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Eurotiomycetes: Eurotiomycetidae and Chaetothyriomycetidae

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Eurotiomycetes: Eurotiomycetidae and Chaetothyriomycetidae Mycologia, 98(6), 2006, pp. 1053–1064. # 2006 by The Mycological Society of America, Lawrence, KS 66044-8897 Eurotiomycetes: Eurotiomycetidae and Chaetothyriomycetidae David M. Geiser1 phylogenetically associated with this group. The Department of Plant Pathology, Pennsylvania State recently proposed order Mycocaliciales shows a sister University, University Park, Pennsylvania 16802 relationship with Eurotiomycetes. The great majority Ce´cile Gueidan of human pathogenic Pezizomycotina are Eurotiomy- Jolanta Miadlikowska cetes, particularly in Eurotiales, Onygenales and Franc¸ois Lutzoni Chaetothyriales. Due to their broad importance in Frank Kauff basic research, industry and public health, several Vale´rie Hofstetter genome projects have focused on species in Onyge- Emily Fraker nales and Eurotiales. Department of Biology, Duke University, Durham, Key words: Cleistothecium, industrial fungi, North Carolina, 27708 medically important fungi Conrad L. Schoch Department of Botany and Plant Pathology, Oregon INTRODUCTION State University, Corvallis, Oregon, 93133 Molecular data have been crucial in defining the class Leif Tibell Eurotiomycetes, which is now known to comprise Department of Systematic Botany, Uppsala University, a morphologically and ecologically disparate set of Norbyva¨gen 18 D, Uppsala, Sweden fungi. Early phylogenetic analyses of the Ascomycota Wendy A. Untereiner based on nuclear small ribosomal subunit sequences Department of Botany, Brandon University, Brandon, revealed a common ancestry between Capronia Manitoba, Canada R7A 6A9 pilosella (Chaetothyriales), with bitunicate asci and ascolocular development, and the fungi then recog- Andre´ Aptroot nized as the monophyletic Plectomycetes (Geiser and ABL Herbarium, G. v.d. Veenstraat 107, NL-3762 XK Soest, The Netherlands LoBuglio 2001) and as Eurotiomycetes by Eriksson (1999) (Berbee 1996, Spatafora et al 1995), which generally produce prototunicate asci in enclosed Abstract: The class Eurotiomycetes (Ascomycota, ascomata. This link led Berbee (1996) to propose Pezizomycotina) is a monophyletic group comprising that the Eurotiomycetes evolved by loss of the two major clades of very different ascomycetous fungi: bitunicate ascus and its corresponding mode of (i) the subclass Eurotiomycetidae, a clade that forcible discharge. The possibility of the cleistothe- contains most of the fungi previously recognized as cium evolving by means of paedomorphosis or Plectomycetes because of their mostly enclosed ‘‘arrested development’’ was proposed by Eriksson ascomata and prototunicate asci; and (ii) the subclass (1982). Later phylogenetic analyses further supported Chaetothyriomycetidae, a group of fungi that pro- a connection between the Chaetothyriales and the duce ascomata with an opening reminiscent of those prototunicate Eurotiomycetes (Liu et al 1999, produced by Dothideomycetes or Sordariomycetes. In Lumbsch et al 2000, Silva-Hanlin and Hanlin 1999, this paper we use phylogenetic analyses based on data Winka et al 1998). Based on the distinctiveness of available from the Assembling the Fungal Tree of Life Chaetothyriales, Chaetothyriomycetes (Eriksson and project (AFTOL), in addition to sequences in Winka 1997) and Chaetothyriomycetidae (Kirk et al GenBank, to outline this important group of fungi. 2001) were proposed as supraordinal taxa. The Eurotiomycetidae include producers of toxic and Despite the generally low node support in some useful secondary metabolites, fermentation agents previous studies of the Eurotiomycetes comprising used to make food products and enzymes, xerophiles both Eurotiomycetidae and Chaetothyriomycetidae and psychrophiles, and the important genetics model (Liu and Hall 2004, Lutzoni et al 2001, Reeb et al Aspergillus nidulans. The Chaetothyriomycetidae in- 2004), the result appears to be supported by multiple clude the common black yeast fungi, some of which datasets involving multiple genes and taxon sets are pathogens of humans and animals, as well as some (Lutzoni et al 2004). As shown in this volume, primarily lichenized groups newly found to be weighted parsimony analysis of sequences from five gene regions yielded 89% bootstrap support and Accepted for publication 29 November 2006. Bayesian analysis yielded 100% posterior probability 1 Corresponding author. E-mail: [email protected] for the common ancestry of the subclasses (Spatafora 1053 1054 MYCOLOGIA et al 2006). Furthermore this analysis placed Coryne- sequences showed Ascosphaera and Eremascus to form liales in a basal position within a strongly supported a clade distinct from Onygenales (Berbee and Taylor Eurotiomycetidae clade, indicating that members of 1992), leading Geiser and LoBuglio (2001) to infer this clade evolved from fissitunicate/ascolocular Ascosphaerales as a distinct order. (Lutzoni et al ancestors (Schoch et al 2006, Spatafora et al 2006). 2004) added further evidence in support of Asco- sphaerales based on SSU and nuclear ribosomal large Changing concepts of class Eurotiomycetes.—Nannfeldt subunit RNA gene (LSU) sequences, showing Asco- (1932) played a key role in integrating ontogenetic sphaera apis, Eremascus albus and Paracoccidioides features into ascomycete taxonomy, creating three brasiliensis to form a strongly supported clade. major groups based on ascomal development. One of these groups, Plectascales, was defined based on the Newly included orders.—The subclass Chaetothyrio- production of naked asci and antheridia. In this mycetidae first was proposed to accommodate the group enclosed cleistothecial ascomata form after order Chaetothyriales (Kirk et al 2001). The order ascogenous hyphae are enveloped in sterile mycelia. Verrucariales subsequently was shown to be sister to This group included all fungi with globose ascomata Chaetothyriales (Lutzoni et al 2001) and was added to and irregularly disposed evanescent asci. this subclass (Eriksson 2001). Recent molecular Eurotiomycetidae is a monophyletic group encom- studies also placed the order Pyrenulales in this passing a wide variety of morphologies, which group (reviewed in Lutzoni et al 2004). Members of includes many traditionally defined plectomycete-like these three orders all are characterized by perithecial fungi. Based on phylogenetic analyses of the nuclear ascomata and bitunicate asci with a dehiscence ribosomal small subunit RNA gene (SSU), Eriksson ranging from fissitunicate to evanescent. Historically (1999) proposed the class Eurotiomycetes for the classifications of ascomycetes treated either liche- clade comprising most fungi known morphologically nized or nonlichenized taxa, but rarely both, because as ‘‘Plectomycetes’’ and outlined as ‘‘the mono- they were recognized as two different groups (Achar- phyletic Plectomycetes’’ by Geiser and LoBuglio ius 1810, Lindau 1897, Zahlbruckner 1926). It was (2001). Although some concepts have included only in the 20th century that these classifications were perithecial taxa (Benny and Kimbrough 1980, Luttrell merged (Luttrell 1951, 1955; Nannfeldt 1932), and 1951) ‘‘Plectomycetes’’ generally refers to fungi with indeed the Chaetothyriomycetidae stands as the these morphological characters: (i) thin-walled, glo- prime example of the need for such a combined bose to pyriform, prototunicate asci (i.e. asci with system. The family Pyrenulaceae, together with walls that break down at maturity to release the species from the Verrucariaceae, then were in- ascospores within the ascoma in a passive fashion, cluded in the order Xylariales based on their ascus rather than forcible discharge through an apical type and centrum, identified as Xylaria-type (Lut- pore); (ii) ascomata without a distinct hymenial layer trell 1951, 1955). In the same classification the and with asci forming scattered within the ascomatal family Herpotrichiellaceae was assigned to Pleospo- cavity; (iii) unicellular ascospores; (iv) ascomata rales based on its centrum development (Luttrell varying from gymnothecial to cleistothecial, lacking 1951, 1955). an ostiolar opening and with highly variable cleis- Eriksson’s (1982) system divided what is now tothecial peridia, that may or may not be produced recognized as the Pezizomycotina into four groups within a stromatal structure; and (v) highly variable according to ascus type; the new orders Pyrenulales phialoblastic and thallic hyphomycetous anamorphs and Verrucariales were placed in the bitunicate (Alexopoulos et al 1996, Geiser and LoBuglio 2001). group. The existing families Chaetothyriaceae and Both Eriksson (1999) and Geiser and LoBuglio Herpotrichiellaceae were included in the bitunicate (2001) recognized similar fungi as making up this order Dothideales (Eriksson 1982). Barr was one of clade. Eriksson organized them into two major the first authors to consider the three orders orders. Eurotiales contained families Elaphomyce- Verrucariales, Chaetothyriales and Pyrenulales (at taceae, Monascaceae and Trichocomaceae and that time included in the Melanommatales) as closely Onygenales comprised Arthrodermataceae, Asco- related, based on ascus type (bitunicate or secondarily sphaeraceae, Eremascaceae, Gymnoascaceae and prototunicate) and hamathecium structure (insertion Onygenaceae. Based on SSU sequences Gibas et al of sterile filaments in the centrum, either pseudopar- (2002) defined the new order Arachnomycetales to aphyses or periphysoids) (Barr 1983). Molecular accommodate fungi in the genus Arachnomyces. This studies confirmed the close phylogenetic relation- genus previously had been placed within Onygenales ships
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