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Department of Biology, Clark University, 950 Main Street, Worcester, Massachusetts 01610
Peter R. Johnston
Herbarium PDD, Landcare Research, Private bag 92170, Auckland, New Zealand
Susumu Takamatsu
Faculty of Bioresources, Mie University, 1515, Kamihama, Tsu 514-8507, Japan
Joseph W. Spatafora
Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon 97331
David S. Hibbett
Department of Biology, Clark University, 950 Main Street, Worcester, Massachusetts 01610
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIAL AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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Phylogenetic relationships of one of the largest nonlichen-forming ascomycetous groups, the Leotiomycetes, were inferred from genes encoding three rDNA regions (SSU+LSU+5.8S rDNA). A dataset was prepared with rDNA sequences data from 108 isolates, among which we sampled 85 taxa representing four orders and 16 families in the Leotiomycetes. Equally weighted parsimony and Bayesian analyses were performed. Bootstrap proportion and Bayesian posterior probability under the GTR+
+I model were estimated along the branches. Based on our results the Leotiomycetes is relatively well defined as a class and it includes the Cyttariales, Erysiphales, Helotiales, Rhytismatales and two families of uncertain position, Myxotrichaceae and Pseudeurotiaceae. The placements of the Thelebolales and Ascocorticiaceae are not examined and are accepted as tentative in the Leotiomycetes. Our results agree with previous studies to remove the Geoglossaceae, including Geoglossum, Trichoglossum and Sarcoleotia, from the Leotiomycetes. Positions of the Erysiphales and Rhytismatales in the Leotiomycetes are confirmed. The Helotiales and Myxotrichaceae are paraphyletic. Close relationships are supported strongly among the Hemiphacidiaceae, Rutstroemiaceae and Sclerotiniaceae, among Loramycetaceae, the northern hemisphere Vibrisseaceae, the Dark Septate Endophyte fungus Phialocephala fortinii and Mollisia cinerea, and between species of Bulgaria and Phadidiopycnis. Sequence data of rDNA regions are not adequate to resolve the relationships among major groups of the Leotiomycetes.
Key words: Ascomycetes, Geoglossaceae, Pseudeurotiaceae
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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, Kirk et al 2001).
Morphologically the Leotiomycetes is a highly diverse group of the Pezizomycotina. The apothecia vary in their appearance. For example species of Cyttaria (Cyttariales) produce bright colored, globose fruiting bodies the size of ping-pong balls on hardwood trees, while apothecia of Lophodermium species (Rhytismatales) often mature as small, dark dots on conifer needles. In addition to appearance, the texture of the ascoma can range from highly gelatinous as in Bulgaria or hairy and fleshy to fragile as in members of the Hyaloscyphaceae. Among the Leotiomycetes the fruiting bodies of the Erysiphales and Thelebolales are exceptions, with tiny, closed ascomata with one to many asci. Their position in the Leotiomycetes is based mainly on molecular data. Most fungi in the Leotiomycetes produce asci with eight ascospores, but more than 2000 spores can be found in a single ascus of Thelebolus stercoreus (Thelebolales) (de Hoog et al 2005). The ultrastructure and histochemistry of asci and ascospores has been used in some groups in the class (e.g. Baral 1987, van Brummelen 1998, Verkley 1994) but lack of widespread use of these characters in many groups somewhat limits the broad utility of these techniques in taxonomic or phylogenetic studies.
Characters relating to the ecology and biology of the Leotiomycetes have potential taxonomic value. Some orders, such as the Erysiphales, Cyttariales, Thelebolales and Rhytismatales, are associated with distinct ecological characters and nutritional modes in addition to morphology almost unique for each group. Members of the Helotiales, one of the largest nonlichen-forming ascomycetous groups, thrive in various ecosystems and cover a broad range of niches, and helotialean fungi have been described as plant pathogens, endophytes, nematode-trapping fungi, mycorrhizae, ectomycorrhizal parasites, fungal parasites, terrestrial saprobes, aquatic saprobes, root symbionts and wood rot fungi (Wang et al 2006). Further complicating systematics of the Helotiales are the interconnections between anamorphs and teleomorphs. Many helotialean fungi are known only from a teleomorphic stage, and their anamorphs either are undiscovered or it is assumed that they have been lost in the process of evolution. On the other hand anamorphs in various environmental samples have been suggested as members of the Helotiales without any clear teleomorph connections (Raja and Shearer http://fm5web.life.uiuc.edu/fungi/).
Most evolutionary studies of the Leotiomycetes are based primarily on specimens from the temperate northern hemisphere, but many members within the Leotiomycetes are patchy in their broad geographic distribution. For example there is no evidence that Sclerotiniaceae sensu Holst-Jensen et al (1997) occur naturally in native ecosystems of Australasia and these fungi might have evolved primarily in the northern hemisphere. However other genera such as Cyttaria and Chlorovibrissea are restricted to the southern hemisphere. Some genera such as Chlorociboria appear to have an Asian/Australasian center of diversity (Johnston and Park 2005), while the basal lineages of the Erysiphales seem restricted to narrow areas of South America and Asia (Takamatsu et al 2005a, b). To properly represent the genetic diversity of the Leotiomycetes requires a broad geographic focus to phylogenetic studies.
The historical classifications of the Leotiomycetes orders and families are based primarily on morphological investigations (Dennis 1968, Kimbrough 1970, Korf 1973, Nannfeldt 1932, Pfister and Kimbrough 2001). In contrast molecular phylogenetic analysis of this group of fungi is comparatively young. Several studies have revealed polyphyletic assemblages of some orders and families in the class (Gernandt et al 2001, Lutzoni et al 2004), but none of these studies have focused at the class level with sampling from all major groups in the Leotiomycetes. The aims of this study are to (i) reconstruct the phylogeny of the Leotiomycetes based on the most inclusive rDNA dataset so far and (ii) briefly discuss phylogenetic relationships at the family level based on recognized clades in our tree and from previous studies.
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MATERIAL AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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, Goodwin 2002, Holst-Jensen et al 1997, Lumbsch et al 2005, Lutzoni et al 2004, Mori et al 2000, Rossman et al 2004, Wang et al 2002, 2005, 2006), were downloaded from GenBank and the AFTOL databases (SUPPLEMENTARY TABLE I). Eighty-five taxa were sampled for 16 of 21 families in the Leotiomycetes accepted by Kirk et al (2001) and Eriksson (2005). A lack of adequate data excluded from our analysis the Ascocorticiaceae and Phacidiaceae (Helotiales), the Cryptomycetaceae and Ascodichaenaceae (Rhytismatales) and the Thelebolales. Species belonging to the Dothideomycetes, Lecanoromycetes, Eurotiomycetes, Orbiliomycetes, Pezizomycetes and of two budding yeasts also were sampled to address outgroup diversity. Because Neolecta irregularis has been suggested having a basal position in the Ascomycota (Landvik et al 2001, Liu and Hall 2004) it was used to root the tree.
Phylogenetic analyses.— –
A nuc-rDNA dataset of 108 taxa was prepared, which includes 1995 characters with 602 parsimony informative positions after the ambiguous or unalignable positions in the LSU-rDNA region were excluded. Sequences were aligned by eye in the data editor of PAUP* 4.0b (Swofford 1999), and the dataset was analyzed in PAUP* 4.0b and MrBayes 3.1.1 (Huelsenbeck and Ronquist 2001) with gaps treated as missing data. Maximum parsimony analyses were based on heuristic searches of 1000 replicates of random sequence addition. MAXREES was set to auto-increase, and TBR branch swapping was employed. Bootstrap proportions (BP) were computed with a bootstrap analysis performed with 500 replicates, each with 20 random taxon addition sequences, MAXTREES was set to 1000, and TBR branch swapping was employed. Bayesian posterior probabilities were estimated with the metropolis-coupled Markov chain Monte Carlo method (MCMCMC) under the GTR++I model in MrBayes 3.1.1 by running four chains with 2 000 000 generations. Trees were sampled every 100 generations. Likelihoods converged to a stable value after 150 000 generations, and all trees before the convergence were discarded before computing a consensus tree in PAUP*. Bayesian posterior probabilities (PP) were obtained from the 50% majority rule consensus of the remaining trees. Clades receiving both BP 
70% and PP 95% were considered to be significantly supported (Lutzoni et al 2004). Alignments are available at TreeBASE (accession number sn2880).
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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Parsimony and Bayesian analyses.— –
One of the 338 equally parsimonious trees generated is shown and clades with BP 50% were marked under the branches (FIG. 1). Bayesian posterior probabilities (PP) were estimated from the 50% majority rule consensus of the 18 500 trees, and clades with PP 0.90 (90%) were marked above the branches (FIG. 1). The Leotiomycetes with the exclusion of the Geoglossaceae, including the Cyttariales, Erysiphales, Helotiales, Rhytismatales, Myxotrichaceae and Pseudeurotiaceae, was supported as a clade (BP = 61%, PP = 100%). The Erysiphales (BP = 63%, PP = 97%) and Rhytismatales (BP = 100%, PP = 100%) were supported as monophyletic groups. A notable exception of support (PP = 95%) of supraordinal relationships was the clade containing the Erysiphales, Cyttaria darwinii (Cyttariales) and two species of Chlorociboria (Helotiales). For the Erysiphales Parauncinula septata was supported as the most ancestral lineage with other Erysiphales as the sister group, which was composed of two clades. The one included a subclade of Podosphaera tridactyla and Sawadaea polyfida (BP = 100%, PP = 100%) with Blumeria graminis as the moderately supported sister group (BP = 69%, PP = 90%). The other clade (BP = 87%, PP = 100%) included two subclades that are without support. Leveillula taurica and Phyllactinia moricola were closely related (BP = 99%, PP = 100%). The Helotiales is not resolved as monophyletic, and strongly supported (BP > 70%, PP > 95%) terminal clades of two or more genera included the Leotia-Northern Hemisphere Microglossum clade (BP = 100%, PP = 100%), Bulgaria-Phacidiopycnis clade (BP = 98%, PP = 100%), Ciboria-Sclerotinia-Monilinia-Rutstroemia-Scleromitrula clade (BP = 95%, PP = 100%), Chlorencoelia-Hemiphacidium-Heyderia-Fabrella-Rhabdocline (teleomorph of Meria) clade (BP = 97%, PP = 100%), Dermea-Neofabraea clade (BP = 84%, PP = 100%), Cudoniella-Ombrophila clade (BP = 88%, PP = 100%), Phialocephala-northern hemisphere Vibrissea clade (BP = 71%, PP = 100%), Loramyces-Mollisia clade (BP = 99%, PP = 100%), Chlorovibrissea-Vibrissea albofusca clade (BP = 82%, PP = 100%) and Ascocoryne-Chloroscypha clade (BP = 95%, PP = 100%). The Loramyces-Mollisia clade was the sister group of the Phialocephala-northern hemisphere Vibrissea clade (BP = 98%, PP = 100%), and the Ciboria-Sclerotinia-Monilinia clade was grouped with species of Rutstroemia, Scleromitrula and Piceomphale (BP = 94%, PP = 100%), which was supported strongly (BP = 95%, PP = 100%) as the sister group of the Chlorencoelia-Hemiphacidium-Heyderia-Fabrella-Rhabdocline clade. The Rhytismatales formed a well supported clade (BP = 100%, PP = 100%) that included the Cudoniaceae and members of the Rhytismataceae (Coccomyces, Rhytisma and Lophodermium). The Myxotrichaceae was not monophyletic in our tree and consisted of two distinct lineages. One lineage included Byssoascus striatisporus and Myxotrichum deflexum (BP = 92%, PP = 100%). The second was represented by Pseudogymnoascus roseus, which was part of a larger clade that included Pseudeurotium zonatum (Pseudeurotiaceae), Leotia (Leotiaceae) and Microglossum (Geoglossaceae).
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), excluding the Geoglossaceae and including the Pseudeurotiaceae, is supported in this study as a monophyletic group. Here we accept the Leotiomycetes to include the Cyttariales, Erysiphales, Helotiales, Rhytismatales, Thelebolales, Myxotrichaceae and Pseudeurotiaceae. Two genera of the Geoglossaceae, Geoglossum and Trichoglossum, and genus Sarcoleotia of the Helotiaceae are removed from the class.
Cyttariales.— –
There is a single family, Cyttariaceae, with a single genus, Cyttaria, of about a dozen parasitic species on Nothofagus (southern beech) in the southern hemisphere. The fungus produces large and fleshy globose or pyriform stromata on galls on living branches. The stromata sometimes form spermatial pycnidia at early stages and later develop numerous separate, cup-shaped chambers containing asci and dark ascospores (Korf 1983, Pfister and Kimbrough 2001). Different authors have used morphological evidence to place the genus variously in the Pezizales and the Helotiales (see discussion in Gamundí 1991). Megoni (1986) showed that the asci have a thin cell wall and an apical amyloid ring, characters shared by some helotialean fungi. Our results placing the Cyttariales in the Leotiomycetes agree with the Landvik and Eriksson (1994) SSU-rDNA study, and Bayesian analyses strongly support (PP = 100%) a close relationship among species of Cyttaria and Chlorociboria (Helotiales) in a clade including species of the Erysiphales. Species of Chlorociboria produce small disk-shaped apothecia on dead wood, and their hyphae grow inside the wood and stain the substrate blue-green. Fifteen species, including 13 new species, were reported from New Zealand based on morphological characters and ITS sequence data, and a possible Asian/Australasian center of diversity for Chlorociboria was suggested (Johnston and Park 2005).
Erysiphales.— –
The Erysiphales with one family of 15 genera (Braun et al 2002, Takamatsu et al 2005a, b) are obligate plant pathogens that cause powdery mildew diseases on about 10 000 plant species (Amano 1986). There are no direct morphological features supporting inclusion of these fungi in the Leotiomycetes. The 16 sequences from the family group into a clade with 97% of posterior probability and 63% bootstrap values. Without exception all Erysiphales have closed, nonostiolate fruit bodies (chasmothecium, Braun et al 2002) with persistent asci and basal hymenium. These characters might further support monophyly of the Erysiphales, suggesting that the morphological characters as well as the holobiotrophy were acquired in the common ancestor of the Erysiphales.
Evolutionary relationships of the Erysiphales have been based on morphological characteristics and host plants for about 100 y. They are concerned with which characters are primitive and which derived, such as (i) numbers of asci in an ascoma, (ii) number of ascospores in an ascus, (iii) morphology of appendage, (iv) conidiogenesis (i.e. conidia produced in chains [Euoidium type] or solitary [Pseudoidium type]) and (v) ecto- or endoparasitism, ectotrophic or endotrophic. Of the 15 genera of the Erysiphales, 12 are ectoparasitic and only the remaining three genera, Leveillula, Phyllactinia and Pleochaeta, are endoparasitic. Arnaud (1921) and Katumoto (1973) regarded the endoparasitic genus Leveillula as primitive and all the ectoparasitic genera derivatives from it. On the other hand Raymond (1927), Blumer (1933) and Braun (1987) argued that the ectoparasitic habit of Leveillula was a xerophytic adaptation and not a primitive feature. The three endoparasitic genera form a monophyletic clade in this study, suggesting that the presence of internal mycelia is a synapomorphic character for these genera, which were derived from ectoparasitic genera by a single event. Morphology of ascomatal appendages has been important to define genera of the Erysiphales. Mori et al (2000) performed phylogenetic analyses of the Erysiphales based on the combined dataset of sequences from the same three rDNA regions as used here. They reported that the mycelioid appendage, which long has been regarded as a primitive character (e.g. Blumer 1933, Braun 1981, 1987), is a derived character of recent origin. They suggested that the development of mycelioid appendages convergently occurred many times in the respective lineages along with host expansion of the Erysiphales from trees to herbs. The basal position of Parauncinula septata on the present tree supports the report of Mori et al (2000) that the uncinate-circinate appendage is the most primitive in the Erysiphales.
A phylogeny covering all known tribes of the Erysiphales based on three rDNA regions by Takamatsu et al (2005a, b) suggested that Caespitotheca forestalis and the species of Parauncinula septata are basal in the order. Caespitotheca forestalis is restricted to South America, while P. septata is found only in eastern Asia.
Helotiales.— –
Although the backbone of our tree is not resolved, the current concept of the Helotiales (Eriksson 2005) almost certainly includes nonmono-phyletic taxa. Although the Helotiales has been receiving more attention recently (e.g. Gernandt et al 2001, Lutzoni et al 2004, Wang et al 2005). Even with exclusion of groups such as the Cyttariales, Erysiphales, Myxotrichaceae, Pseudeurotiaceae, Geoglossaceae and genetically widely divergent taxa such as Chlorociboria and Neobulgaria species, the monophyly of the Helotiales is not strongly supported by rDNA data and relationships among major helotialean clades are not well resolved. No taxon represents the Ascocorticiaceae or Phacidiaceae in our tree.
The family Bulgariaceae contains only two species, Bulgaria inquinans and B. nana, which produce brown-black to black, turbinate, highly gelatinous apothecia with brown-walled ascospores on bark of living hardwoods and might be weak plant pathogens (Döring and Triebel 1998). From our results B. inquinans shares a clade with a weak canker-causing pathogen, Phacidiopycnis pyri (teleomorph: Potebniamyces pyri), that produces small, black, gelatinous disks from stromata beneath bark. Potebniamyces has been doubtfully placed in the Rhytismatales by some authors (Eriksson 2005), with DiCosmo et al (1984) suggesting a possible relationship with either Phacidiaceae, Rhytismataceae or Dermateaceae. A LSU-rDNA sequence is available for one Phacidium lacerum from the AFTOL database, and analyses including the sequence suggests a sister relationship between Phacidiopycnis pyri and Phacidium lacerum. This calls into doubt the morphological differences between Potebniamyces and Phacidium discussed by DiCosmo et al (1984). Another black and slightly gelatinous fungus, Holwaya mucida, forms a sister group of the Bulgaria-Phacidiopycnis clade, although without support.
The Dermateaceae is a large, poorly studied, and heterogeneous family (Nauta and Spooner 1999, Pfister and Kimbrough 2001). Only four of the 77 genera placed in the family (Eriksson 2005) are sampled in this study. Species of Dermea and Neofabraea form a strongly supported clade, which we consider to represent the Dermateaceae sensu stricto. Previous studies using only the ITS region show that species of Pezicula and Ocellaria in the Dermateaceae also belong to this clade (Abeln et al 2000, de Jong et al 2001, Goodwin 2002, Verkley 1999). Species in this family produce erumpent or superficial, fleshy and small apothecia on plants, with an excipulum consisting of rounded or angular cells with dark walls. The hymenium frequently covered by a gelatinized "epithecium" and the thick walled ascospores found in several genera raise a hypothesis about their endophytic habits and the possible role of insect vectors (Wang et al unpubl). It is likely that the family will be restricted to endophytic species morphologically similar to Dermea and Pezicula. The other two genera sampled here traditionally placed in the Dermateaceae fall outside the Dermateaceae clade, Mollisia and Pilidium (teleomorph Discohainesia). Mollisia is a large, heterogeneous genus inadequately represented by the single species in our study. Crous et al (2003) discussed two phylogenetically distinct groups of Mollisia characterized in part by different anamorphs, while Pärtel and Raitviir (2005) described two different types of ascus ultra-structure among Mollisia species.
Concepts of the Geoglossaceae have changed many times recently (Eriksson 2005, Kirk et al 2001, Pfister and Kimbrough 2001, Platt 2000, Spooner 1987, Verkley 1994, Wang et al 2002, 2005). The separation of the Geoglossaceae from other helotialean fungi has been suggested, but an alternative systematic position of the family has not been proposed due to weak phylogenetic resolution (e.g. Platt 2000, Lutzoni et al 2004). Club-shaped apothecia, dark colored paraphyses and ascospores were considered as unique characters defining this group, and some authors have suggested that the hyaline-spored taxa be removed from the family (Platt 2000, Pfister and Kimbrough 2001). Species of Geoglossum and Trichoglossum form a basal branch within the inoperculate ascomycetes (Leotiomyceta) with the hyaline-spored Sarcoleotia species (Helotiaceae). Paraphyses (or homologous structures) cover the stipe surface in Geoglossum and Trichoglossum and obscure the boundary of the fertile hymenium (Spooner 1987). The pileate apothecia in Sarcoleotia globosa have a hymenium that is continuous with the stipe at an early stage and then recedes from the stipe (Schumacher and Sivertsen 1987). The genera, such as Cudonia, Spathularia, and helotialean Microglossum and Bryoglossum, differ in that the hymenium is always clearly demarcated from the stipe, even when no pileus is formed.
The family Helotiaceae is polyphyletic in our tree, and species of the family are found in eight clades. The first of these, the Cudoniella-Hymenoscyphus clade, although not strongly supported in our tree, could form the core of a monophyletic Helotiaceae sensu stricto, as suggested by Pfister and Kimbrough (2001). The genus Hymenoscyphus might include paraphyletic lineages recognized as ericoid mycorrhizal fungi and saprobes (Monreal et al 1999, Vrålstad et al 2002, Zhang and Zhuang 2004). The second clade of the Helotiaceae, Ascocoryne-Chloroscypha, receives strong support, and species of Neobulgaria also might group in this clade (Wang et al unpubl). Fungi in the Ascocoryne-Chloroscypha clade are characterized by a gelatinous apothecium and endophytic habits. The third clade is unsupported statistically and includes the aero-aquatic genera Mitrula, Hydrocina, Clathrosporium (anamorph) and the pathogenic Gremmeniella abietina. An accurate phylogeny here would provide insights into the evolution of the aquatic helotialean fungi. Two helotiaceous genera, Chlorencoelia and Heyderia, are nested within the Hemiphacidiaceae. We suggest removal of these genera from the Helotiaceae to the Hemiphacidiaceae (see notes below). The other genera in our analysis that traditionally have been included in Helotiaceae are Sarcoleotia (included here in the Geoglossaceae), Holwaya (forming an unsupported clade that includes Bulgaria), Chlorociboria (see discussion under Cyttariales) and Bisporella.
The families Hemiphacidiaceae, Rutstroemiaceae and Sclerotiniaceae, and Piceomphale bulgarioides, Heyderia abietis and Chlorencoelia versiformis form a clade with high support; a new order could be an appropriate classification for this clade. The Hemiphacidiaceae traditionally contains foliar pathogens producing small, simple apothecia beneath the leaf surface, the erumpent apothecia pushing back the covering host tissue (Korf 1962). In contrast species of Heyderia and Chlorencoelia produce large apothecia with a well developed excipulum. A PCR-based study shows that Heyderia species colonize conifer needles as endophytes and then produce apothecia on fallen leaves (Jean Bérubé pers comm). Chlorencoelia and Heyderia are examples of significant morphological changes associated with the shift in habits from obligate pathogen to endophyte/saprobe, also illustrated by the Cudoniaceae in the Rhytismatales. The Hemiphacidiaceae might need to be expanded to include such genera previously placed in the Helotiaceae. Except for the angiosperm-associated Chlorencoelia species, fungi of the expanded Hemiphacidiaceae are restricted to coniferous hosts. The Sclerotiniaceae and Rutstroemiaceae are among the best studied in the Helotiales (e.g. Dumont and Korf 1971, Holst-Jensen et al 1997, Kohn and Schumacher 1984, Novak and Kohn 1991, Schumacher and Holst-Jensen 1997, Spooner 1987, Zhuang 1998). Piceomphale bulgarioides, a spruce endophyte, is basal in this tree to the Sclerotiniaceae (sclerotial stromata producing) plus Rutstroemiaceae (substratal stromata producing) clade. A recent study of a chestnut pathogen Sclerotinia pseudotuberosa (= Ciboria batschiana) showed that the fungus could occur asymptomatically in different tissues of the host (Vettraino et al 2005). The ancestor of this "Sclerotiniales" clade was probably an endophyte living on conifers, with lineages in the Sclerotiniaceae and Rutstroemiaceae shifting from coniferous hosts to angiospermous hosts and becoming opportunistic pathogens. Lambertella tuberosa has been placed in the Rutstroemiaceae because of its pigmented ascospores. It has an aero-aquatic anamorph (Helicodendron tubulosum) and in this study it forms a clade with another aero-aquatic fungus, Spirosphaera floriformis, distinct from the Rutstroemiaceae. Only LSU-rDNA data were available for species of Lambertella and Spriosphaera for this study.
The Hyaloscyphaceae is poorly represented in this study, including only three of the more than 60 genera listed by Eriksson (2005). These fall in a poorly resolved part of our tree. Phylogenies from studies based on ITS sequences (Cantrell and Hanlin 1997, Abeln et al 2000, Vrålstad et al 2002) suggest the Hyaloscyphaceae subfamilies Lachnioideae and Hyaloscyphoideae are phylogenetically distinct, and Raitviir (2004) subsequently has treated these two taxa at the family level. The analysis in this paper supports removing Bryoglossum from the Geoglossaceae by Wang et al (2005), however the placement of Bryoglossum in the Hyaloscyphaceae require investigation with more inclusive taxa and gene sampling. Habits of fungi in this family are basically unknown. Many species have been recorded as host-restricted saprobes, often an indication of an endophytic stage in their life cycle.
The Leotiaceae is represented by Leotia lubrica and three species of Microglossum, and our results support studies (e.g. Landvik 1996, Liu and Hall 2004, Platt 2000) that suggest a close relationship between Leotia and Microglossum despite morphological differences. Both Leotia and Microglossum have worldwide distribution, but the southern and northern hemisphere species of Microglossum are genetically distinct in our tree. The Leotia-Microglossum clade is weakly supported as forming a clade with Pseudeurotium, a finding however that is supported by analyses of protein coding data (Spatafora et al this volume).
The Loramycetaceae, Mollisia cinerea, Phialocephala fortinii (anamorphic dark septate endophyte), and two northern hemisphere species of the Vibrisseaceae form a strongly supported clade. Ecological linkages among these fungi support molecular evidence of evolutionary relationships between aquatic fungi and root endophytes that has been observed also within aquatic hyphomycetes (e.g. Sati and Belwal 2005). The monotypic Loramycetaceae contains only two species that are aquatic and so adapted to the aquatic environment that they morphologically are hard to classify in other families in the Helotiales. Dark cells present at the base of Loramyces apothecium and the hyphal structure of the apothecia are analogous to those of the Dermateaceae (Digby and Goos 1987). Dark cells also can be found at the base of the apothecium of Vibrissea. Two southern hemisphere species of the Vibrisseaceae, Chlorovibrissea sp. and Vibrissea albofusca, are not included in this clade. The Vibrisseaceae is characterized by morphological features associated with an aquatic habit, and the origin of the southern hemisphere vibrisseaceous fungi could be independent from the northern hemisphere representatives. One Mollisia species is reported as aquatic (Fisher and Webster 1983).
Rhytismatales.— –
A complete rDNA dataset is available for only five of the 73 genera listed under the Rhytismatales by Eriksson (2005). Less complete datasets, or sequences from other genes, have been published for several other genera either currently placed in the Rhytismatales or that have been referred to the order in the past, including Colpoma, Cyclaneusma, Elytroderma, Lirula, Meloderma, Naemacyclus, Nematococcomyces, Phacidium, Rhabdocline, Rhytisma, Terriera, and Tryblidiopsis (Gernandt et al 1997, Gernandt et al 2001, Hou et al 2004, Ortiz-Garcia et al 2003).
Many of the taxa placed in the Rhytismatales are poorly understood, with both ordinal and familial relationships of several genera remaining tentative. For most species the teleomorph comprises an apothecium with a reduced excipulum that develops within a dark stroma, the stroma typically immersed within host tissue and sometimes covered by a clypeus (Johnston 2001). The hymenium becomes exposed after the covering host and fungal tissue splits by one or more elongate slits. The asci are typically thin-walled, undifferentiated at the apex, nonamyloid, the ascospores typically with gelatinous sheaths or appendages. The anamorphs are mostly Leptostroma-like, the spermatial conidia developing on often percurrently proliferating conidiogenous cells. Exceptions to this typical morphology include a few genera with ascospores lacking a gelatinous sheath or appendage (e.g. Discocainia [Reid and Funk 1966], Myriophacidium [Cannon and Minter 1986], Terriera [Johnston 2001] and Therrya [Reid and Cain 1961, Yuan and Mohammed 1997] within the Rhytismataceae, Ascodichaena [Hawksworth and Sherwood 1982] within the Ascodichaenaceae and Ocotomyces [Evans and Minter 1985] incertae sedis within the Rhytismatales). The phylogenetic significance of an ascospore sheath is not yet understood, although the position of Terriera within the Rhytismatales is supported by ITS sequences (Ortiz-Garcia et al 2003). Nothorhytisma is the only genus in the order with an amyloid pore at the apex (Minter et al 1998). The presence or absence of an amyloid ascus pore has been found to be of little phylogenetic significance at higher level in discomycetes (e.g. Rhabdocline, see Gernandt et al 1997) although the presence of such a pore in Phacidium was one of the factors leading DiCosmo et al (1984) to suggest this genus was more closely related to the helotialean fungi than it was to the Rhytismatales. The exclusion of Phacidium from the Rhytismatales has been supported by molecular data (Gernandt et al 1997). Cyclaneusma and Naemacyclus, included in the Rhytismatales on the basis of morphology (Kirk et al 2001) and the molecular analyses of Gernandt et al (1997, 2001), showed them to be phylogenetically distinct from the Rhytismatales.
Most genera of Rhytismatales form ascomata immersed within the host tissue, but Cudonia and Spathularia, recently added to the Rhytismatales on the basis of DNA data (Kirk et al 2001, Wang et al 2002), are different. In both genera ascomata develop on soil and form erect ascomata. The ascomata of Cudonia and Spathularia are macroscopically Helotiales-like, but careful anatomical studies have shown the hymenium covered by a stromatic layer at early stages of development (Landvik 1996, Wang et al 2002). Other Rhytismatales-like features of Cudonia and Spathularia are ascospores with gelatinous sheaths and simple asci lacking an amyloid pore (Wang et al 2002).
Available molecular data is insufficient to understand the morphological characteristics useful for defining the order Rhytismatales. Sequence data from genera such as Lophodermium, Meloderma and Elytroderma (Ortiz-Garcia et al 2003) suggest that generic limits within the order are artificial, but sampling intensity is too low to suggest yet what might be more appropriate generic or family limits.
Thelebolales.— –
A recent study of Thelebolus in Antarctica by de Hoog et al (2005) reveal the remarkable ecology and biology of these fungi. Species of Thelebolus produce small, globose to disk-shaped ascomata with sometimes polysporus asci, and the development of the ascomata varies from a cleistohymenial type to a eugymnohymenial type (van Brummelen 1967). The Thelebolaceae has been placed in the Pezizales (Eckblad 1968, Kimbrough and Korf 1967), and this placement has been studied from the apothecium macromorphology to ascus ultrastructure (e.g. Brummelen 1998). The placement of the Thelebolales in the Leotiomycetes is based on SSU-rDNA sequence data, and many of the order still have not been included in molecular phylogenetic studies (e.g. Gernandt et al 2001, Landvik et al 1998, Momol et al 1996). The order might not be monophyletic and its position in the Leotiomycetes should be regarded as a temporary treatment until sufficient proof becomes available.
Myxotrichaceae and Pseudeurotiaceae.— –
Myxotrichaceae and Pseudeurotiaceae are two families of cleistothecial ascomycetes, both of which contain genera linked to the Leotiomycetes in molecular studies (Sogonov et al 2005, Sugiyama et al 1999, Suh and Blackwell 1999). Three genera of the Myxotrichaceae are sampled in this study, and they resolve as two widely separated lineages; one includes Byssoascus striatisporus and Myxotrichum deflexum and the other includes Pseudogymnoascus roseus, along with Pseudeurotium zonatum from the Pseudeurotiaceae. The separation of Pseudogymnascus from Myxotrichum and Byssoascus supports earlier studies (Sugiyama et al 1999, Sugiyama and Mikawa 2001). The link between Pseudogymnascus and Pseudeurotium supports Sogonov et al (2005). The molecular-based phylogenies are supported by electron microscope studies, with the highly reduced cleistothecial ascomata of Myxotrichum showing a striking similarity in morphogenesis and gross morphology to typical helotialean fungi such as Hymenoscyphus species (Tsuneda and Currah 2004). Sequence data of Pseudogymnoascus and Pseudeurotium are limited, and our inclusion of Pseudeurotiaceae in the Leotiomycetes is tentative. However analysis of protein coding data of Pseudeurotium also supported its affinity to Leotia (Spatafora et al this volume), although Pseudogymnoascus was not included in those analyses.
Conclusion.— – The Leotiomycetes represents a morphologically and ecologically diverse class of Pezizomycotina whose evolutionary history is only beginning to be unraveled through phylogenetic analyses of molecular data. Significant advances have been made and include the classification of the Cudoniaceae in the Rhytismatales, the inclusion of the Erysiphales, Cyttariales and Pseudeurotiaceae in the Leotiomycetes, and the exclusion of Geoglossaceae from the Leotiomycetes. Current taxon and character sampling is insufficient to address many of the internal nodes of the class, and future phylogenetic studies must strive to significantly increase character sampling, especially that of protein-coding genes, from the diversity of species characterized as inoperculate discomycetes.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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1 Corresponding author. E-mail: zheng-wang{at}uiowa.edu. Current address: Roy J. Carver Center for Comparative Genomics, Department of Biological Sciences, University of Iowa, Iowa City, IA 52242-1324.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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