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Systematics of the Pezizomycetes—The Operculate Discomycetes

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Systematics of the Pezizomycetes—The Operculate Discomycetes Mycologia, 98(6), 2006, pp. 1029–1040. # 2006 by The Mycological Society of America, Lawrence, KS 66044-8897 Systematics of the Pezizomycetes—the operculate discomycetes K. Hansen1,2 Key words: classification, LSU rDNA, SSU rDNA, D.H. Pfister subordinal groupings Harvard University Herbaria, Cambridge, Massachusetts 02138 INTRODUCTION The Pezizales, the only order of the Pezizomycetes, is Abstract: The Pezizomycetes (order Pezizales) is an characterized by asci that generally open by rupturing early diverging lineage within the Pezizomycotina. A to form a terminal or eccentric lid or operculum. The shared derived character, the operculate ascus, ascomata are apothecia or are closed structures of supports the Pezizales as monophyletic, although various forms that are derived from apothecia. functional opercula have been lost in certain taxa. Apothecia range in size from less than a millimeter Phylogenetic relationships within Pezizales were to ca. 15 cm and may be sessile or stalked (FIG. 1). studied using parsimony and Bayesian analyses of The order includes epigeous, semihypogeous to partial SSU and LSU rDNA sequences from 100 taxa hypogeous (truffles) taxa. The ascospores are single- representing 82 genera and 13 of the 15 families celled, bipolar symmetrical, and usually bilaterally currently recognized. Three primary lineages are symmetrical, ranging from globose to ellipsoidal or identified that more or less correspond to the A, B occasionally fusoid. Some ascospores develop surface and C lineages resolved in previous analyses using ornamentations in the form of warts, ridges or spines. SSU rDNA: (A) Ascobolaceae and Pezizaceae; (B) The tissues of the ascomata are fleshy and often Discinaceae-Morchellaceae and Helvellaceae-Tubera- fragile. In a few cases ascomata are highly reduced or ceae; (C) Ascodesmidaceae, Glaziellaceae, Pyronema- lacking. Anamorphic states are reported from several taceae, Sarcoscyphaceae and Sarcosomataceae. In hyphomycetous form genera. The conidia are formed contrast the monotypic Rhizinaceae and Caloscypha- blastically; no phialidic states are known in the ceae are resolved as two independent lineages. Pezizales. The Pezizales are saprobic, mycorrhizal or Bayesian analyses support a relationship among plant parasitic; the biotic interactions of many taxa Rhizina and two species of Psilopezia (Pyronemata- are not known. Species are collected on soil, wood, ceae). Only lineage C is highly supported. The B and leaves and dung. Soil-inhabiting species often fruit in C lineages form a strongly supported monophyletic habitats with a high pH and low content of organic group. None of these lineages corresponds to earlier matter, including disturbed ground (for ecology see proposed suborders. The A and B lineages are Petersen 1985). The greatest diversity of species supported by certain morphological features (e.g. occurs in temperate regions or at high elevation. ascus bluing reaction in iodine, cytology of spores and Several members of the Sarcoscyphaceae and Sarco- paraphyses, septal pore structures and excipulum somataceae are common in tropical regions. The structure); these characters have been subject to order includes ca. 1125 described species (Kirk et al homoplasy. Lineage C is the largest and most 2001), classified in 15 families (Eriksson 2006). heterogeneous, and no unifying morphological fea- tures support its recognition. The Pyronemataceae, in Characters used in the classification.—The layering of which almost half of the species in the order are walls, structure of the apical apparatus and histo- found, is not monophyletic because the Ascodesmi- chemistry of the ascus, as observed with light and transmission electron microscopy (TEM), are used in daceae and Glaziellaceae are nested within it. The the classification of the Pezizales (summarized by relationships among all families in the C lineage Brummelen 1994). In Pezizaceae and Ascobolaceae, remain uncertain. The origin of various forms of the periascus (a mucilaginous extra-ascal layer) ascomata, including hypogeous forms (truffles and becomes blue in iodine solutions. In the Sarcoscy- truffle-like), epigeous cleistothecia, simple reduced phaceae, Sarcosomataceae and the Chorioactis clade apothecia and highly elaborate, stipitate forms (hel- the lateral walls of the asci are thick and have velloid and morchelloid), are discussed. particular layering as seen in TEM. In the Sarcoscy- phaceae the operculum is eccentric and thickened. Accepted for publication 21 November 2006. 1 Corresponding author. E-mail: [email protected] The interpretation of the structures in such asci has 2 Current address: The Swedish Museum of Natural History, Stock- been the subject of debate (Eckblad 1968, Samuelson holm, P.O. Box 50007 SE-10405 Sweden. 1975). Asci in most hypogeous and cleistothecial 1029 1030 MYCOLOGIA HANSEN AND PFISTER:PHYLOGENETICS IN PEZIZALES 1031 forms lack an operculum and spores are discharged with cleistothecia of other unrelated groups (e.g. passively. In some taxa (e.g. Carbomyces and Orbicula) Eurotiales). asci disintegrate and the spores form a powdery mass. Operculate asci are known outside Pezizales (Brum- The circumscription of the order.—In early treatments melen 1998, Kohlmeyer and Kohlmeyer 1979, Verkley both operculate and inoperculate taxa were included 1995) but these are structurally different in wall in the Pezizales (Bessey 1907, EA Bessey 1950, Seaver layering, and their similarity to the pezizalean 1928). The use of the Pezizales in the restricted sense operculum seems to be a case of convergence. of the operculate discomycetes can be traced to Additional features employed in classification are Nannfeldt (1932). Eckblad (1968), Rifai (1968), arrangement of hyphae in the sterile tissues of the Kimbrough (1970), Korf (1972), Brummelen apothecium, presence of hairs and/or tomentum, (1994), Landvik et al (1997) and Pfister and spore shape, ornamentation, presence or absence of Kimbrough (2001) reviewed the order and its oil guttules and hymenial pigmentation (Boudier evolving classification. While not always recovered as 1907, Nannfeldt 1932, 1949, Eckblad 1968, Korf 1972, a monophyletic group, the five-gene molecular 1973). The number of nuclei (uni- or multinucleate) phylogenetic study of the Pezizomycotina in this in ascospores and paraphyses (Berthet 1964) has been volume (Spatafora et al) resolves the Pezizales as used to assign taxa to families. Presence, absence and monophyletic, although only with weak support. types of carotenoid pigments were studied by Arpin The circumscription of the Pezizales has been (1969) and used as a basis of a classification he shaped by inclusion and exclusion of taxa. On the presented. Ultrastructural characters of septal pore one hand, the Pezizales was expanded considerably plugs and Woronin bodies correlate to some degree when (Trappe 1979) abandoned the order Tuberales with families and lineages in the order (Kimbrough and transferred most hypogeous genera to families of 1994). the Pezizales. Since then the hypothesis that the ascomycete truffles evolved independently within Variation in apothecial form.—Although formation of different evolutionary lineages of Pezizales has been an apothecial ascomata is normally the rule in confirmed and refined by ascus septal ultrastructure, members of the Pezizales, in some cases the ascomata number of nuclei in spores and molecular phyloge- develop cleistothecium- and perithecium-like netics (summarized by Læssøe and Hansen in review). morphologies (Corner 1931, Do¨bbeler 2004, Hansen On the other hand, Thelebolus and related genera et al 2005b). In other cases there is a reduction or loss (Thelebolaceae) were excluded from the Pezizales of sterile tissues entirely. Brummelen (1967) de- based on ascoma development and ascus structure scribed the developmental patterns in the genera (e.g. Samuelson and Kimbrough 1978) and molecular Ascobolus and Saccobolus, and this system has been phylogenetic studies (Landvik et al 1998). These taxa adopted widely across the order. Development may be now are considered as allied with the Leotiomycetes. cleistohymenial or gymnohymenial. Cleistohymenial Nevertheless, Thelebolaceae show a wide range of ascomata never open or may open at different stages ascus dehiscence mechanisms (operculate, bilabiate in development of the hymenial layers. Thus, hyme- or inoperculate; Brummelen 1998) and some taxa still nia of cleistohymenial types may be exposed early in might belong to the Pezizales. development of the ascoma, before asci are formed or mature, or opening of the ascoma may occur only at Subordinal classifications.—Chadefaud (1946) and Le the final stages when asci are fully mature. Cleistohy- Gal (1946a, b) introduced the idea that there are two menial types that remain closed might be confused types of operculate asci: thin-walled asci with terminal r FIG. 1. Examples of ascoma types and habits in the Pezizales. a–b. Pezizaceae and Ascobolaceae (lineage A). a. Peziza succosa apothecia exuding yellow milk where cut, on disturbed soil (KH-98-34, C). b. Saccobolus sp. apothecia with protruding asci, dark colored by purplish spores, on dung (JHP-96.006). c–d. Discinaceae-Morchellaceae (lineage B). c. Gyromitra californica (KH-97-26, FH). d. Morchella esculenta. e. Rhizinaceae: Rhizina undulata (TL-5357, C). f. Psilopezia juruensis (T. Læssøe, AAU 59604, C). g. Caloscyphaceae: Caloscypha fulgens, insert shows the green color of the apothecia when brushed (KH-97-17, FH). h.–o. Pyronemataceae-Ascodesmidaceae-Sarcosomataceae-Sarcoscyphaceae
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