. Ueda & Udagawa) Arx, Persoonia 13: 282. 1987.

• ≡ Sagenoma ryukyuense S. Ueda & Udagawa, Mycotaxon 20: 499. 1984.

Note: We have not seen the type but the description and the ITS sequences available in GenBank (AB176628) show that this is a distinct species of Talaromyces.

Talaromyces rubicundus (J.H. Mill., Giddens & A.A. Foster) Samson, Yilmaz, Frisvad & Seifert, comb. nov. MycoBank MB560671.

Basionym: Penicillium rubicundum J.H. Mill., Giddens & A.A. Foster, Mycologia 49: 797. 1957.

Talaromyces rugulosus (Thom) Samson, Yilmaz, Frisvad & Seifert, comb. nov. MycoBank MB560672.

Basionym: Penicillium rugulosum Thom, Bull. Bur. Anim. Ind. US Dept. Agric. 118: 60. 1910.

Talaromyces sabulosus (Pitt & A.D. Hocking) Samson, Yilmaz & Frisvad, comb. nov. MycoBank MB560673.

Basionym: Penicillium sabulosum Pitt & A. D. Hocking, Mycologia 77: 818. 1985.

Talaromyces siamensis (Manoch & C. Ramírez) Samson, Yilmaz & Frisvad, comb. nov. MycoBank MB560674.

Basionym: Penicillium siamense Manoch & C. Ramírez, Mycopathol. 101: 32. 1988.

Talaromyces stipitatus (Thom) C.R. Benj., Mycologia 47: 684. 1955.

• ≡ Penicillium stipitatum Thom, Mycologia 27: 138. 1935.

Talaromyces sublevisporus (Yaguchi & Udagawa) Samson, Yilmaz & Frisvad, comb. et stat. nov. MycoBank MB560675.

Basionym: Talaromyces wortmannii var. sublevisporus Yaguchi & Udagawa, Mycoscience 35: 63. 1994.

Note: We have not examined the ex-type of this species but from the ITS data (GenBank AB176638), this seems to be a separate species.

Talaromyces tardifaciens Udagawa, Mycotaxon 48: 150. 1993.

Anamorphic synonym: Penicillium tardifaciens Udagawa (simultaneously published, identical holotype).

Talaromyces trachyspermus (Shear) Stolk & Samson, Stud. Mycol. 2: 32. 1972.

Anamorphic synonym: Penicillium spiculisporum Leman, Mycologia 12: 268. 1920.

Talaromyces ucrainicus Udagawa, in Stolk & Samson, Stud. Mycol. 2: 34. 1972.

Anamorphic synonym: Penicillium ucrainicum Panasenko, Mycologia 56: 59. 1964.

Talaromyces udagawae Stolk & Samson, Stud. Mycol. 2: 36. 1972.

Anamorphic synonym: Penicillium udagawae Stolk & Samson (simultaneously published, identical holotype).

Talaromyces unicus Tzean, J.L. Chen & Shiu, Mycologia 84: 739. 1992.

Anamorphic synonym: Penicillium unicum Tzean, J.L. Chen & Shiu (simultaneously published, identical holotype).

Talaromyces variabilis (Sopp) Samson, Yilmaz, Frisvad & Seifert, comb. nov. MycoBank MB560676.

Basionym: Penicillium variabile Sopp, Skr. Vidensk.-Selsk. Christiania, Math.-Naturvidensk. Kl. 11: 169. 1912.

Talaromyces varians (G. Sm.) Samson, Yilmaz & Frisvad, comb. nov. MycoBank MB560677.

Basionym: Penicillium varians G. Sm., Trans. Brit. Mycol. Soc. 18: 89. 1933.

Talaromyces verruculosus (Peyronel) Samson, Yilmaz, Frisvad & Seifert, comb. nov. MycoBank MB560678.

Basionym: Penicillium verruculosum Peyronel, Germi Atmosf. Fung. Micel.: 22. 1913.

Talaromyces viridis (Stolk & G.F. Orr) von Arx, Persoonia 13: 2821. 1987.

• ≡ Sagenoma viride Stolk & G.F. Orr, Mycologia 66: 677. 1974.

Talaromyces viridulus Samson, Yilmaz & Frisvad, nom. nov. MycoBank MB560679.

Basionym: Geosmithia viridis Pitt & A.D. Hocking, Mycologia 77: 822. 1985 = P. viride (Pitt & A.D. Hocking) Frisvad, Samson & Stolk, Persoonia 14: 229. 1990, nom. illegit. Art. 53 (non Fres. 1851 nec Rivera 1873 nec Sopp 1912 nec (Matr.) Biourge 1923). Non Talaromyces viridis (Stolk & G.F. Orr) Arx.

Talaromyces wortmannii (Klöcker) C.R. Benjamin, Mycologia 47: 683. 1955.

• ≡ Penicillium wortmannii Klöcker, Compt-Rend. Trav. Carlsberg Lab. 6: 100. 1903.

EXCLUDED SPECIES AND TAXA, WHICH NEED FURTHER TAXONOMIC STUDY

Penicillium concavorugulosum S. Abe, J. Gen. Appl. Microbiol, Tokyo 2: 127. 1956 (nom. inval. Art. 36).

Note: This species was invalidly described, but our ITS data (Fig. 2) show that it is related to T. wortmanii. Further study is required but extrolite data indicate that this species is unique (J.C. Frisvad, unpubl. data).

Penicillium crateriforme J.C. Gilman & E.V. Abbott, Iowa State Coll. J. Sc. 1: 293. 1927.

Note: Our ITS data (Fig. 2) show that this species is a synonym of P. purpurogenum.

Penicillium ilerdanum C. Ramírez, A.T. Martínez & Berer., Mycopathol. 72: 32. 1980.

Note: Frisvad et al. (1990b) considered this species synononymous with Penicillium piceum Raper & Fennell, which is confirmed by our ITS data (Fig. 2).

Penicillium isariiforme Stolk & J.A. Mey., Trans. Brit. Mycol. Soc. 40: 187. 1957.

Note: According to Houbraken & Samson (2011), this species, included in subgenus Biverticillium by Pitt (1980), is correctly classified in Penicillium sensu lato.

Penicillium korosum J.N. Rai, Wadhwani & J.P. Tewari, Ant. van Leeuwenhoek 35: 430. 1969.

Note: This species requires further investigation, but our ITS sequence (Fig. 2) indicates that it is similar to P. pinophilum.

Penicillium krugeri C. Ramírez, Mycopathol. 110: 23. 1990.

Note: We have been unable to examine authentic material, and the correct classification of this species is uncertain.

Penicillium lignorum Stolk, Ant. van Leeuwenhoek 35: 264. 1969.

Note: A preliminary phylogenetic analysis indicates that this species does not belong to Talaromyces and might represent a new genus (J. Houbraken, unpubl. data).

Penicillium mirabile Beliakova & Milko, Mikol. Fitopatol. 6: 145. 1972.

Note: The ex-type culture is in poor condition and although our ITS data (Fig. 2) indicate that is a distinct species, it should be further investigated.

Penicillium oblatum Pitt & A.D. Hocking, Mycologia 77: 810. 1985.

Note: In our ITS phylogeny (Fig. 2), this species is close to Paecilomyces pascuus and Penicillium dendriticum and needs further study.

Penicillium pascuum (Pitt & A.D. Hocking) Frisvad, Samson & Stolk, Persoonia 14: 229. 1990.

• ≡ Paecilomyces pascuus Pitt & A. D. Hocking, Mycologia 77: 822. 1985.

Note: See on the position of this species under P. oblatum above.

Penicillium rubrum Stoll, Beitr. Charakt. Penicillium-Arten: 35. 1904.

Note: Although the name is well-known, the taxonomic position of the taxon remains doubtful because no type material has been located. A possible solution would be lectotypification from Stoll's illustrations, followed by epitypification to become a usable name.

Penicillium purpurogenum var. rubrisclerotium Thom, Mycologia 7: 137. 1915.

Note: Our ITS data (Fig. 2) indicate that this species is synonymous with P. minioluteum.

Penicillium samsonii Quintan., Mycopathol. 91: 69. 1985.

• = Talaromyces minioluteus (Dierckx) Samson, Yilmaz, Frisvad & Seifert (see above).

Penicillium tardum Thom, The Penicillia: 485. 1930.

Note: Raper & Thom (1949) pointed out that there is confusion about the type culture and the status of this species will be subject of further studies.

Penicillium victoriae Szilv., Archiv. Hydrobiol. 14, Suppl. 6: 535. 1936.

• = Penicillium janthinellum Biourge, Cellule 33: 258. 1923 (Pitt, 1980).

Note: Pitt (1980) synonymised this species under Penicillium janthinellum, but our studies showed that it clearly belongs in Talaromyces. Because there is only one strain, the exact identity of this fungus requires further study.

Talaromyces barcinensis Yaguchi & Udagawa, Trans. Mycol. Soc. Japan 34: 15. 1993.

Anamorphic synonym: Penicillium barcinense Yaguchi & Udagawa (simultaneously published, identical holotype).

Note: Our ITS sequence data show that this species is close to Talaromyces helicus and further study should determine its correct taxonomic position.

Talaromyces brevicompactus Kong, Mycosystema 18: 9. 1999.

Anamorphic synonym: Merimbla brevicompacta Kong, Mycosystema 18: 9. 1999 (simultaneously published, identical holotype).

Note: Fig. 1 shows that this species belongs in Hamigera. Comparison of partial β-tubulin and calmodulin sequences of the ex-type strain of T. brevicompactus with recent published data shows that this species represents a distinct species (J. Houbraken, unpubl. data). The new combination in Hamigera will be made elsewhere.

Talaromyces byssochlamydoides Stolk & Samson, Stud. Mycol. 2: 45. 1972.

Anamorphic synonym: Paecilomyces byssochlamydoides Stolk & Samson (simultaneously published, same holotype).

• = Rasamsonia byssochlamydoides (Stolk & Samson) Houbraken & Frisvad, Ant. van Leeuwenhoek, in press.

Talaromyces eburneus Yaguchi, Someya & Udagawa, Mycoscience 35: 249. 1994.

Anamorphic synonym: Geosmithia eburnea Yaguchi, Someya & Udagawa (simultaneously described, holotype identical)

• ≡ Rasamsonia eburnea (Yaguchi, Someya & Udagawa) Houbraken & Frisvad, Ant. van Leeuwenhoek, in press.

Talaromyces emersonii Stolk, Ant. van Leeuwenhoek 31: 262. 1965.

Anamorphic synonym: Penicillium emersonii Stolk (simultaneously described, holotype identical), Ant. van Leeuwenhoek 31: 262. 1965.

• = Rasamsonia emersonii (Stolk) Houbraken & Frisvad, Ant. van Leeuwenhoek, in press.

Talaromyces gossypii Pitt, The Genus Penicillium: 500. 1980

• = Talaromyces assiutensis, Samson & Abdel-Fattah, Persoonia 9: 501. 1978 (fide Frisvad et al. 1990a).

Talaromyces lagunensis Udagawa, Uchiy. & Kamiya, Mycoscience 35: 403. 1994.

Anamorphic synonym: Penicillium lagunense Udagawa, Uchiy. & Kamiya (simultaneously published, identical holotype).

Note: We have been unable to examine authentic material, and the correct classification of this species is uncertain.

Talaromyces leycettanus H.C. Evans & Stolk, Trans. Brit. Mycol. Soc. 56: 45. 1971.

Anamorphic synonym: Penicillium leycettanus H.C. Evans & Stolk (simultaneously published, identical holotype).

• ≡ Paecilomyces leycettanus (H.C. Evans & Stolk) Stolk, Samson & H.C. Evans, Persoonia 6: 342. 1971.

Note: Houbraken & Samson (2011) showed that this species is phylogenetically unrelated to Talaromyces and close to Hamigera. Its taxonomic position requires further investigation.

Talaromyces luteus (Zukal) C.R. Benj., Mycologia 47: 681. 1955.

• ≡ Penicillium luteum Zukal, Sitzungsber Kaiserl. Akad. Wiss. Math-Naturwiss. C1., Abt. 1, 98: 561. 1890.

Note: Although the phenotype of this species resembles species of Talaromyces, our molecular analysis shows that it is phylogenetically unique and basal to T. thermophilus.

Talaromyces malagensis (Thüm.) Stalpers & Samson 1984, in Stalpers, Stud. Mycol. 24: 69. 1984.

Note: Stolk & Samson (1972) considered Sporotrichum malagense a dubious synonym of T. udagawae, based on their failure to find ascospores and conidia in the type material (herb. W). Later, Stalpers (1984) studied material preserved in herb. BR which is authentic and labelled as “type”. It agrees with Thümen's original diagnosis and contains both fertile Talaromyces cleistothecia and a sporulating biverticillate anamorph. Therefore, the new combination to Talaromyces was proposed. The species resembles T. udagawae or T. luteus, but in the absence of a living culture we cannot determine its precise taxonomic identity.

Talaromyces ocotl Bills & Heredia, Mycologia 90: 533. 1998.

Note: Figure 1 shows that this species belongs to Sagenomella and the new combination is proposed here:

Sagenomella ocotl (Bills & Heredia) Samson, Houbraken & Frisvad, comb. nov. MycoBank MB560681.

Basionym: Talaromyces ocotl Bills & Heredia, Mycologia 93: 533. 1998.

Talaromyces ohiensis Pitt, The Genus Penicillium: 502. 1980.

Anamorphic synonym: Penicillium ohiense L. H. Huang & J. A. Schmitt, Ohio J. Sci. 75: 78. 1975.

Note: Pitt (1980) considered this species to be related to T. luteus, but our ITS data clearly show that is synonymous with T. ucrainicus.

Talaromyces panasenkoi Pitt, The Genus Penicillium: 482. 1980.

Anamorphic synonym: Penicillium panasenkoi Pitt (simultaneously published, identical holotype).

Note: Pitt (1980) proposed T. panasenkoi as a new species for the invalidly published P. ucraininum Panasenko; however, Stolk & Samson (1972) had already proposed Talaromyces ucrainicus Udagawa for this taxon. Talaromyces panasenkoi Pitt is therefore a synonym of T. ucrainicus.

Talaromyces retardatus Udagawa, Kamiya & Kaori Osada, Trans. Mycol. Soc. Japan 34: 9. 1993.

Anamorphic synonym: Penicillium retardatum Udagawa, Kamiya & Kaori Osada (simultaneously published, identical holotype).

Note: No strain was available for examination and the status of this species is thus unknown.

Talaromyces spectabilis Udagawa & Suzuki, Mycotaxon 50: 82. 1994.

• = Byssochlamys spectabilis (Udagawa & Suzuki) Houbraken & Samson, Appl. Environ. Microbiol. 74: 1618. 2008.

• = Paecilomyces variotii Bainier Bull. Soc. mycol. Fr. 23: 27. 1907.

Note: The oldest generic and species name for this species is P. variotii, which becomes the correct name for the holomorph.

Talaromyces striatus (Raper & Fennell) C.R. Benj., Mycologia 47: 682. 1955.

• = Hamigera striata (Raper & Fennell) Stolk & Samson, Persoonia 6: 347. 1971.

Talaromyces thermocitrinus Subrahm. & Gopalkr., Ind. Bot. Reporter 35: 35. 1984 (as ‘T. thermocitrinum’).

Note: We have not seen the type, but judging from the substrate (dust on books), and the mention of yellow cleistothecia, it is possible that this is an Eurotium species, a typical contaminant of books and other material in archives. However, its reported thermophily is different from known species of the mesophilic genus Eurotium.

Talaromyces thermophilus Stolk, Ant. van Leeuwenhoek 31: 268. 1965.

Basionym: Penicillium dupontii Griffon & Maubl., Bull. Trimmest. Soc. mycol. Fr. 27: 73. 1911.

Note: Figure 1 shows that this species is related to Thermomyces lanuginosus, and should be transferred to Thermomyces (Houbraken et al. 2011,2011, Houbraken & Samson 2011).

APPENDIX: OTHER POSSIBLE GENERIC NAMES

As noted above in the Taxonomy section, in order to adopt Talaromyces as the generic name for the former Penicillium subgenus Biverticillium, older genera considered synonyms of Penicillium sensu lato had to be considered. These are treated below.

Aspergillopsis Sopp, Vid.-Selsk. Skr. I. Math.-naturv. Kl. 11: 201. 1912. (Taf. xx, Fig. 149, Taf. xxiii, Fig. 31).

Type species: A. fumosus Sopp 1912.

Note: This generic name is illegitimate (Art. 53), being a later homonym of Aspergillopsis Speg. 1910. Pitt (1980) considered Sopp's genus a tentative synonym of Merimbla Pitt.

Citromyces Wehmer, Ber. dt. Bot. Ges. 11: 338. 1893.

Type species: C. pfefferianus Wehmer 1893 = Penicillium glabrum (Wehmer) Westling 1911, fide Pitt 1980.

Note: Wehmer's genus was considered a synonym of Penicillium by many authors, including Raper & Thom (1949) and Pitt (1980), with C. pfefferianus considered a probable synonym of P. glabrum (subgenus Aspergillioides) by Pitt (1980). Therefore, the genus remains a synonym of Penicillium sensu stricto.

Coremium Link: Fr., Mag. Ges. naturf. Freunde, Berlin 3: 19. 1809: Fries, Syst. mycol. 1: xlviii, 1821.

Type species: C. glaucum Link 1809.

Note: This genus was described in the same publication as Penicillium. Raper & Thom (1949) and Seifert & Samson (1985) both considered the type species to be a synonym of the type species of Penicillium, P. expansum Link 1809. Therefore, Coremium remains a synonym of Penicillium sensu stricto.

Eladia G. Sm., Trans. Br. mycol. Soc. 44: 47. 1961.

Type species: Eladia saccula (Dale) G. Sm. 1961 = Penicillium sacculum Dale 1926.

Note: This genus was considered a synonym of Penicillium by Stolk & Samson (1985), but was considered distinct by Pitt (1980), and von Arx (1981). In the multigene phylogenetic study by Houbraken & Samson (2011), Eladia is clearly included in Penicillium sensu stricto and that synonymy is accepted here.

Floccaria Grev., Scott. Crypt. Fl., Vol. 6, Pl. 301. 1828.

Type species: F. glauca Grev. 1828.

Note: There is no known extant type according to Seifert & Samson (1985), who searched for it in K and E. The illustration shows a synnematous fungus that could well be P. expansum, but there are no microscopic details. Therefore, this name can be discounted as a possible generic name for the species formerly ascribed to subgenus Biverticillium.

Geosmithia Pitt, Can. J. Bot. 57: 2021. 1980.

Type species: Geosmithia lavendula (Raper & Fennell) Pitt 1980 = Penicillium lavendulum Raper & Fennell 1948.

Note: Although von Arx (1981) considered Geosmithia a synonym of Penicillium, it is polyphyletic as presently circumscribed. Using SSU sequences, Ogawa et al. (1997) showed that G. lavendula, and a second common species G. putterilli, belong to the Bionectriaceae, Hypocreales. Similar results were obtained using ITS sequences by Kolařík et al. (2004), using LSU sequences by Schroers et al. (2005) and then multigene phylogenies by Kolařík & Kirkendall (2010). Despite this, some anamorphs attributed to Geosmithia have been described recently in Talaromyces (e.g. Yaguchi et al. 2005). Because the type species is not associated with the same order as Penicillium, Geosmithia need not be considered as a possible home for species of subgenus Biverticillium, but neither should it be considered a synonym of Penicillium.

Hormodendrum Bonord., Handbuch allg. Mykol.: 76. 1851.

Type species: Amphitrichum olivaceum Corda 1837 = Hormodendrum olivaceum (Corda) Bonord. 1851, lectotype selected by Clements & Shear 1931.

Note: Hormodendron has variously been treated as a synonym of Penicillium by von Arx (1974) and de Hoog & Hermanides-Nijhoff (1977) but more often as a synonym of Cladosporium Link, following the study of the type specimen by Hughes (1958). There is no reason to consider this name further as a synonym of Penicillium or as a possible receptacle for the species of subgenus Biverticillium.

Merimbla Pitt, Can. J. Bot. 57: 2394. 1980.

Type species: M. ingelheimensis (F.H. Beyma) Pitt 1980 = Penicillium ingelheimense F.H. Beyma 1942.

Note: Merimbla was considered a possible synonym of Penicillium by von Arx (1981), but this has not generally been accepted. Merimbla ingelheimensis was considered the anamorph of Hamigera avellanea by Stolk & Samson (1971), but is now known to be a closely related but phylogenetically distinct species (Peterson et al. 2010). The Hamigera clade is phylogenetically distinct from subgenus Biverticillium in the multigene analyses of Peterson et al. (2010) and Houbraken & Samson (2011). In a single name system, we consider Merimbla a synonym of the older genus Hamigera.

Monilia Fr., Syst. mycol. 3: 409. 1832.

Type species: M. caespitosa (L.: Fr.) Fr. 1832 / Mucor caespitosus L. 1753.

Note: Donk (1963) suggested that M. caespitosa might be a species of Penicillium based on the protologue. However, this generic name was formally rejected to conserve usage of Monilia Bonorden for the well-known genus of fruit pathogens. Therefore, it is unavailable as a possible generic name for species included in subgenus Biverticillium.

Moniliger Letell., Fig. Champ., Pl. 668. 1839. Figs 3, 4.

Type species: not designated, two original species.

Note: According to Seifert et al. (2011), Letellier included two species, with illustrations clearly representing Aspergillus. The synonymy of Moniliger with Penicillium proposed by Kirk et al. (2008) thus seems unlikely, and the genus is better listed as a synonym of Aspergillus.

Penicillium Link: Fr., Mag. Ges. naturf. Freunde, Berlin 3: 16. 1809.: Fries, Syst. mycol. 3: 406. 1832.

Type species: P. expansum Link 1809, fide Thom 1910.

Note: With this revision, and that of Houbraken & Samson (2011), Penicillium is now used exclusively for the nominal Clade including P. expansum, and species in the now synonymous genus Eupenicillium F. Ludw. 1892 (Houbraken & Samson 2011).

Pritzeliella Henn., Hedwigia Beibl. 42: 88. 1903.

Type species: P. caerulea Henn. 1903.

Note: Clements & Shear (1931) suggested that Pritzeliella should be considered a synonym of Penicillium without further commenting on the identity of its type species. Seifert & Samson (1985) examined the holotype of P. caerulea and considered it a synonym of Penicillium coprophilum (subgenus Penicillium). Its status as a synonym of Penicillium sensu stricto thus remains unchanged.

Rhodocephalus Corda, Ic. Fung. 1: 21. 1837 (Tab. vi, Fig. 282).

Type species: R. candidus Corda 1837 = Penicillium leucocephalum Rabenh. 1844.

Note: Corda (1837) illustrated and described his species as having aseptate stipes, a branched, asymmetrical penicillate head, with long chains of ameroconidia. Rabenhorst (1844) renamed the species in Penicillium, changing the epithet, a conclusion followed by Lindau (1907). Thom (1930) and Raper & Thom (1949) disagreed, stating that the illustration in the protologue has branched conidial chains that would exclude the fungus from Penicillium. This a debatable conclusion, because the chains are simply overlapping in the illustration and there is no clear indication of branching. Pitt (1980) evidently did not examine the protologue when he suggested a synonymy with Aspergillus candidus. Hughes (1958) did not report on the type, and according to Holubová (in litt. to Seifert, 1991), there is no material of Rhodocephalus in the Corda herbarium (PRM). The asymmetrical conidiophores illustrated by Corda discount this as a possible genus for species of subgenus Biverticillium, but its exact identity is unknown.

Torulomyces Delitsch, Systematik der Schimmelpilze: 91. 1943 (Taf. 30, Figs 232–235).

Type species: T. lagena Delitsch 1943 = Monocillium lagena (Delitsch) Hashmi, W.B. Kendr. & Morgan-Jones 1972 = Penicillium lagena (Delitsch) Stolk & Samson 1983.

Note: Torulomyces was included as a synonym of Penicillium sensu stricto in the phylogenetic study of Houbraken & Samson (2011).

Yunnania H.-Z. Kong, Mycotaxon 69: 320. 1998.

Type species: Y. penicillata H.-Z. Kong 1998.

Note: Houbraken & Samson (2011) sequenced the ITS of authentic cultures of Y. penicillata, showing a relationship with the Microascales, suggesting a synonymy with Scopulariopsis or Scedosporium might be appropriate.

Acknowledgments

REFERENCES