Phylogeny and nomenclature of the genus Talaromyces and taxa accommodated in Penicillium subgenus Biverticillium.

The taxonomic history of anamorphic species attributed to Penicillium subgenus Biverticillium is reviewed, along with evidence supporting their relationship with teleomorphic species classified in Talaromyces. To supplement previous conclusions based on ITS, SSU and/or LSU sequencing that Talaromyces and subgenus Biverticillium comprise a monophyletic group that is distinct from Penicillium at the generic level, the phylogenetic relationships of these two groups with other genera of Trichocomaceae was further studied by sequencing a part of the RPB1 (RNA polymerase II largest subunit) gene. Talaromyces species and most species of Penicillium subgenus Biverticilliumsensu Pitt reside in a monophyletic clade distant from species of other subgenera of Penicillium. For detailed phylogenetic analysis of species relationships, the ITS region (incl. 5.8S nrDNA) was sequenced for the available type strains and/or representative isolates of Talaromyces and related biverticillate anamorphic species. Extrolite profiles were compiled for all type strains and many supplementary cultures. All evidence supports our conclusions that Penicillium subgenus Biverticillium is distinct from other subgenera in Penicillium and should be taxonomically unified with the Talaromyces species that reside in the same clade. Following the concepts of nomenclatural priority and single name nomenclature, we transfer all accepted species of Penicillium subgenus Biverticillium to Talaromyces. A holomorphic generic diagnosis for the expanded concept of Talaromyces, including teleomorph and anamorph characters, is provided. A list of accepted Talaromyces names and newly combined Penicillium names is given. Species of biotechnological and medical importance, such as P. funiculosum and P. marneffei, are now combined in Talaromyces. Excluded species and taxa that need further taxonomic study are discussed. An appendix lists other generic names, usually considered synonyms of Penicillium sensu lato that were considered prior to our adoption of the name Talaromyces. TAXONOMIC NOVELTIES: Taxonomic novelties:New species - Talaromyces apiculatus Samson, Yilmaz & Frisvad, sp. nov. New combinationsand names - Talaromyces aculeatus (Raper & Fennell) Samson, Yilmaz, Frisvad & Seifert, T. albobiverticillius (H.-M. Hsieh, Y.-M. Ju & S.-Y. Hsieh) Samson, Yilmaz, Frisvad & Seifert, T. allahabadensis (B.S. Mehrotra & D. Kumar) Samson, Yilmaz & Frisvad, T. aurantiacus (J.H. Mill., Giddens & A.A. Foster) Samson, Yilmaz, & Frisvad, T. boninensis (Yaguchi & Udagawa) Samson, Yilmaz, & Frisvad, T. brunneus (Udagawa) Samson, Yilmaz & Frisvad, T. calidicanius (J.L. Chen) Samson, Yilmaz & Frisvad, T. cecidicola (Seifert, Hoekstra & Frisvad) Samson, Yilmaz, Frisvad & Seifert, T. coalescens (Quintan.) Samson, Yilmaz & Frisvad, T. dendriticus (Pitt) Samson, Yilmaz, Frisvad & Seifert, T. diversus (Raper & Fennell) Samson, Yilmaz & Frisvad, T. duclauxii (Delacr.) Samson, Yilmaz, Frisvad & Seifert, T. echinosporus (Nehira) Samson, Yilmaz & Frisvad, comb. nov. T. erythromellis (A.D. Hocking) Samson, Yilmaz, Frisvad & Seifert, T. funiculosus (Thom) Samson, Yilmaz, Frisvad & Seifert, T. islandicus (Sopp) Samson, Yilmaz, Frisvad & Seifert, T. loliensis (Pitt) Samson, Yilmaz & Frisvad, T. marneffei (Segretain, Capponi & Sureau) Samson, Yilmaz, Frisvad & Seifert, T. minioluteus (Dierckx) Samson, Yilmaz, Frisvad & Seifert, T. palmae (Samson, Stolk & Frisvad) Samson, Yilmaz, Frisvad & Seifert, T. panamensis (Samson, Stolk & Frisvad) Samson, Yilmaz, Frisvad & Seifert, T. paucisporus (Yaguchi, Someya & Udagawa) Samson & Houbraken T. phialosporus (Udagawa) Samson, Yilmaz & Frisvad, T. piceus (Raper & Fennell) Samson, Yilmaz, Frisvad & Seifert, T. pinophilus (Hedgcock) Samson, Yilmaz, Frisvad & Seifert, T. pittii (Quintan.) Samson, Yilmaz, Frisvad & Seifert, T. primulinus (Pitt) Samson, Yilmaz & Frisvad, T. proteolyticus (Kamyschko) Samson, Yilmaz & Frisvad, T. pseudostromaticus (Hodges, G.M. Warner, Rogerson) Samson, Yilmaz, Frisvad & Seifert, T. purpurogenus (Stoll) Samson, Yilmaz, Frisvad & Seifert, T. rademirici (Quintan.) Samson, Yilmaz & Frisvad, T. radicus (A.D. Hocking & Whitelaw) Samson, Yilmaz, Frisvad & Seifert, T. ramulosus (Visagie & K. Jacobs) Samson, Yilmaz, Frisvad & Seifert, T. rubicundus (J.H. Mill., Giddens & A.A. Foster) Samson, Yilmaz, Frisvad & Seifert, T. rugulosus (Thom) Samson, Yilmaz, Frisvad & Seifert, T. sabulosus (Pitt & A.D. Hocking) Samson, Yilmaz & Frisvad, T. siamensis (Manoch & C. Ramírez) Samson, Yilmaz & Frisvad, T. sublevisporus (Yaguchi & Udagawa) Samson, Yilmaz & Frisvad, T. variabilis (Sopp) Samson, Yilmaz, Frisvad & Seifert, T. varians (G. Sm.) Samson, Yilmaz & Frisvad, T. verruculosus (Peyronel) Samson, Yilmaz, Frisvad & Seifert, T. viridulus Samson, Yilmaz & Frisvad.

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 , 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 , 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 ).

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 ). 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 ).

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 ). 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

Sources of cultures

The fungi examined include type strains or representatives of all available species of Talaromyces and Biverticillium. The strains are maintained in the CBS-KNAW Fungal Biodiversity Centre (CBS) culture collection and an overview of strains used for phylogenetic analysis is shown in Table 1. In a few cases, the ex-type strain was unavailable and sequence data present in GenBank were used.

Table 1

Strains used in phylogenetic analysis of Talaromyces.

Name	Collection no.	Origin	GenBank Accession number
			RPB1	ITS
“Aphanoascus cinnabarinus”	CBS 267.72 = ATCC 26215	Soil, Japan	JN121625	JN899376
Aspergillus aculeatus	CBS 172.66T = ATCC 16872 = IMI 211388	Tropical soil	JN121590
Aspergillus clavatoflavus	CBS 473.65NT = ATCC 16866 = IMI 124937	Rain forest soil, Tulley, Queensland, Australia	JN121686
Aspergillus flavus	NRRL 3357 = CBS 128202 = ATCC 200026	Peanut cotyledons, USA	Unpublished
Aspergillus fumigatus	Af293	Patient with invasive aspergillosis	Nierman et al. (2005)
Aspergillus niger	CBS 513.88	Derived from NRRL 3122 and currently used as enzyme production strain	Pel et al. (2007)
Aspergillus ochraceoroseus	CBS 101887 = ATCC 42001 = IBT 14580	Soil, Tai National Forest, Ivory Coast	JN121557
Aspergillus ochraceus	CBS 108.08NT = ATCC 1008 = CBS 547.65 = IMI 016247 = IMI 016247iii = IMI 016247iv = NRRL 1642 = NRRL 398	Unknown source	JN121562
Aspergillus penicillioides	CBS 130294	Indoor environment, Germany	JN121578
Aspergillus robustus	CBS 649.93T = CBS 428.77 = IBT 14305	Surface soil from thorn-forest, near Mombasa, Kenya	JN121711
Aspergillus sparsus	CBS 139.61NT = ATCC 16851 = IMI 019394 = IMI 019394ii = MUCL 31314 = NRRL 1933	Soil, Costa Rica	JN121586
Aspergillus steynii	CBS 112812T = IBT 23096	Dried arabica green coffee bean, on parchment, internal infection, Chamumdeshuran Estata, Karnataka, district Giris, India	JN121569
Aspergillus sydowii	CBS 264.81	Grains and milling fractions, Triticum aestivum, India	JN121624
Aspergillus versicolor	CBS 245.65 = ATCC 11730 = ATCC 16020 = IMI 045554 = IMI 045554ii = IMI 045554iii = IMI 045554iv = MUCL 19008	Cellophane, Indiana, USA	JN121614
Aspergillus zonatus	CBS 506.65NT = ATCC 16867 = IMI 124936	Forest soil, Province of Linon, Fortuna, Costa Rica	JN121691
Byssochlamys nivea	CBS 100.11T = ATCC 22260	Unknown source	JN121511
Byssochlamys spectabilis	CBS 101075T = ATCC 90900 = FRR 5219	Heat processed fruit beverage, Tokyo, Japan	JN121554
Byssochlamys verrucosa	CBS 605.74T = ATCC 34163	Nesting material of Leipoa ocellata (Malleefowl), Pulletop Nature Reserve, New South Wales, Australia	JN680311
Chrysosporium inops	CBS 132.31T = IMI 096729 = UAMH 802	Skin of man, Italy	JN121584
Coccidioides immitis	Strain “RS”	Vaccine strain - origin unknown	Sharpton et al. (2009)
Emericella nidulans	FGSC A4 (= ATCC 38163 = CBS 112.46)	Unknown source	Galagan et al. (2005)
Eurotium herbariorum	CBS 516.65NT = ATCC 16469 = IMI 211383 = NRRL 116	Unpainted board, Washington, USA	JN121693
Geosmithia viridis	CBS 252.87T = FRR 1863 = IMI 288716	Soil, bank of creek flowing into Little River, New South Wales	JN680284	JN899314
Hamigera avellanea	CBS 295.48T = ATCC 10414 = IMI 040230 = NRRL 1938	Soil, San Antonio, Texas, USA	JN121632
Hamigera striata	CBS 377.48NT = ATCC 10501 = IMI 039741 = NRRL 717	Canned blueberries, USA	JN121665
Monascus purpureus	CBS 109.07T = ATCC 16365 = ATCC 16426 = IMI 210765 = NRRL 1596	Fermented rice grain, ‘ang-quac’ (purple coloured rice), Kagok-Tegal, imported from China, Prov. Quouan-toung, Java, Indonesia	JN121563
Paecilomyces aerugineus	CBS 350.66T = IMI 105412	Debris of Glyceria maxima, Attenborough, Notts., UK	JN121657	JN899388
Paecilomyces pascuus	CBS 253.87T = FRR 1925	Pasture grass, Otara, New Zealand	JN899292	JN899321
Penicilliopsis clavariiformis	CBS 761.68 = CSIR 1135	Unknown source, Pretoria, South Africa	JN121716
Penicillium aculeatum	CBS 100105 = CBS 289.48 = ATCC 10409 = IMI 040588 = NRRL 2129 = NRRL A-1474	Textile, USA		JN899389
	CBS 289.48NT = ATCC 10409 = IMI 040588 = NRRL 2129 = NRRL A-1474	Textile, USA		JN899378
Penicillium aculeatum var. apiculatum	CBS 312.59T = ATCC 18315 = FRR 635 = IMI 068239	Soil, Japan	JN680293	JN899375
Penicillium allahabadense	CBS 453.93T = ATCC 15067 = CBS 304.63	Soil of cultivated field, pH 6.9, Allahabad, India	JN680309	JN899345
Penicillium arenicola	CBS 220.66T = ATCC 18321 = ATCC 18330 = IMI 117658 = NRRL 3392	Soil from pine forest, Kiev, Ukraine	JN121601
Penicillium aurantiacum	CBS 314.59T = ATCC 13216 = IMI 099722 = NRRL 3398	Soil, Georgia		JN899380
Penicillium aureocephalum	CBS 102801T	Quercus ruber, Gerona, Selva de Mar, Catalania, Spain		JN899392
Penicillium brunneum	CBS 227.60T = ATCC 18229 = FRR 646 = IFO 6438 = IHEM 3907 = IMI 078259 = MUCL 31318	Milled rice imported into Japan, Thailand	JN680281	JN899365
Penicillium calidicanium	CBS 112002T	Soil, Nantou County, Taiwan	JN899305	JN899319
Penicillium canescens	CBS 300.48NT = ATCC 10419 = IMI 028260 = MUCL 29169 = NRRL 910	Soil, England	JN121636
Penicillium catenatum	CBS 352.67T = ATCC 18543 = IMI 136241	Desert soil, Upington, Cape Province, South Africa	JN121659
Penicillium cinnamopurpureum	CBS 490.66 = ATCC 18337 = IMI 114483	Cultivated soil, South Africa	JN121690
Penicillium citrinum	CBS 139.45T = ATCC 1109 = IMI 091961 = MUCL 29781 = NRRL 1841	Unknown source	JN121585
Penicillium coalescens	CBS 103.83T	Soil under Pinus sp., near Vulladolid, Spain		JN899366
Penicillium concavorugulosum	CBS 898.73T = ATCC 20202	Unknown substrate, Japan	JN899304	JN899390
Penicillium crateriforme	CBS 184.27T = FRR 1057 = IMI 094165 = LSHB P164 = MUCL 29224 = NRRL 1057	Soil, Luisiana	JN680270	JN899373
Penicillium dendriticum	CBS 660.80T = IMI 216897	Leaf litter of Eucalyptus pauciflora, Kosciusko National Park, New South Wales, Australia	JN121714	JN899339
Penicillium diversum	CBS 320.48T = ATCC 10437 = DSM 2212 = IMI 040579 = IMI 040579ii = NRRL 2121	Leather, USA	JN680297	JN899341
Penicillium duclauxii	CBS 322.48T = ATCC 10439 = IMI 040044 = MUCL 28672 = MUCL 29094 = MUCL 29212 = NRRL 1030	Canvas, France	JN121643	JN899342
Penicillium echinosporum	CBS 293.62T = ATCC 18319 = DSM 2230 = FRR 3411 = IMI 080450 = IMI 101214	Wood pulp, Surrey, Kenley, UK		JN899363
Penicillium erythromellis	CBS 644.80T = FRR 1868 = IMI 216899	Soil from creek bank, Little River, New South Wales, Australia	JN680315	JN899383
Penicillium euglaucum	CBS 323.71NT	Soil, Argentina	JN121644
Penicillium expansum	CBS 325.48 = ATCC 7861 = IBT 5101 = IMI 039761= MUCL 29192 = NRRL 976	Fruit of Malus sylvestris, USA	JN121645
Penicillium fellutanum	CBS 229.81NT = ATCC 10443 = CBS 326.48 = FRR 746 = IFO 5761 = IMI 039734 = IMI 039734iii = NRRL 746	Unknown source, USA	JN121605
Penicillium funiculosum	CBS 272.86NT = IMI 193019	Lagenaria vulgaris, India	JN680288	JN899377
Penicillium glabrum	CBS 125543NT = IBT 22658 = IMI 91944	Unknown source	JN121717
Penicillium herquei	CBS 336.48T = ATCC 10118 = FRR 1040 = IMI 028809 = MUCL 29213 = NRRL 1040	Leaf, France	JN121647
Penicillium ilerdanum	CBS 168.81T = IJFM 5596 = IMI 253793	Air, Madrid, Spain		JN899311
Penicillium isariiforme	CBS 247.56T = ATCC 18425 = IMI 060371 = MUCL 31191 = MUCL 31323 = NRRL 2638	Woodland soil, Zaire	JN121616
Penicillium islandicum	CBS 338.48NT = ATCC 10127 = IMI 040042 = MUCL 31324 = NRRL 1036	Unknown source, Cape Town, South Africa	JN121648	JN899318
Penicillium janthinellum	CBS 340.48NT = ATCC 10455 = IMI 040238 = NRRL 2016	Soil, Nicaragua	JN131650
Penicillium javanicum	CBS 341.48T = ATCC 9099 = IMI 039733 = MUCL 29099 = NRRL 707	Root of Camellia sinensis, Indonesia, Java	JN121651
Penicillium kewense	CBS 344.61T = ATCC 18240 = IMI 086561 = MUCL 2685 = NRRL 3332	Culture contaminant of mineral oil CMI 1959; Kew, Surrey, UK	JN121654
Penicillium korosum	CBS 762.68T	Rhizosphere, India		JN899347
Penicillium lapidosum	CBS 343.48T = ATCC 10462 = IMI 039743 = NRRL 718	Canned blueberry, Washington, USA	JN121653
Penicillium liani	CBS 225.66T = ATCC 18325 = ATCC 18331 = IMI 098480 = NRRL 3380 = VKM F-301	Soil, China	JN680280	JN899395
Penicillium loliense	CBS 643.80T = ATCC 52252 = FRR 1798 = IMI 216901 = MUCL 31325	Lolium, Palmerston North, New Zealand	JN680314	JN899379
Penicillium marneffei	CBS 388.87T = ATCC 18224= CBS 334.59 = IMI 068794ii = IMI 068794iii	Rhizomys sinensis (bamboo rat), Vietnam	JN899298	JN899344
Penicillium minioluteum	CBS 642.68T = IMI 089377 = MUCL 28666	Unknown source	JN121709	JN899346
Penicillium mirabile	CBS 624.72T = CCRC 31665 = FRR 1959 = IMI 167383 = MUCL 31206	Forest soil, Crimea, Ukraine	JN680312	JN899322
Penicillium namylowskii	CBS 353.48T = ATCC 11127 = IMI 040033 = MUCL 29226 = NRRL 1070	Soil under Pinus sp., Puszceza Bialowieska, square “652”, Poland	JN121660
Penicillium oblatum	CBS 258.87T = FRR 2234	Spoiled baby food, Sydney, New South Wales, Australia	JN680285	JN899364
Penicillium ochrosalmoneum	CBS 489.66 = ATCC 18338 = IMI 116248ii	Cornmeal, South Africa	JN121689
Penicillium osmophilum	CBS 462.72T = IBT 14679	Agricultural soil, Wageningen, Netherlands	JN121683
Penicillium palmae	CBS 442.88T = IMI 343640	Seed, Wageningen, Netherlands	JN680308	JN899396
Penicillium panamense	CBS 128.89T = IMI 297546	Soil, Barro Colorado Island, Panama	JN899291	JN899362
Penicillium phialosporum	CBS 233.60T = ATCC 18481 = FRR 203 = IMI 078256	Milled Californian rice, California, USA	JN680282	JN899340
Penicillium piceum	CBS 361.48T = ATCC 10519 = IMI 040038 = NRRL 1051	Unknown source		JN899370
Penicillium pinophilum	CBS 631.66NT = ATCC 36839 = CECT 2809 = DSM 1944 = IAM 7013 =IMI 114933	PVC, Centre d'Études du Bouchet, M. Magnoux, France	JN680313	JN899382
Penicillium pittii	CBS 139.84T = IMI 327871	Clay soil, under poplar trees, bank of Duero River, Valladolid, Spain	JN680274	JN899325
Penicillium primulinum	CBS 321.48T = ATCC 10438 = CBS 439.88 = FRR 1074 = IMI 040031 = MUCL 31321 = MUCL 31330 = NRRL 1074	USA	JN680298	JN899317
Penicillium proteolyticum	CBS 303.67T = ATCC 18326 = NRRL 3378	Granite soil, Ukraine	JN680292	JN899387
Penicillium pseudostromaticum	CBS 470.70T = ATCC 18919 = FRR 2039	Feather, near Itasca State Park, Hubbard Co., Minnesota, USA	JN899300	JN899371
Penicillium purpurogenum	CBS 286.36T = IMI 091926	Unknown source	JN680271	JN899372
Penicillium purpurogenum var. rubisclerotium	CBS 274.95	Sculpture, castle Troja, Prague, Czech Republic	JN899295	JN899316
	CBS 270.35T = ATCC 4713 = ATCC 52244 = FRR 1064 = IBT 4302 = MUCL 29225 = NRRL 1064 = NRRL 1142	Zea mays, Castle Rock, Virginia, USA	JN680287	JN899381
Penicillium rademirici	CBS 140.84T = CECT 2771 = IMI 282406 = IMI 327870	Air under willow tree, bank of river Duero, Herrera, Valladolid, Spain		JN899386
Penicillium radicum	CBS 100489T = FRR 4718	Root of seedling of Triticum aestivum, Wagga Wagga, New South Wales, Australia		JN899324
Penicillium rotundum	CBS 369.48T = ATCC 10493 = IMI 040589 = NRRL 2107	Wood, Chiriqui Prov., Panama		JN899353
Penicillium rubicundum	CBS 342.59T = ATCC 13217 = IMI 099723 = NRRL 3400	Soil, Georgia, USA	JN680301	JN899384
“Penicillium rubrum”	CBS 196.88 = FRR1714	Unknown source	JN680278	JN899312
	CBS 206.89 = IFO 6580	Japan	JN680279	JN899313
	CBS 263.93	Bronchoalveolair lavage of immunecompetent female patient with pneumonia by Nocardia	JN680286	JN899315
Penicillium rugulosum	CBS 371.48T = ATCC 10128 = IMI 040041 = MUCL 31201 = NRRL 1045	Tuber (Solanum tuberosum), Connecticut, USA	JN680302	JN899374
Penicillium sabulosum	CBS 261.87T = FRR 2743	Spoiled pasteurized fruit juice, New South Wales, Sydney, Australia	JN899294
Penicillium samsonii	CBS 137.84T = CECT 2772 = IMI 282404 = IMI 327872	Fruit, damaged by insect, Valladolid, Spain	JN680273	JN899369
Penicillium shearii	CBS 290.48T = ATCC 10410 = IMI 039739 = IMI 039739iv = NRRL 715	Soil, Tela, Honduras	JN121631
Penicillium siamense	CBS 475.88T = IMI 323204	Forest soil, Lampang, Thurn District, Ban Daen Tham, Thailand		JN899385
Penicillium simplicissimum	CBS 372.48NT = ATCC 10495 = IMI 039816	Flannel bag, Cape, South Africa	JN121662
Penicillium stipitatum	CBS 375.48T = ATCC 10500 = NRRL 1006 = IMI 39805	Rotting wood, Louisiana, USA	JN680303	JN899348
Penicillium stolkiae	CBS 315.67T = IMI 136210 = ATCC 18546	Peaty forest soil, Eastern Transvaal, South-Africa	JN680295
Penicillium tardum	CBS 258.37T = NRRL 2116	Unknown source	JN899293
	CBS 378.48T = ATCC 10503 = IMI 040034 = NRRL 1073	Dead twig, France	JN899297
Penicillium tularense	CBS 430.69T = ATCC 22056 = IMI 148394	Soil, under Pinus ponderosa and Quercus kelloggii, Tulare Co., Pine Flat, California, USA	JN121681
Penicillium variabile	CBS 385.48NT = ATCC 10508= IMI 040040 = NRRL 1048	Cocos fibre, Johannesburg, South Africa	JN680304	JN899343
Penicillium varians	CBS 386.48T = ATCC 10509 = IMI 040586 = NRRL 2096	Cotton yarn, UK	JN680305	JN899368
Penicillium verruculosum	CBS 388.48NT = ATCC 10513= DSM 2263= IMI 040039 = NRRL 1050	Soil, Texas, USA		JN899367
Penicillium victoriae	CBS 274.36T = IMI 058412 = MUCL 9651	Dried leaf, Tobaheide, Sumatra	JN680289	JN899393
Penicillium viridicatum	CBS 390.48NT = ATCC 10515= IBT 23041 = IMI 039758 = IMI 039758ii = NRRL 963	Air, District of Columbia, Washington D.C., USA	JN121668
Phialosimplex caninus	CBS 128032T = UAMH 10337	Bone marrow aspirate ex canine, San Antonio, Texas, USA	JN121587
Phialosimplex chlamydosporus	CBS 109945T = FMR 7371 = IMI 387422	Disseminated infection in a dog	JN121566
Phialosimplex sclerotialis	CBS 366.77T = IAM 14794	Fodder of ray-grass and lucerne, France	JN121661
Rasamsonia eburnea	CBS 100538T = IBT 17519	Soil, Taipei, Taiwan	JN680325
Rasamsonia argillacea	CBS 101.69T = IMI 156096 = IBT 31199	Mine tip with a very high surface temperature; Staffordshire, UK	JN121556
Rasamsonia byssochlamydoides	CBS 413.71T = IBT 11604	Dry soil under Douglas fir, Oregon, USA	JN121675
Rasamsonia emersonii	CBS 393.64T = DTO 48I1 = IBT 21695 = ATCC 16479 = IMI 116815 = IMI 116815ii	Compost, Italy	JN121670
Sagenoma viride	CBS 114.72T ATCC 22467 = NRRL 5575	Soil, Australia	JN121571
Sagenomella bohemica	CBS 545.86T = CCF 2330 = IAM 14789	Peloids for balneological purposes, Frantiskovy Lázne Spa, West Bohemia, Czech Republic	JN121699	JN899400
Sagenomella diversispora	CBS 398.69	Forest soil under Populus tremuloides, Petawawa, Ontario, Canada	JN121673
	CBS 399.69 = MUCL 15012	Forest soil under Thuja occidentalis, Aberfoyle, Ontario, Canada	JN121674
Sagenomella griseoviridis	CBS 426.67T = ATCC 18505 = IMI 113160	Unknown source	JN121677
Sagenomella humicola	CBS 427.67T = ATCC 18506 = IMI 113166	Forest soil under Thuja occidentalis, Ontario, Canada	JN121678
Sagenomella striatispora	CBS 429.67T = ATCC 18510 = IMI 113163	Soil, Guelph, Ontario, Canada	JN121679
Sagenomella verticillata	CBS 415.78A	Gymnosperm forest soil, Sweden	JN680307
Sclerocleista ornata	CBS 124.53NT = ATCC 16921 = IMI 055295 = MUCL 15643 = NRRL 2256	Soil in oak forest, Dane Co., Madison, Wisconsin, USA	JN121581
Talaromyces assiutensis	CBS 118440	Soil, Fes, Morocco		JN899320
	CBS 147.78T	Soil, amended with crushed buffalo hoofs and incubated for 5 months at 35 oC, Egypt	JN680275	JN899323
Talaromyces austrocalifornicus	CBS 644.95T = IBT 17522	Soil, campus Univ. South California, Los Angelos, USA	JN680316	JN899357
Talaromyces bacillisporus	CBS 296.48T = ATCC 10126 = IMI 040045 = NRRL 1025	Begonia leaf, New York City, New York, USA	JN121634	JN899329
Talaromyces barcinensis	CBS 649.95T = IBT 17518	Soil, Barcelona, Spain	JN680318	JN899349
Talaromyces brevicompactus	CBS 102661T = AS 3.4676	Moulded vegetables, Prov. Sechuan, Wolong, China	JN680326
Talaromyces convolutus	CBS 100537T = IBT 14989	Soil, Kathmandu, Nepal	JN121553	JN899330
Talaromyces cyanescens	CBS 114900 = FMR 8388	Tortosa, Catalina, Spain		JN899391
Talaromyces derxii	CBS 412.89T = NHL 2981	Cultivated soil, Okayama Prefecture, Kurashiki City, Higashitomii, Japan	JN680306	JN899327
	CBS 413.89T = NHL 2982	Cultivated soil, Okayama Prefecture, Kurashiki City, Higashitomii, Japan	JN899299	JN899326
Talaromyces emodensis	CBS 100536T = IBT 14990	Soil, Kathmandu, Nepal	JN121552	JN899337
Talaromyces flavus	CBS 310.38NT = IMI 197477 = NRRL 2098	Unknown substrate, New Zealand	JN121639	JN899360
Talaromyces galapagensis	CBS 751.74T = IFO 31796	Shaded soil under Maytenus obovata, Isla Santa Cruz, Galapagos Islands, Ecuador	JN680321	JN899358
Talaromyces gossypii	CBS 645.80T = FRR 1966 = IMI 198365	Gossypium, India	JN680317	JN899334
Talaromyces helicus var. boninensis	CBS 650.95T = IBT 17516	Lawn soil, Kominato, Chichijima, Ogasawara-mura, Tokyo-to, Japan	JN680319	JN899356
Talaromyces helicus var. helicus	CBS 335.48T = ATCC 10451 = DSM 3705 = IMI 040593 = NRRL 2106	Soil, Sweden	JN680300	JN899359
Talaromyces helicus var. major	CBS 652.66T = IMI 100914	Swamp soil, near Attenborough, Nottingham, UK	JN680320	JN899335
Talaromyces indigoticus	CBS 100534T = IBT 17590	Soil, Nagasaki-ken, Minamikushiyama-mura, Japan	JN680323	JN899331
Talaromyces intermedius	CBS 152.65T = BDUN 267 = IFO 31752= IMI100874	Alluvial pasture and swamp soil, Attenborough, Nottingham, England	JN680276	JN899332
Talaromyces leycettanus	CBS 398.68T = ATCC 22469 = IMI 178525	Coal spoil tip soil, Leycett, Staffordshire, England, UK	JN121672
Talaromyces luteus	CBS 348.51NT = IMI 089305	Soil, UK	JN121656
Talaromyces macrosporus	CBS 317.63T = FRR 404 = IMI 197478	Apple juice, Stellenbosch, South Africa	JN680296	JN899333
Talaromyces mimosinus	CBS 659.80T = FRR 1875 = IMI 223991	Soil from creek bank, Nattai River, New South Wales, Australia	JN899302	JN899338
Talaromyces muroii	CBS 756.96T = PF 1153	Soil, Hualien County, Chingpu, Taiwan	JN680322	JN899351
Talaromyces ocotl	CBS 102855T	Heat-treated soil from forest of Pinus hartwegii, Veracruz, Mexico	JN680327
Talaromyces ohiensis	CBS 127.64T	Soil treated with cyanamide, Germany	JN680272	JN899355
Talaromyces purpureus	CBS 475.71T = ATCC 24069 = ATCC 52513 = FRR 1731 = IMI 181546	Soil, near Esterel, France	JN121687	JN899328
Talaromyces subinflatus	CBS 652.95T = IBT 17520	Copse soil, Hahajima, Ogasawara-mura, Tokyo-to, Japan	JN899301	JN899397
Talaromyces tardifaciens	CBS 250.94T	Unknown source	JN680283	JN599361
Talaromyces thermophilus	CBS 236.58T = ATCC 10518 = IMI 048593 = NRRL 2155	Parthenium argentatum, decaying plant; California, USA	JN121611
Talaromyces trachyspermus	CBS 373.48T = ATCC 10497 = IMI 040043 = NRRL 1028	Unknown source, USA	JN121664	JN899354
Talaromyces ucrainicus	CBS 162.67T = ATCC 22344 = FRR 3462	Unknown source	JN680277	JN899394
Talaromyces udagawae	CBS 579.72T = FRR 1727 = IMI 197482	Soil, Misugimura, Japan	JN680310	JN899350
Talaromyces unicus	CBS 100535T = CCRC 32703 = IBT 18385	Soil, Chiayi County, Funlu, Taiwan	JN680324	JN899336
Talaromyces wortmanii	CBS 391.48T = ATCC 10517 = IMI 040047 = NRRL 1017	Unknown source	JN121669	JN899352
Thermoascus aurantiacus	CBS 396.78	Sawdust, in lumber yard, Toronto, Ontario, Canada	JN121671
	CBS 891.70 = IMI 173037	Wood, Firenze, Italy	JN121719
Thermoascus crustaceus	CBS 181.67T = ATCC 16462 = IMI 126333	Parthenium argentatum, decaying plant; Salinas, California, USA	JN121591
Thermoascus thermophilus	CBS 528.71NT = IMI 123298 = NRRL 5208	Wood and bark of Pinus, Sweden	JN121697
Thermomyces lanuginosus	CBS 218.34 = MUCL 8338	Fruit shell of Theobroma cacao	JN121599
	CBS 224.63 = MUCL 8337	Mushroom compost; Gossau-Zürich Switzerland	JN121602
	CBS 288.54 = MUCL 8340	Stomach of bovine foetus, Netherlands	JN680291
Trichocoma paradoxa	CBS 103.73	Unknown source, Japan	JN121558
	CBS 247.57 = MUCL 39666 = IBT 31159	Unknown source, Hachijô, Japan	JN121617
	CBS 788.83	Rotting stump of cut down tree, Myojoji Temple near Hakui Noto Park, Ishikawa Pref., Japan	JN121718	JN899398
Warcupiella spinulosa	CBS 512.65NT = ATCC 16919 = IMI 075885 = NRRL 4376	Jungle soil, Berakas-Muara, Brunei	JN121692

Morphology and physiology

Cultures were grown for 7 d on Czapek agar, Czapek yeast autolysate agar (CYA), oatmeal agar (OA) and/or malt extract agar (MEA) plates at 25 °C or, if required, another temperature. Medium compositions follow Samson et al. (2010). Cultures were grown for up to 3 wk for ascomata production.

Extrolite analysis

Nearly all species described in the genera Penicillium sensu lato (including those formerly classified in Eupenicillium), Penicillium subgenus Biverticillium, Talaromyces, Aspergillus and its many associated teleomorphic genera, and Paecilomyces (including those formerly or still classified in the associated teleomorph genus Byssochlamys) were analysed qualitatively for their profiles of secondary metabolites as determined by HPLC with diode array detection. Many strains of each species were examined, whenever available, but in some cases only the ex-type culture was available. Cultures were inoculated on the media CYA, MEA (Blakeslee formula, using Difco malt extract), YES agar (Samson , Difco yeast extract) and OA. All cultures were analysed chemically using three agar plugs from a 7 d old culture grown at 25 °C (Smedsgaard 1997). Different methods were used for HPLC analysis, but the methods were essentially based on Frisvad & Thrane (1987, 1993). Since 1997, the method for Nielsen & Smedsgaard (2003) was used and after 2010 the UPLC method of Nielsen et al. (2011) was applied. Metabolites were identified via their diode-array based UV-VIS spectra and in some cases by their mass spectra, and by comparison to authenticated standards (Nielsen ).

For the extrolites analyses, the biosynthetic families of the sampled genera were compared using UPGMA cluster analysis (NTSYS version 2.11). All metabolites were classified according to biosynthetic families; for example the viridicatin biosynthetic family consists of cyclopenol, cyclopenin, cyclopeptin, dehydrocyclopeptin, viridicatin, viridicatol and 3-methoxyviridicatin (Turner & Aldridge 1983). This family was scored as one character in the cluster analysis. The exometabolites were also combined into biosynthetic families and tabulated as such. For example, many species of Talaromyces and Penicillium subgenus Biverticillium produce the azaphilones mitorubrin, mitorubrinal, mitorubrinol, mitorubrinol acetate, mitorubrinic acid, funicone, deoxyfunicone, actofunicone, 3-O-methylfunicone, kasanosin A and B, diazaphilonic acid, and wortmin; they are here collectively called the mitorubrins, while the related metabolites vermistatins and penicidones are called vermistatins (see Šturdíková , Nicoletti , Osmanova ). Some chlorinated azaphilones such as helicusins (Yoshida ) and luteusins (Fujimoto , Yoshida , b) are epimers of the sclerotiorins from P. sclerotiorum, and are treated as two families, albeit closely related to the mitorubrins.

DNA extraction, amplification and sequencing

Isolates used for molecular studies were grown on MEA for 7–14 d at the required temperature prior to DNA extraction. DNA was extracted from the cells using the UltraClean™ Microbial DNA Kit (MoBio Laboratories), following the protocols of the manufacturer. A part of the RPB1 gene was amplified to study the phylogenetic relationships among Penicillium and other related genera. This fragment was amplified using the primer pair RPB1-F1843 5'-ATTTYGAYGGTGAYGARATGAAC-3' and RPB1-R3096 5'-GRACRGTDCCRTCATAYTTRACC-3' (Houbraken & Samson 2011). Primer RPB1-F1843 corresponds with position 1490–1512 of GenBank no. XM_002146871 (P. marneffei, ATCC 18224) and RPB1-R3096 corresponds with position 2610–2633. An addition primer, RPB1-R2623 5'-GCRTTGTTSARATCCTTMARRCTC-3' was occasionally used as an internal primer for sequencing (Houbraken & Samson 2011). The ITS regions were sequenced to study the relationship among Talaromyces and the related biverticillate anamorphic species. Fragments containing the ITS region were amplified using primers V9G (de Hoog & Gerrits van den Ende 1998) and LS266 (Masclaux ). Sequencing reactions were performed with the Big Dye Terminator Cycle Sequencing Ready Reaction Kit v. 3.1 (Applied Biosystems) and carried out for both strands to ensure consistency of the consensus sequence.

Data analyses

For the DNA sequence analyses, alignments were performed using the software Muscle as implemented in the MEGA5 programme (Tamura ). The RAxML (randomised accelerated maximum likelihood) software (v. 7.2.8, Stamatakis ) was used for the Maximum Likelihood (ML) analysis. The robustness of trees in the ML analyses was evaluated by 100 bootstrap replications. The phylogram based on RPB1 sequences is rooted with Coccidioides immitis (strain RS; full genome strain), and Trichocoma paradoxa (CBS 788.83) is used as an outgroup in the ITS analysis.

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 ). 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 ). 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 ). 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).

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 545.86T), Paecilomyces aerugineus (CBS 350.66T), Geosmithia viridis (CBS 252.87T) and Sagenoma viride (CBS 114.72T). 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.

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 ).

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)

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 , Frisvad & Samson 2004, Houbraken ). 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 , Nicoletti , Osmanova ), 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 , 1996a, b). Austdiol was isolated from Aspergillus pseudoustus (Vleggaar , Samson ), but 7-epi-austdiol from a Talaromyces species (Liu ).

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 ), 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 , Cole & Kirksey 1973), but the strain was later reidentified as P. brasilianum (Frisvad 1989).

Penicillium isariiforme (Samson ) 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 ). 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.

Penicillium and Talaromyces species excluded from the revised Talaromyces genus

Figure 1 shows that a number of species described in the genus should be excluded from Talaromyces s. str. Phylogenetically, T. ocotl CBS 102855T belongs to Sagenomella, as also suggested using phenotypic characters (Heredia ). The anamorph of this species was not formally named, described only as Sagenomella sp., and thus the new combination Sagenomella ocotl is proposed in the taxonomy section below.

Our analysis confirms the distinctiveness of the recently described genus Rasamsonia erected for thermotolerant or thermophilic species with distinctly rough-walled conidiphore stipes, olive-brown conidia, and ascomata, if present, with a scanty hyphal covering. Talaromyces eburneus, T. emersonii, T. byssochlamydoides were assigned to this genus, together with the anamorphic species originally described as Geosmithia argillacea and G. cylindrospora (Houbraken 2011).

Talaromyces thermophilus is the only member of Talaromyces section Thermophila (Stolk & Samson 1972). LoBuglio et al. (1993) already noted that this species is the most divergent Talaromyces species, occupying a basal position to the major Talaromyces clade. Houbraken et al. (20112011) showed that this species is closely related to Thermomyces lanuginosus and our partial RPB1 sequence data confirm this relationship (Fig. 1). We did not examine type material of Talaromyces thermocitrinus (as ‘thermocitrinum’) and the conclusion of Mouchacca (2007), who tentatively placed this species in synonymy with T. thermophilus, is not followed here. Talaromyces luteus is further basal to T. thermophilus and Therm. lanuginosus and this species might represent a distinct genus. For the present, T. thermophilus and T. luteus will be retained in Talaromyces. More research is needed to confirm whether the assignment of these species to Thermomyces is warranted.

Udagawa & Suzuki (1994) described Talaromyces spectabilis with a Paecilomyces anamorph. Houbraken et al. (2008) transferred this species to Byssochlamys and showed that it is the teleomorph of Paec. variotii. In a single name system, Paec. variotii is the oldest genus and species name for this taxon, and thus the correct name for the holomorph.

Talaromyces brevicompactus, T. striatus (= Hamigera striata) and T. leycettanus are distant from Talaromyces s. str. and phylogenetically more closely related to Penicillium s. str. and Aspergillus. Figure 1 shows that H. striata and T. leycettanus are closely related. Further phylogenetic support for this relationship was presented in the studies of Ogawa & Sugiyama (2000) and Houbraken & Samson (2011). These two species are phylogenetically distant from Talaromyces s. str. and more closely related to Hamigera. Peterson et al. (2010) delimited Hamigera phylogenetically but stated that T. leycettanus and H. striata do not belong to this genus, and followed Benjamin's (1955) placement of H. striata in Talaromyces. In this study, we retain H. striata and T. leycettanus in Hamigera and Talaromyces, respectively. A thorough study on Hamigera and related genera is needed to clarify the correct placement of these species. Kong (1999) described Talaromyces brevicompactus, stating that this species is closely related to Hamigera avellanea (as Talaromyces avellaneus). The anamorph of this species was described in Merimbla, thus confirming the relationship with Hamigera. Sequence comparisons of this species showed that it is similar to NRRL 2108, a phylogenetically undescribed Hamigera species (J. Houbraken, unpubl. data, Peterson ). We wait with combining this species in Hamigera until a more data and strains become available.

Species described in other genera but phylogenetically within Talaromyces

Phylogenetic analysis shows that “Aphanoascus cinnabarinus”, Sagenomella bohemica, Paecilomyces aerugineus, Geosmithia viridis and Sagenoma viride belong to Talaromyces. The genus Sagenoma is typified with S. viride, and therefore this genus can be considered as a synonym of Talaromyces. Our data support the conclusions of von Arx (1987), who correctly transferred this species in Talaromyces, and this is reflected in the taxonomy section below.

Houbraken & Samson (2011) discussed the confusion over Aphanoascus cinnabarinus, which has persisted since the description of the genus Aphanoascus by Zukal (1890). Most authors follow Apinis (1968) and consider the genus Aphanoascus to be typified by A. fulvescens Zukal. In addition, the neotypification of A. cinnabarinus by Udagawa & Takada (1973) was incorrect, because their neotype strain had a Paecilomyces anamorph, whereas Zukal's original description and illustrations clearly showed a Chrysosporium-like anamorph (Stolk & Samson 1983). Based on morphological features, Stolk & Samson (1983) indicated that Chromocleista cinnabarina (as A. cinnabarinus sensu Udagawa & Takada) belongs to the Eurotiales and suggested that this species is intermediate between Thermoascus and Talaromyces. Our phylogenetic study, and that of Houbraken & Samson (2011), clarified that C. cinnabarina belongs to Talaromyces s. str. The taxonomic position of Chromocleista cinnabarina (as A. cinnabarinus sensu Udagawa & Takada) will be discussed in a forthcoming paper. Paecilomyces aerugineus was proposed by Samson (1974) for Spicaria silvatica Oudemans sensu Apinis. This species resembles the anamorph of A. cinnabarinus sensu Udagawa & Takada and a more detailed study is necessary to clarify this relationship.

TAXONOMY

Penicillium itself has a long list of generic synonyms (see Seifert ) 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 ).

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 ). 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.

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.

List of species

The following list includes previously accepted species of Talaromyces and proposals to transfer the species of Penicillium subgenus Biverticillium to Talaromyces.

Our phylogenetic studies demonstrate that several taxa represent complexes of morphologically cryptic phylogenetic species, requiring further study. For example, we analysed members of the Penicillium purpurogenum complex (including P. purpurogenum, P. rubrum, P. crateriforme, P. sanguineum) and found that several species group could be distinguished by sequencing certain genes (N. Yilmaz, unpubl. data) and had distinct macromorphological features and unique extrolite profiles. The full phylogenetic diversity of the P. purpurogenum species complex requires more investigation, and a more detailed account will be published elsewhere.

ACCEPTED SPECIES IN TALAROMYCES

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

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

(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.

(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.

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).

(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.

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

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

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

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

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

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

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

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

(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).

(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).

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

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

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

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

(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).

(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.

(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.

(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.

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

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

(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).

(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).

(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.

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

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

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

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

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

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

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

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

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

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

(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.

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

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

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

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

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

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

(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.

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

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

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

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

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

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

(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.

(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.

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

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

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

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

(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.

(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).

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

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

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

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

(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.

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, .

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, .

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, .

Talaromyces gossypii Pitt, The Genus Penicillium: 500. 1980

= Talaromyces assiutensis, Samson & Abdel-Fattah, Persoonia 9: 501. 1978 (fide Frisvad ).

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 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 ). 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 ). 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.