2 pezizomycotina: pezizomycetes, orbiliomycetes

2 Pezizomycotina: Pezizomycetes, Orbiliomycetes

DONALD H. PFISTER1

CONTENTS

I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35II. Orbiliomycetes: An Overview . . . . . . . . . . . . . . 37III. Occurrence and Distribution . . . . . . . . . . . . . . 37

A. Species Trapping Nematodesand Other Invertebrates . . . . . . . . . . . . . . . . . 38

B. Saprobic Species . . . . . . . . . . . . . . . . . . . . . . . . . 38IV. Morphological Features . . . . . . . . . . . . . . . . . . . . 38

A. Ascomata . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38B. Asci . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39C. Ascospores . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39D. Paraphyses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39E. Septal Structures . . . . . . . . . . . . . . . . . . . . . . . . . 40F. Nuclear Division . . . . . . . . . . . . . . . . . . . . . . . . . 40G. Anamorphic States . . . . . . . . . . . . . . . . . . . . . . 40

V. Reproduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41VI. History of Classification and Current

Hypotheses. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41VII. Growth in Culture . . . . . . . . . . . . . . . . . . . . . . . . . . 41VIII. Pezizomycetes: An Overview. . . . . . . . . . . . . . . 41IX. Occurrence and Distribution . . . . . . . . . . . . . . 41

A. Parasitic Species . . . . . . . . . . . . . . . . . . . . . . . . . 42B. Mycorrhizal Species . . . . . . . . . . . . . . . . . . . . . 42C. Saprobic Species . . . . . . . . . . . . . . . . . . . . . . . . . 42

X. Morphological Features . . . . . . . . . . . . . . . . . . . . 42A. Ascomata . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 42B. Asci . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43C. Ascospores . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43D. Paraphyses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43E. Septal Structures . . . . . . . . . . . . . . . . . . . . . . . . . 44F. Anamorphic States. . . . . . . . . . . . . . . . . . . . . . . 44

XI. Reproduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44XII. History of Classification and Current

Hypotheses. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44A. Families of the Pezizomycetes . . . . . . . . . . 46

1. Ascobolaceae . . . . . . . . . . . . . . . . . . . . . . . . . . 462. Ascodesmidiaceae. . . . . . . . . . . . . . . . . . . . . 463. Caloscyphaceae. . . . . . . . . . . . . . . . . . . . . . . . 464. Chorioactidaceae . . . . . . . . . . . . . . . . . . . . . . 46

5. Discinaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . 476. Glaziellaceae. . . . . . . . . . . . . . . . . . . . . . . . . . . 477. Helvellaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . 478. Karstenellaceae . . . . . . . . . . . . . . . . . . . . . . . . 479. Morchellaceae . . . . . . . . . . . . . . . . . . . . . . . . . 4710. Pezizaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4811. Pyronemataceae. . . . . . . . . . . . . . . . . . . . . . 4812. Rhizinaceae . . . . . . . . . . . . . . . . . . . . . . . . . . 4913. Sarcoscyphaceae . . . . . . . . . . . . . . . . . . . . . 4914. Sarcosomataceae . . . . . . . . . . . . . . . . . . . . . 4915. Tuberaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . 49

XIII. Growth in Culture . . . . . . . . . . . . . . . . . . . . . . . . . . 50XIV. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 50

References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 50

I. Introduction

Members of two classes, Orbiliomycetes andPezizomycetes, of Pezizomycotina are consis-tently shown in molecular phylogenetic studiesto diverge at the base of the Pezizomycotinaphylogeny (Gernandt et al. 2001; Hansen andPfister 2006; Spatafora et al. 2006). Kumar et al.(2012) give ultrastructural data on the septalstructure, ascus wall construction, and nucleardivision that suggest the Orbiliomycetes repre-sent the earliest diverging lineage of the Pezi-zomycotina. The relationship of these twoclasses and the family diversity within the Pezi-zomycetes are shown in Fig. 2.1. These twogroups show very few shared characteristicsother than the formation, for the most part, ofwell-developed apothecial ascomata in whichasci are generally arranged in a hymeniumwith paraphyses. Orbiliomycetes was recog-nized as a class only recently (Baral 2003).There is a single order, Orbiliales, and a singlefamily, Orbiliaceae, with perhaps 300 speciescurrently arranged in three teleomorphic

1Farlow Herbarium and Library of Cryptogamic Botany,

Department of Organismic and EvolutionaryBiology, Harvard University, Cambridge, MA, 02138, USA;

e-mail: [email protected]

Systematics and Evolution, 2nd EditionThe Mycota VII Part BD.J. McLaughlin and J.W. Spatafora (Eds.)© Springer-Verlag Berlin Heidelberg 2015

mailto:[email protected]

Fig. 2.1 A diagrammatic representation of the relation-ships of the Pezizomycetes and Orbiliomycetes, includ-ing the families of the Pezizomycetes, based on Hansenet al. (2013) and Pfister et al. (2013). Branches that

received maximum parsimony, posterior probability,and maximum-likelihood support �75 %, 95 %, and75 %, respectively, are in bold

36 D.H. Pfister

genera. An early diverging position of the classhas been confirmed by morphological studiesand molecular phylogenetic analyses (Kumaret al. 2012; Spatafora 2006; Wang et al. 2006).Previously, the Orbiliaceae was placed amongthe Helotiales as a family based on Nannfelt’s(1932) classic work on the nonlichenized inop-erculate discomycetes. The Pezizomyceteshave long been recognized to include a singleorder, the Pezizales, and include 16 familiesand approximately 1,200 species. The group,in whole or in part, has been the subject ofrecent surveys (Hansen and Pfister 2006; Har-rington et al. 1999; Perry et al. 2007; Pfisteret al. 2008).

In regard to morphological characteristicsand ecology, the two classes also are distinct.The Orbiliomycetes are saprobic and in somecases supplement their nutrition through thecapture and consumption of small inverte-brates. Their spores are small, nonseptate(save for a single example), uninucleate, andcontain a membrane-bound structure, thespore body (Baral 1994; Benny et al. 1978;Kumar et al. 2012). Spores are dischargedactively. Asci are small and generally lack awell-developed apical apparatus. Anamorphicstates are frequently formed, and their numberhas increased steadily in the literature in recentyears. Species are found on dung, on wet woodon the forest floor, in water-soaked areas wherethey are somewhat ephemeral, or on dead woodhanging in trees where, because of theirdrought resistance, they are persistent (Baral2011). No species are plant parasitic.

The Pezizomycetes are saprobic, plant par-asitic, or associated with plants as ectotrophicmycorrhizae (Hansen and Pfister 2006; Teder-soo et al. 2006; Wei et al. 2010). The ascomataare always to some degree ephemeral. Sporesare large, generally more than 10 mm and mayreach a length of 60 mm, and single-celled.Spores generally are actively dischargedthrough a well-developed opening created bythe rupture of the ascus wall forming an oper-culum that is either terminal or eccentric inposition. The trufflelike habit has developedindependently in several lineages across theclass (Læssøe and Hansen 2007). These hypo-geous taxa generally do not have active sporerelease.

In this chapter, the two classes are treatedindependently in separate sections.

II. Orbiliomycetes: An Overview

The family Orbiliaceae was proposed by Nann-feldt (1932) and was restricted to those fungiwith small so-called inoperculate asci, minuteascospores, and a waxy texture. The asci andparaphyses are often agglutinated. Nannfeldtillustrated several species showing details ofthe thin-walled globose to angular cells of theexcipulum. A monograph on the genus Orbiliaby Svrcek (1954) included 16 species that weredistinguished based on ascospore size andshape, the color of the ascomata, and the formof the paraphyses. The groundbreaking work ofHans-Otto Baral and his collaborator, Guy Mar-son, has led to a refinement of the family andrecognition of many more species. Kirk et al.(2008) proposed 288 species, but the extent ofthe diversity to be described is in flux. A mono-graph has been in preparation by Baral formany years. Modern methods employ morpho-logical and histochemical characters previouslynot used and incorporate ecological charactersas well. Of particular note is the reliance onfresh, living material (Baral 1992). There hasbeen a burst of activity focusing on the descrip-tion of teleomorphic taxa and associated ana-morphs (e.g., Kohlmeyer et al. 1998; Liu et al.2005a, b, 2006; Mo et al. 2005; Pfister 1994;Pfister and Liftik 1995; Qiao et al. 2011; Qinet al. 2010; Su et al. 2011; Tanabe et al. 1999;Webster et al. 1998; Wu et al. 2007; Yang andLiu 2005; Yu et al. 2007a, b, c, 2011; Zhang et al.2007), and in this work there has been anintense interest in the diversity and functionalmorphology of the anamorphic states. This isparticularly the case regarding those thatcapture nematodes, i.e., species referred toArthrobotrys and allied form genera.

III. Occurrence and Distribution

Members of the Orbiliomycetes are foundaround the world in boreal to tropical habitats.Furthermore, several species complexes, such

Pezizomycotina: Pezizomycetes Orbiliomycetes 37

as O. luteorubella and O. xanthostigma, thatrepresent morphologically very similar collec-tions seem to be found broadly distributedaround the world and across latitudes. Thereare two major ecological groups—those thatoccur in moist habitats such as on dung, oldpolypores, and moist wood on the forest flooror near streams and species that are droughttolerant. These drought-tolerant species arefound on dead twigs and small woody branchesin the canopy of living trees. Often species ofboth ecological types are found in associationwith unicellular green algae, but there is noevidence that the fungi are lichenized.

A. Species Trapping Nematodesand Other Invertebrates

Since the classic work of Drechsler (1937a) onthe nematode-trapping hyphomycetes, thesefungi have attracted many researchers to thisfascinating system. The work of Barron (1977,1981) further set the stage for ecological anddescriptive work on these fungi. Pfister (1994,1997) and Pfister and Liftik (1995) documentedthe life history connection between thesenematode-trapping hyphomycetes and teleo-morphic members of the Orbiliomycetes. Theseveral anamorphic form genera involved arediscussed in what follows.

Trapping of nematodes and other inverte-brates is accomplished by the formation ofconstricting rings, hyphal networks, or stickyknobs. These trapping structures are often, butnot exclusively, initiated in the presence ofprey. When nematodes become ensnarled inthe trap, the fungus then grows and penetratesthe body of its prey and proliferates within it.Conidia are formed in the presence or absenceof nematodes and are generally dispersedacross the medium, that is, they are not con-centrated around trapped nematodes (Barron1977). Earlier classification schemes for thesefungi relied primarily on conidial morphology,particularly spore shape and septation. Phylo-genetic studies have indicated that the form ofthe trapping devices gives important informa-tion for classification (Hagedorn and Scholler1999; Rubner 1996; Scholler et al. 1999). In

addition to trapping nematodes, some hypho-mycetes in the orbiliaceous lineage trap othersmall invertebrates such as collembolans andrhizopods (e.g., Barron 1981; Drechsler 1936,1937b). Even though these fungi may occur onwood or cellulose-rich substrates, there is evi-dence that few of the nematode-trapping fungiare able to break down cellulose (Park et al.2002).

B. Saprobic Species

Until the work of Baral (2011) and Marson, moststudies of diversity within the Orbiliomyceteswere focused on those species on moist sub-strates. The discovery that these fungi arehighly diverse in the dry habitats of hangingbranches in living trees has greatly expandedthe number of species that have been describedthrough intense collecting in such habitats.Although these species are treated here assaprobic, there is little clear evidence of theirmode of nutrition. Drechsler (1938) discussedat length hyphomycetes that are parasitic onoospores of Oomycota; these also seem now tobe clearly referable to the Orbiliaceae. Thesefungi were “considered from a morphologicalviewpoint. . . [to] fit acceptably in the preda-cious series” (Drechsler 1938). Whether theyfall in the main clade of nematode trappingOrbiliaceae or outside it remains to be studied,but that a variety of life styles and biotic modesare found within the family is unquestionable.It is important to note as well that no plantparasitic species have been discovered so farin this lineage.

IV. Morphological Features

A. Ascomata

Apothecial ascomata range in size from 0.5 to5 mm and are saucer-shaped to pulvinate.Macroscopically they have been described asappearing waxy at sight or to touch. This isa reference at least in part to their shiny, trans-lucent appearance. The sterile tissues of theascomata are composed of an outer layer, or

38 D.H. Pfister

ectal excipulum, of globose or angular cells thatin some species give rise to superficial hairs.These cells may contain one or more cytoplas-mic bodies that may take on several differentshapes but disappear when material is mountedin KOH. Cells in the outer excipulum may beencrusted with granules or produce glassy pro-jections or the cells may be embedded in anamorphous matrix. The inner layers of theascomata are of interwoven hyphae or com-pressed angular cells (Nannfeldt 1932).

B. Asci

The asci of members of this class are small cylin-drical to broad cylindrical with or without cro-ziers; in some cases they have elongate, forkedbases. Asci contain eight to many ascospores perascus. Asci are inamyloid. The apex ranges fromhemispherical conical to truncate. Walls are thin,composed of two layers in transmission electronmicroscopy (Benny et al. 1978; Kumar et al.2012). The apex is generally little developed.Benny et al. (1978) reported no pores; Kumaret al. (2012) found an electron-light zone at theapex. In some taxa, an opening develops on theshoulder of the truncate asci (Zhang et al. 2007),and this was confirmed by Kumar et al. (2012). Insome species, the apical walls may be thickenedto form a cap (Kohlmeyer et al. 1998), as inOrbilia subgenus Hemiorbilia, in which theapex of the ascus is thickened (Baral 2011). Inall cases, asci appear to dehisce by irregular tear-ing. Kumar et al. (2012) found similaritiesbetween the asci of the Orbilia species they stud-ied and members of the Taphrinomycotina. Asciand paraphyses may be embedded in a gelati-nous matrix that causes them to stick togetherand not fan out when crushed for microscopicobservation. This is particularly the case inmem-bers of the genus Hyalorbilia.

C. Ascospores

The initial striking feature of the ascospores istheir small size. They range in size from 3 to8 mm. Observation of them is difficult in somesituations and requires oil immersion and

enhanced magnification. Spores are globose,ellipsoidal, ovoid, reniform, acicular, or filiformand mostly smooth, although spore wallornamentations are known, for example, inO. xanthostigma. Ascospores of the Orbiliomy-cetes contain an inclusion, the spore body. Thismembrane-bound body was suggested to derivefrom the plasma membrane by Baral (2003),but Kumar et al. (2012) and Benny et al.(1978) showed that the spore body is derivedfrom mitochondria. The spore body is attachedto the cell membrane and is surrounded by arough endoplasmic reticulum (Benny et al.1978). The contents are electron dense (Bennyet al. 1978). Under a light microscope it is seenin unstained living spores as a refractive body.Its appearance can be enhanced by applicationof aqueous brilliant cresyl blue or other vitalstains. It disappears in dead spores and can bedestroyed by application of KOH. The sporebody is a synapomorphy for the class and cantake on many different forms, from globose totear-shaped to elongate. Its shape and orienta-tion is consistent within the ascospores of aparticular species. The shape and position ofthe spore body is considered a critical taxo-nomic character. Generally spores have a singlespore body, but an example of a spore with twospore bodies is known (Wu et al. 2007). Asmentioned previously, its contents are electrondense; it does not appear to be composed oflipids but may be proteinaceous (Kumar et al.2012). No function has been attributed to thespore body, but Benny et al. (1978) offeredthree possible functions: for flotation and bal-ance in a liquid environment before and duringgermination, storage of waste products, andstorage of materials for use during germination.None of these functions has been documented,and ultimately the function of the spore bodymay have to do with special metabolic activitieswithin the spore.

D. Paraphyses

Paraphyses are sparingly septate, broad, some-times with a prominent capitate terminal cell.They may be encrusted or contain refractivematerials. In some species, the paraphyses and


asci are closely adherent and are difficult toseparate.

E. Septal Structures

Ascus, ascogenous, and nonascogenous hyphaehave simple septa, with septal pores plugged byunelaborated electron-dense, nonmembranousocclusions. Globose Woronin bodies werelocated on both sides of the septum (Kumaret al. 2012).

F. Nuclear Division

Division is characterized by the retention of anintact nuclear envelope and a two-layered disk-shaped spindle pole body (Kumar et al. 2012).

G. Anamorphic States

Many members of the Orbiliomycetes havebeen shown to produce mitospores in culture;they are hyphomycetous or synnematous. Allconidia are formed by holoblastic wall exten-sion. A variety of named form genera have beenapplied to these conidial states. Anamorphs canprovide some useful information on the biologyand ecology of these fungi. Those that havebeen demonstrated to trap nematodes andother invertebrates fall into the followinggenera: Arthrobotrys (Li et al. 2005; Mo et al.2005; Pfister 1994, 1997; Pfister and Liftik 1995;Qiao et al. 2011), Drechslerella (Li et al. 2005),Dwayaangam (Barron 1991), Gamsylella,known only in its anamorphic state (Scholleret al. 1999), Lecophagus (Tanabe et al. 1999),and Monacrosporium (Li et al. 2005; Pfister1997). There remains debate about the applica-tion of some of these names. For generaloverviews the interested reader may consultHagedorn and Scholler (1999), Liou and Tzean(1997), and Scholler et al. (1999). Through amultigene analysis Yang et al. (2007) postulatedthat two lineages evolved trapping mechanisms,with one lineage giving rise to constricting rings

and the other adhesive traps, but, importantly,these fungi form a single clade. Yang et al. (2007)proposed a scheme for the evolution of trappingstructures.

Other form genera are those that producestaurosporous or helicosporous conidia or areassociated with aquatic habitats. These includeAngulospora (Pfister 1997; Webster 1992;Webster andDescals 1979),Dicranidion (reportssummarized by Pfister 1997), Dwayaangam(Kohlmeyer et al. 1998), Helicoon (Pfister 1997),Trinacrium (Matsushima 1995), and Triden-taria. Others are found on a variety of plantmaterials in terrestrial habitats, and theseinclude Brachyphoris (Chen et al. 2007a, c), Dac-tylellina (Li et al. 2005; Qin et al. 2010),Dactylella(Chen et al. 2007a, b, c; Pfister 1997; Qin et al.2010), and Pseudotripoconidium (Yu et al. 2011).

Staurosporous conidia and those reportedfrom other aquatic anamorphs are detected instem flow, through-fall, and treeholes (Gonczoland Revay 2003, 2004, 2006; Revay and Gonczol2011). Among these are conidia referred toform genera of anamorphs associated withspecies of Orbiliomycetes. These include spe-cies of Angulospora, Dactylaria, Dicranidion,Dwayaangam, Trinacrium, and Tridentaria.Of these Gonczol and Revay (2004) foundthat Trinacrium in particular was prevalentand that Dwayaangam and Trinacrium specieswere particularly diverse and geographicallywidespread (Gonczol and Revay 2006). Suchobservations suggest that canopies are impor-tant habitats for these fungi. We expect thatthese are likely Orbilia anamorphs that areassociated with the drought-tolerant, canopy-inhabiting Orbiliomycetes, which are fungi ondead branches in many woody plants. Gonczoland Revay (2006) say, regarding their findingsof aquatic hyphomycetes in these terrestrialhabitats, that “this reinforces our belief thatan ecological group of hyphomycetes distinctfrom those in lotic habitats exists and functionsin canopies.” By extension, we might assumethat branches and twigs inhabited by Orbi-liomycetes are a major part of this canopyecosystem.

40 D.H. Pfister

V. Reproduction

Although many of the Orbiliomycetes havebeen grown in culture, few reports have beenpublished on apothecial production in the lab.Spontaneous production of ascomata has beennoted (Drechsler 1937a; Rubner 1994). Zachar-iah (1983) was able to induce ascomatalprimorida. Breeding systems have not beenstudied in part because of the unpredictabilityof producing ascomata in culture.

VI. History of Classification andCurrent Hypotheses

The family Orbiliaceae was created in 1932in Nannfeldt’s (1932) classic treatment of theinoperculate discomycetes. Recognizing thespecial features of this group, he removed thegenera Orbilia andHyalina from the core groupof inoperculate discomycetes. Primary treat-ments of the family were those by Svrcek(1954) and Spooner (1987). Nannfeldt’s cir-cumscription of the family was used with fewchanges until the 1990s. The placement of thefamily outside the Leotiomycetes lineage initi-ally began to be questioned by Pfister (1997),and subsequent work has confirmed the place-ment as an early diverging lineage within thePezizomycotina (Gernandt et al. 2001; Spata-fora et al. 2006). The position of the Orbiliomy-cetes as an early diverging lineage in thefilamentous Ascomycota along with the Pezizo-mycetes was one of the major surprises in theera of molecular phylogenetic studies.

Within the Orbiliomycetes there is a singleorder, and only three teleomorphic genera arerecognized. Other genera may well be proposedas more of these fungi come to be knownthrough wider collection of them and collec-tions come under deeper scrutiny. Thedescribed genera are Orbilia, the largest andmost diverse genus with two subgenera andnine sections in Baral’s treatment (2011), Hya-lorbilia with six to eight species (Baral andMarson 2000), and Pseudorbilia, with a singlespecies (Zhang et al. 2007). These genera aredistinguished based on characteristics of the

ascus, the ectal excipulum, spore bodies, thepresence or absence of gelatinous material inthe hymenium, and pigmentation [see Zhanget al. (2007) for a summary of the genera].

VII. Growth in Culture

One of the most remarkable features of theOrbiliomycetes is the ease with which most ofthe species can be cultivated on standardmedia. Spores deposited on the surface of agarmedia germinate readily, with the exception ofthe species of Hyalorbilia for which there areonly a few reports of successful cultivation.Spores germinate quickly, and growth is oftenluxuriant on substrates containing glucose.Sporulation is common under room condi-tions.

VIII. Pezizomycetes: An Overview

The Pezizomycetes comprise a single order,Pezizales, with 16 families currently recognized.The full diversity of the order has not yet beencompletely recognized in the classification, andno doubt other lineages will of necessity benamed. Ascomata are both epigeous and hypo-geous. The epigeous types are apothecial, cleis-tothecial, or highly reduced, being composed ofonly a few asci in clusters on vegetative hyphaewith little or no excipular tissue. In epigeouslineages, spores are generally forcibly dis-charged with the asci rupturing by the forma-tion of an operculum. Hypogeous membersoccur in most families containing mycorrhizalmembers. To date, more than 15 independentorigins of trufflelike members are knownwithin a majority of the families (Læssøe andHansen 2007).

IX. Occurrence and Distribution

Pezizomycetes can be found around theworld, but representatives are unevenlydistributed. Members of certain families, suchas the Pezizaceae, Morchellaceae, Helvellaceae,


Rhizinaceae, and many of the Pyronemataceae,show a particularly high diversity in tempera-ture regions. Others are more abundant intropical areas, as exemplified by the Sarcoso-mataceae and Sarcoscyphaceae. Recent studieshave made clear that, although collecting in thisgroup is robust in many areas of the NorthernHemisphere, the Southern Hemisphere ispoorly documented. Nutritionally, Pezizomy-cetes are saprobic or mutualistic (Tedersooet al. 2006) or are parasitic on bryophytes andvascular plants (Hansen and Pfister 2006).Many of the species collected on soil occur indisturbed areas or in soil that has a high pH andlow content of organic matter. Petersen (1985)provides a review of the edaphic factorsinvolved in growth and reproduction.

A. Parasitic Species

The plant parasitic species are scattered in var-ious lineages. Rhizina undulata is a seriousroot parasite of conifers (Ginns 1968). Pithyaspecies may cause dieback on conifers. Calos-cypha fulgens is implicated as a seed pathogenof conifers (Paden et al. 1978; Salt 1974).Urnulacraterium has been implicated as the causalagent of strumella canker in oak (Davidson1950). Phymatothrichopsis ominivora is a rootpathogen of cotton and other dicotyledonousplants and is known only in its anamorphicstate (Uppalapati et al. 2010). A clade in thePyronemataceae, including Octospora andLamprospora, is parasitic on bryophytes (Han-sen and Pfister 2006). Apothecia occur on thethalli or surrounding soil if they are rhizoidalparasites (Dobbler 1979).

B. Mycorrhizal Species

With the advent of molecular approaches tostudying mycorrhizal root tips a number ofexamples of mycorrhizal Pezizomycetes havebeen documented, and it is now known thatmycorrhizal lineages are found throughout theclass (Tedersoo et al. 2006). Morphologically,the mycorrhizae have a mantle that is oftenthin, have a well-developed Hartig net, and

generally do not form rhizomorphs (Tedersooet al. 2006; Wei et al. 2010). Mycorrhizal speciesseem to predominate in areas that experiencexeric conditions (Smith et al. 2006). Mycorrhi-zal lineages are often also those that containtruffle or trufflelike taxa. There are no truffle-like species in the families Sarcoscyphaceae andSarcosomataceae, and likewise there are noknown mycorrhizal species.

C. Saprobic Species

Pezizomycetes occur on organic material ofvarious types—decaying wood, dung, leaf litter,and twigs. The diversity of Pezizales on dung iswell documented, with many studies and keysavailable (Bell 1983; Doveri 2004; Richardsonand Watling 1997). Some clades are nearlyexclusively found on dung, most notably spe-cies of Ascobolaceae (Brummelen 1967). Dung-inhabiting species are found in several clades ofthe Pyronemataceae and Pezizaceae (Hansenand Pfister 2006; Hansen et al. 2001; Perryet al. 2007). In most cases, little is known ofthe biology of saprobic species. Sarcoscypha-ceae, Sarcosomataceae, and Chorioactidaceaeare found exclusively on wood, leaves, andplant debris.

X. Morphological Features

A. Ascomata

Apothecia are the basic type of ascomata. Theserange in size from several millimeters to severalcentimeters and vary from sessile cups of smallto large size to stalked cups to the stipitatepiliate structures found in the Helvellaceae,Discinaceae, and Morchellaceae. Some highlyreduced members are little more than smallfascicules of asci such as in Ascodesmis. Furtherreductions include highly reduced forms foundin Eleutherascus and Monascella (Guarro andArx 1986; Stchigel et al. 2001). Here the asci areformed in clusters on unspecialized hyphae.Ascomata are often highly pigmented, particu-larly the hymenium. Carotenoid pigments havebeen characterized (Arpin 1969).

42 D.H. Pfister

Variations are found in typical apothecialascomata. On the one hand, there are highlyreduced types that are merely asci scatteredon hyphae as mentioned previously, but smallcleistothecial ascomata have also been found ina few cases (Hansen et al. 2005b). In the case ofOrbicula parietina, active discharge is lost andspores are presented in a powdery mass. Hey-denia species form stalked cleistothecial fruitbodies closely related to O. parietina (Lecht-mann and Clemencon 2011). The ascomata ofHeydenia, which was recently placed in thePyronemataceae (Lechtmann and Clemencon2011), deserve special comment. H. alpina is asmall fungus that occurs on plant debris andmosses. It is stipitate with a dark stipe that atthe top expands to hold a pale mass of hyalinespores and radiating hyphae. No asci are pres-ent, but molecular evidence confirms that thisspecies belongs in the Pyronemataceae as aclose neighbor of Orbicula, another fungusthat produces dry powdery masses of sporesat maturity. The two genera share a cleistothe-cial fruit body and asci that seem to disintegrateearly in the development of the ascomata butdiverge on important morphological features(Lechtmann and Clemencon 2011). Thesegenera, often placed outside of the Pezizales,have been demonstrated through molecularsystematic studies to be members of the order.

Truffleoid fruit bodies are found in severallineages. Following the terminology of Weberet al. (1997), these are stereothecia, exothecia,or ptycothecia, depending on the arrangementof the asci and the presence or absence ofwell-developed hymenial layers. Truffle-typeascomata are derived from apothecial forms.Læssøe and Hansen (2007) summarize muchof the literature on these taxa.

Some highly reduced forms are foundamong bryophyte parasites. The fruit bodiesare partly closed and have only a few asci.They give the appearance of perithecia.

B. Asci

Brummelen (1978, 1994) summarized thestructural characters of the ascus in the Pezizo-mycetes. The apical apparatus, when present, is

in the form of an operculum, and its position,the reaction of the wall layers in various stain-ing agents in light microscopy, and the ultra-structure of the ascus wall are all importantcharacters. Amyloid asci are found in Peziza-ceae and Ascobolaceae (Hansen et al. 2001), butthis character has been lost several times, mostnotably in the hypogeous members of the Pezi-zaceae. Amyloid asci are not found outsidethese families.

The layering of the wall as seen in transmis-sion electron microscopy helps delimit groups,particularly the taxa with thick lateral walls inthe Sarcoscyphaceae and Sarcosomataceae. Theasci of these fungi were termed suboperculateby Le Gal (1946a, b, 1953). Subsequently,Ecblad (1968) and Samuelson (1975) dis-counted the term.

Not all members of the class have opercula.Hypogeous (Læssøe and Hansen 2007) andsome cleistothecial taxa (Hansen et al. 2005a,b) have lost the operculum and spores remaineither within asci until eaten and the fruit bodyis broken down, or the asci disintegrate and apowdery mass is formed.

C. Ascospores

No member of the Pezizomycetes has septatespores at maturity. Septa may form in germinat-ing spores, but only when a germ tube hasalready been established. The spores may takeon a variety of shapes from globose to naviculate,with smooth or ornamented surfaces. Generally,the ornamentations are derived from secondarywall material, although a few examples areknown of spore ornamentation without a contri-bution of secondary walls. The spore walls aremultilayered and may be thin or thick (Merkus1976). The number of nuclei per spore variesfrom one, two, or four to many, and such varia-tion has been shown to have some taxonomicvalue (Berthet 1964; Korf 1972, 1973).

D. Paraphyses

The pigmentation of the hymenium is attribu-ted to the pigments found in the paraphyses.


Yellow, red, and orange carotenoid pigmentsare distinctive features of some of these fungi.These pigments are dissolved in oil dropletsin the paraphyses. A variety of carotenoid pig-ments are known to occur in these fungi, assummarized by Arpin (1969). Paraphyses aregenerally septate and may be either uninucleateor multinucleate, this latter character beingused in the classification (Berthet 1964; Pfisteret al. 2008). In some cases, paraphyses are inter-spersed with hyaline or darkly pigmented, oftenthick-walled elements or setae. Examples ofsuch setae are found in members of the Rhizi-naceae, Sarcosomataceae, Chorioactidaceae,and Sarcoscyphaceae.

E. Septal Structures

Ultrastructural characters of septal pore plugsand Woronin bodies correlate to some degreewith families and lineages in the order. Kim-brough (1994) summarizes much of the infor-mation. Septal pores in vegetative hyphaegenerally have lamellae embedded in a matrix.These septa generally have associated Woroninbodies. The Woronin bodies take on severalforms—globular, hexagonal, or cylindrical,sometimes considerably elongate. The form ofthe Woronin bodies is an important taxonomicand phylogenetic character. The septa at thebase of the asci also provide important charac-ters. These septa are occluded by dome-shaped,pyramidal, or dumbbell-shaped structures.These plugging structures show electron-densebands, lamellae, and raylike extensions.

F. Anamorphic States

Anamorphic states have been reported acrossmany families. Conidia are blastic in develop-ment and are generally hyphomycetous.Table 2.1 provides a summary of the knownanamorphs. In many of these anamorphs, thegermination of conidia has not been observed,suggesting that they may rather act as sperma-tia. The investigations by Healy et al. (2013)identify anamorphic spore mats in severalclades in the Pezizaceae and Tuberaceae.

Attempts to germinate mitospores from thesemats have failed, and the function of thesespores remains unknown. Several anamorphicstates have been discovered through molecularphylogenetic studies to belong within thePezizomycetes, but they have no knownteleomorphs. Most notable among these is Phy-matotrichopsis omnivora, the cotton root path-ogen. This falls within the Rhizinaceae based onmolecular studies, but despite intensive studyof this important pathogen, no evidence of ateleomorph has been discovered. Anotherexample is Cephaliophora, a dung-inhabitingfungus and one that has been implicated incausing keratitis (Hoog 2000).

XI. Reproduction

Extensive studies have been carried out on sev-eral members of the class. Ascobolus was earlyincorporated as a genetic tool. Pyronema hasalso been extensively studied. Early cytologicalstudies on members of the Pyronemataceaewere used to explore mitotic events in asci.

XII. History of Classification andCurrent Hypotheses

The current classification has its origins in thework of Boudier (1885, 1907), who was the firstto use the presence of an operculum to definethis group. Hypogeous, truffloid members pre-viously treated in the order Tuberales have nowbeen placed in the Pezizales based on morphol-ogy, cytology (Trappe 1975), and molecularsequence analyses (Læssøe and Hansen 2007).Wide-ranging phylogenetic work within theorder led to the recognition of three primarylineages (Landvik et al. 1997). Subsequent workhas expanded this framework and has sug-gested groupings of families that in part reflectthose previously based on morphological, cyto-logical, and pigment data and are noted inearlier work (Korf 1972, 1973; Rifai 1968). Themost recent comprehensive overview of theclass is that of Hansen and Pfister (2006). Cur-rently, 15 families are recognized (Fig. 2.1),

44 D.H. Pfister

Tab

le2.1Su

mmaryofknownan

amorphsofPezizomycetes

Fam

ily

Anam

orphic

form

genus

Teleomorphic

genus

References

Ascob

olaceae

Rhizostilbella

Ascobolus

Seifert(1985)

Papu

lospora

Ascobolus

Brummelen

(1967)

Anoidialstate

Ascobolus

Brummelen

(1967)

Caloscyphaceae

Geniculodendron

Caloscypha

Paden

etal.(1978)

Chorioactidaceae

Kumanasamuhageaster

Chorioactisgeaster

Nagao

etal.(2009)

Verticicladium

Desmazierella

acicola

Paden

(1972)

Morchellaceae

Costantinella

Morchella

Paden

(1972)

Pezizaceae

Glischroderma

Pezizaceae

Norm

anan

dEgger

(1999),Han

senet

al.(2001),Healy

etal.(2013)

Chromelosporium

Peziza,Plicaria,Muciturbo

Hennebert(1973),Paden

(1972),Warcupan

dTalbot(1989),Healy

etal.(2013)

Oedocephalum,includinghighly

reducedform

sPeziza,Pachyella,Iodophanus,

Cleistoiodophanus

Hennebert(1973),Hennebertan

dBellemere(1979),Paden

(1972),

Bezerra

andKim

brough

(1976)

Pyron

emataceae

Actinosporellamegalspora

Miladinalechithina

Descalset

al.(1998)

Alciphilavu

lgaria

Byssonectria

Harmaja(2002a,b)

Ascorhizoctonia

Tricharina

Yan

gan

dKorf(1985),Barrera

andRomero(2001)

Cephaliophora

Noneknown

Tan

abeet

al.( 1999)

Com

plexipes

Wilcoxina

Yan

gan

dKorf(1985)

Dichobotrys

Trichophaea

Hennebert(1973)

Micronem

atobotrys

Noneknown

Sunan

dGuo(2010)

“Nod

ulosporium”-like

Geopyxismajalis

Paden

(1972)

Rhizinaceae

Phym

atotrichopsis

Noneknown

Uppalapatiet

al.(2010)

Sarcosom

ataceae

Con

oplea

Urnula

craterium,Plectania,

Sarcosom

alatahensis

Hugh

es(1958),Paden

(1972)

Sarcoscyphaceae

Molliardiomyces

Phillipsia,Sarcoscyph

a,N

anoscyph

aPaden

(1984),Pfister

(1973b

)Tuberaceae

Unnam

edsympodulosporous

type

Tuber

Urban

etal.(2004),Healy

etal.(2013)


though the relationship among those families inmany instances is not well resolved. Althoughthis group is reasonably well known, futuresampling will certainly change our understand-ing of the relationships and of these lineages. Aparticular focus is on the large and heteroge-neous family Pyronemataceae, in which severallineages are recognizable based on bothsequence analyses and expanded knowledge ofnutritional modes, morphology, and anamor-phic states.

General overviews of the families can befound in Cannon and Kirk (2007). The follow-ing augmented descriptions include availablestructural and cytological information that hasbeen used in refining the classification.

A. Families of the Pezizomycetes

1. Ascobolaceae

Only epigeous members are known, and theseoccur primarily on dung, but a few species arefound on plant material; Ascobolus carbonariusis found on burned material (Brummelen1967). All species are saprobic and ascomatahave multiple cell layers. Developmental pat-terns have been characterized by Brummelen(1967). Cleistothecial developmental types arefound. Asci blue diffusely along the walls iniodine solutions. Ascospores are uninucleate(Berthet 1964); in Ascobolus and Saccobolusthe spore walls are ornamented with purplebrown pigments that become fissured at matu-rity (Brummelen 1967). The placement here ofThecotheus species, with their hyaline ascos-pores, has been suggested on morphologicalgrounds and has been confirmed in molecularphylogentic studies (Landvik et al. 1997). Septaassociated with the ascogenous system aredome-shaped (Kimbrough 1994; Kimbroughand Curry 1985). Three genera are generallyrecognized.

2. Ascodesmidiaceae

Ascomata are much reduced in most genera; forexample, in Eleutherascus species the asci arescattered on hyphae. In Ascodesmis, several asci

are formed on a much-reduced excipulum(Brummelen 1981). These species are saprobicon dung and often are isolated from soil. Asciare inamyloid and are saccate or pyriform.Ascospores are brownish and have reticulatespore ornamentations. Septa in ascogenouscells and the ascus bases are dome-shapedwith arrays of radiating tubular elements anda striate structure associated with the septalpore rim in vegetative cells (Brummelen 1989;Kimbrough 1994). Four genera are placed in thefamily (Hansen et al. 2005b). A recent study byHansen et al. (2013) places this family withinthe larger and highly diverse sister group to thePyronemataceae sensu stricto.

3. Caloscyphaceae

The brightly colored cupulate ascomata stainblue green when bruised. No hypogeous mem-bers are known. Caloscypha fulgens is a parasiteof conifer seeds and seedlings. The ascomatahave a well-developed inner layer of interwovenhyphae and an outer layer of globose or angularcells. Ascospores are globose, and their wallsare smooth (Harmaja 2002a). The genus Calos-cypha was previously placed in the Pyronema-taceae, in part because of its carotenoidpigments and because of the globose spores(Arpin 1969; Korf 1972, 1973). For details onseptal construction see Kimbrough and Curry(1986b). Recently a second genus was added tothe family, Kallistoskypha, with a single species,K. incarnata, which is associated with Eucalyp-tus found around the Mediterranean region(Pfister et al. 2013).

4. Chorioactidaceae

The ascomata are cupulate or deep urnulateand dark on the outer surface; the hymeniumis beige, brownish, or orange. No hypogeousmembers are known in this family, and all thespecies are considered to be saprobic. The asco-mata have a well-developed inner layer and anouter layer of globose or angular cells that giverise to thick, brown hairs encrusted with gran-ular material. The asci are inamyloid and thick-walled with a terminal operculum. Ascospore

46 D.H. Pfister

ornamention is in the form of warts or ribs.Four genera have been included (Pfister et al.2008).

5. Discinaceae

The ascomata of this family are discoid or gyro-mitroid. Both epigeous and hypogeous mem-bers are known. Many species in the family aremycorrhizal (Tedersoo et al. 2006, 2010). Theascomata are characteristically constructedwith an inner layer of interwoven hyphae andan outer layer of elongate cells oriented perpen-dicularly to the outer surface. Asci are inamy-loid, and ascospores are tetranucleate (Berthet1964), smooth, or elaborately ornamented withwarts, often with apiculae. Woronin bodies areelongate and often surround the septal pore.The septa at the base of asci are accompaniedby an electron-opaque, hemispherical structurethat becomes cone- to dumbbell-shaped withV-shaped structures; an electron-translucenttorus separates the pore plug from the septalpore border (Kimbrough 1991, 1994). Theseptal ultrastructure is similar to that of theHelvellaceae. Generally, five or six genera arerecognized.

6. Glaziellaceae

The ascomata in this family are large and hol-low with a basal opening. The unisporic, clavateto globose asci are embedded in the rindlikewall. Ascus walls break down, but the sporesremain embedded in this peridiumlike wall.The single species, Glaziella aurantiaca, is pre-sumed to be mycorrhizal. See Gibson et al.(1986) for ultrastructural details that initiallysupported the placement of Glaziella in theAscomycota.

7. Helvellaceae

Ascomata are sessile cupulate or stipitate cupu-late, saddle-shaped, or columnar (Abbott andCurrah 1997; Dissing 1966). Both epigeous andhypogeous species are found in the family(Hansen and Pfister 2006; Kimbrough et al.1996). Many or most are mycorrhizal (Tedersoo

et al. 2006). The ascomata are characteristicallyconstructed with an inner layer of interwovenhyphae and an outer layer of elongate cellsoriented perpendicularly to the outer surface.Asci are inamyloid. Ascospores are tetranucle-ate (Berthet 1964), smooth, or ornamented withirregular warts, and Woronin bodies are elon-gate, hexagonal, or globose (Kimbrough 1994).Septa at the base of the asci are electron-opaque. There are hemispherical structuresthat become cone- to dumbbell-shaped withV-shaped striations; in vegetative cells, anelectron-translucent torus separates the poreplug from the septal pore border. Vegetativecells possess globular or slightly angled Woro-nin bodies (Kimbrough 1994; Kimbrough andGibson 1989; Kimbrough et al. 1996).

8. Karstenellaceae

In this family, the ascomata are little more thana very thin, resupinate crust situated on leaflitter and wood surfaces. Asci are scattered onthis mycelial mat. Nothing is known of its modeof nutrition. Asci are inamyloid and operculate.Ascospores are binucleate or multiguttulate(Hansen et al. 2008; Harmaja 1969). No ultra-structural details are known for the vegetativeseptal construction or for the septa of the asci.Molecular data place it in an unresolved posi-tion near Helvellaceae and Tuberaceae. There isa single genus with a single species recognized,Karstenella vernalis.

9. Morchellaceae

The morels are characterized by stipitateapothecia, with an interrupted hymenial layergiving a honeycomb appearance, or by cupulateforms such as Disciotus. Hypogeous membersinclude Leucoangium (Li 1997) and Kalapuya(Trappe et al. 2010). Species are saprobic andhave been implicated in mycorrhizal relation-ships (Buscot 1994; Dahlstrom et al. 2000). Asciare inamyloid. Ascospores are multinucleate(Berthet 1964) and lack both prominent wallornamentation and internal oil droplets. Tradi-tional classifications of the species accept six toeight species, but phylogenetic studies indicate


the presence of many species (Du et al. 2012;Kuo et al. 2012; Taskin et al. 2010) that seemrestricted to specific continents (O’Donnellet al. 2011). Some of these species are morpho-logically distinct; others are cryptic (O’Donnellet al. 1997, 2011). The septal construction issimilar to that found in the Helvellaceae. Atthe base of the asci, dome-shaped structureswith V-shaped striations are found at the septalpore. Lamellate structures are found withinseptal pores of most vegetative cells. ElongateWoronin bodies have been found along withhexagonal ones (Kimbrough 1994). Five or sixgenera are recognized.

10. Pezizaceae

Both epigeous and hypogeous taxa are found;there are multiple origins of the hypogeous taxawithin several clades (Hansen et al. 2001, 2002,2005a; Healy et al. 2009). Saprobic membersinclude those on dung, wood, and other plantdebris. Mycorrhizal taxa are found in severallineages. Some taxa are found exclusively onburned areas. The ascomatal structure varies,but multiple layers composed of large, thin-walled globose cells are often present. Asci gen-erally become blue in iodine solutions. Thisbluing can take several forms. The reactionmay be diffuse along the entire wall or concen-trated in the upper portion of the ascus butmost intensely at the tip, or in the upper por-tion with a more intense ring surrounding theopercular region (Hansen et al. 2001). The blu-ing reaction has been lost in several taxa,including some that are hypogeous. Ascosporesare uninucleate (Berthet 1964), with or withoutsecondary wall ornamentations (Hansen et al.2001, 2002). Oil droplets may or may not bepresent in the ascospores. Septa in vegetativecells are lamellate with large globose Woroninbodies. At the ascus bases, septa are occludedby convex or biconvex bands that become cov-ered with electron-opaque amorphous materialor by an additional secondary wall (Curry andKimbrough 1983; Kimbrough 1994; Kimbroughet al. 1991). Approximately 30 genera are cur-rently recognized in the family, but it is wellestablished that the genus Peziza is nonmono-

phyletic and will need to be broken down intoseveral additional genera (Hansen et al. 2001,2005a, b).

11. Pyronemataceae

Pyronemataceae is the largest of the families ofthe class and the most diverse ecologically andmorphologically. As recognized here, the familyincludes Aleuriaceae, Humariaceae, Otideaceae,and Geneaceae. These fungi are saprobic,mycorrhizal vascular plants or parasitic onbryophytes. Epigeous members are cupulate,often possessing hairs on the outer surface.Hypogeousmembers are scattered in the family.The ascomata show considerable variation inconstruction and development. Asci are inamy-loid, and ascospores vary in shape and orna-mentation from smooth to variouslyornamented (Perry et al. 2007). Several differentseptal types are present; at least four types ofsepta plugging have been associated with asci(Kimbrough 1994). These are the aleurioid type,which have a granular, opaque matrix that bor-ders both the ascal and ascogenous hyphal sidesof pores; later this becomes fan-shaped with alamellate electron-translucent torus adjacent tothe pore rim. The otideoid type, is characterizedby double translucent bands in a granular,opaque pore matrix. Later the pore plug is dif-ferentiated into two zones, an inner dense zoneand an outer less opaque zone. The pulvinuloidtype, is similar to the Helvellaceae at maturitywith V-shaped striations, but these are fewerand less prominent than in Helvellaceae. Thescutellinioid type has a large hemispherical sep-tal pore plug that becomes zonate; the innerzone adjacent to the pore lumen is electron-opaque, and an outer, thicker zone is composedof less dense material. In general, in this family,vegetative cells have a lamellate structure in theseptal pores. Woronin bodies are small andlargely globular, but often hexagonal.

The pyronema type has asci and ascogen-ous hyphae that are similar to those of theAscobolaceae but with a different electron den-sity core and small, radiating tubular bandssimilar to those of Ascodesmis (Kimbrough1994; Kimbrough and Curry 1986a, b).

48 D.H. Pfister

The family includes approximately 80genera. It is perhaps highly heterogeneous andone that will see future division and refinement.The family was recently studied by Hansen et al.(2013), and this work provides the most accu-rate overview of the family.

12. Rhizinaceae

The ascomata in members of this family are flat,recurved, or pulvinate. Rhizina undulata is apathogen of conifer roots. Also included here isPsilopezia, whose species are found on water-soaked wood and which is presumed to be asaprobe (Pfister 1973a). The construction of theascomata follows a pattern of interwovenhyphae forming the medulla, with more denselyinterwoven hyphae contributing to the corticallayer. These fungi are characterized by indeter-minate marginal growth. The asci are inamy-loid, and ascospores are smooth or ornamentedwith warts and apiculae. The spores are pre-sumed to be tetranucleate. Studies are neededon the septal structure. The family encom-passes the two genera mentioned earlier aswell as Phymatotrichopsis omninvora, which isknown only as an anamorph.

13. Sarcoscyphaceae

Ascomata are generally cupulate, bright col-ored, stipitate, or sessile. No hypogeous mem-bers are known; all are considered saprobic.The ascomata have a well-developed innerlayer and an outer layer of globose or angularcells or of tightly interwoven hyphoid cells ori-ented parallel to the outer surface. Cells on theouter surface sometimes give rise to single orfasciculate hairs. Ascospores are smooth orornamented with ridges and ribs. In vegetativecells, lamellate structures are poorly differen-tiated or missing. Septa in vegetative cells areimperforate, plugged by an electron-opaque,fan-shaped matrix surrounded by a number ofglobose electron-dense Woronin bodies. TheWoronin bodies are globose or occasionallyhexagonal and electron-opaque. At maturityobscure V-shaped striations may be found(Benny and Samuelson 1980; Kimbrough 1994;

Li and Kimbrough 1995b). Twelve genera arecommonly recognized within this family.Romero et al. (2012) review the classificationwithin the family.

14. Sarcosomataceae

In this family, ascomata are cupulate or urnu-late, tough and leathery of moderate to largesize, and black or dark brown on the outside,often with a paler hymenium. No hypogeousmembers are known. Most species are pre-sumed to be saprobic on plant debris, but inthe case of Urnula, the species is said to beparasitic. The ascomata have a well-developedinner layer, with gelatinous material, and anouter layer of globose or angular cells that giverise to dark hyphoid hairs. Asci are inamyloidand thick-walled with a terminal operculum.The ultrastructure of the asci and ascosporeshave been studied by Bellemere et al. (1990).The ascospores are smooth or with wrinkled orfolded walls or with low warts. In addition, theyare multinucleate. Septal structures are com-posed of an electron-dense matrix and globoseWoronin bodies that are often accompanied byshort or long, cylindrical, hexagonal Woroninbodies. Septa at the ascus bases are composed ofa dumbbell-shaped matrix with V-shapedbands. The septal structure was studied by Liand Kimbrough (1995b). Five or six genera arecommonly accepted.

15. Tuberaceae

Until recently, all members of this family wereconsidered to be hypogeous. The recent place-ment of Nothojafnea thaxteri among thesefungi is notable as the first epigeous memberof the family (Bonito et al. 2013). The trufflesof commerce (Tuber melanosporum andT. magnatum) belong here. Ascomata arehighly convoluted and folded, often with cham-bers or pockets of asci. The large, primarilyNorthern Hemisphere genus Tuber has beeninvestigated by Bonito et al. (2010). All mem-bers are mycorrhizal on a range of plantfamilies (Tedersoo et al. 2006). The asci areinamyloid, globose, or pyriform with one to


eight spores per ascus. The ascospores, in addi-tion to being often multinucleate, are oftenelaborately ornamented with reticula, ridges,and warts. Septal structure was studied by Liand Kimbrough (1995b), who determined thatthere was some heterogeneity among those spe-cies examined. In that study, the researchersfound long, cylindrical Woronin bodies insome of the species, similar to those of theMorchellaceae, Discinaceae, and Helvellaceae,and rectangular ones in another, similar tothose of the Pyronemataceae. Septa associatedwith ascogenous hyphae and ascus bases alsodiffered among the sampled taxa. O’Donnellet al. (1997) included a series of genera in addi-tion to Tuber. Seven genera are commonlyrecognized. Bonito et al. (2013) estimate a lateJurassic origin of the genus Tuber and discussthe Southern Hemisphere diversity.

XIII. Growth in Culture

The ascospores of saprobic species germinate,and often an anamorphic state is produced.Fungi in mycorrhizal lineages do not easilygerminate, and few examples are known oftheir anamorphic states. In some cases, fieldcollections of anamorphs have proven to bepezizalean, and there are many examples ofenvironmental samples linked with Pezizomy-cetes (Healy et al. 2013).

XIV. Conclusion

The Orbiliomycetes and Pezizomycetes areearly divergent lineages within the filamentousAscomycota. The two classes are remarkablydifferent in their ecology and in the structureof their asci. So far as is known, there are nomycorrhizal taxa in the Orbiliomycetes,whereas the mycorrhizal life style is found inmost families of the Pezizomycetes. Althoughanamorphs are known in the Pezizomycetes,their diversity is low; in the Orbiliomycetes,on the other hand, there is a wide range ofconidial morphologies. Within the Pezizomy-cetes there are no known examples of predatory

behavior, whereas some members of the Orbi-liomycetes trap and consume invertebrates.Recent studies have placed many hypogeousPezizomycetes within families. These studieshighlight the evolutionary patterns within theclass in which suites of changes, including lossof active spore discharge mechanisms andextended ascomata developmental times, takeplace in distantly related clades. Most hypoge-ous Pezizomycetes are found within clades withother mycorrhizal members. The diversity inboth Orbiliomycetes and the Pezizomyceteshas proven to be greater than previously antici-pated, and much researches remains to be doneregarding the biogeography and evolutionaryhistories of the group.

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Baral H-O (1992) Vital versus herbarium taxonomy:morphological differences between living anddead cells of ascomycetes, and their taxonomicimplications. Mycotaxon 44:333–390

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2 pezizomycotina: pezizomycetes, orbiliomycetes

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