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Phylogenetic Studies Within the Pezizales. I. 18S Rrna Sequence Data and Classification Author(S): F Mycological Society of America Phylogenetic Studies within the Pezizales. I. 18S rRNA Sequence Data and Classification Author(s): F. A. Harrington, D. H. Pfister, D. Potter and M. J. Donoghue Source: Mycologia, Vol. 91, No. 1 (Jan. - Feb., 1999), pp. 41-50 Published by: Mycological Society of America Stable URL: http://www.jstor.org/stable/3761192 Accessed: 03-10-2016 15:04 UTC REFERENCES Linked references are available on JSTOR for this article: http://www.jstor.org/stable/3761192?seq=1&cid=pdf-reference#references_tab_contents You may need to log in to JSTOR to access the linked references. JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at http://about.jstor.org/terms Mycological Society of America is collaborating with JSTOR to digitize, preserve and extend access to Mycologia This content downloaded from 140.247.98.12 on Mon, 03 Oct 2016 15:04:27 UTC All use subject to http://about.jstor.org/terms Mycologia, 91(1), 1999, pp. 41-50. © 1999 by The Mycological Society of America, Lawrence, KS 66044-8897 Phylogenetic studies within the Pezizales. I. 18S rRNA sequence data and classification F. A. Harrington1 INTRODUCTION D. H. Pfister Traditional classification schemes (e.g., Schroeter Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138 1893, Boudier 1907, Atkinson 1915, Nannfeldt 1932, Bessey 1964) classified those fungi forming apothe- D. Potter cial ascomata into a major group, the discomycetes, Department of Pomology, University of California, (Ascomycetes). Phylogenetic analyses using gene se- Davis, California 95616 quence data, however, have confirmed that morpho- M. J. Donoghue logical characters such as apothecial ascomata, ascus Department of Organismic and Evolutionary Biology, and ascospore shape are not necessarily reliable char- Harvard University, Cambridge, Massachusetts 02138 acters for inferring phylogenetic relationships (Ber- bee 1996, Berbee and Taylor 1992a, b, 1995, Momol et al 1996, Spatafora and Blackwell 1994, Saenz et al Abstract: The order Pezizales has been divided into 1995). Phylogenetic analyses of 18S rRNA gene se- two suborders. One suborder, the Sarcoscyphineae, quence data (Gargas and Taylor 1995, Spatafora was originally described to include members whose 1995, Landvik 1996, Landvik et al 1997) have shown asci were characterized by an unusual apical struc- the discomycetes to be a paraphyletic assemblage and ture, the suboperculum. Disagreements as to how have confirmed earlier suppositions that the two this structure should be defined, and indeed, wheth- principle orders, the Pezizales and the Helotiales, are er or not it exists at all, have rendered the status of not closely related (Nannfeldt 1932, van Brummelen the suborder controversial. The two families within 1978, Eckblad 1968, 1972). The order Pezizales, how- this suborder are the Sarcoscyphaceae and the Sar- ever, has been considered a monophyletic group, cosomataceae. Recent ultrastructural work demon- though not strongly supported (Spatafora 1995, strates that there is an apical thickening which is re- Landvik 1996, Landvik et al 1997). stricted to the Sarcoscyphaceae. In order to test the Because the ascus has been the single most-studied monophyly of the suborders of the Pezizales and ex- anatomical character within the Pezizales, this study amine the relationships within the Sarcoscyphineae, focuses on the relevance of the ascal apex on the phylogenetic analyses were carried out using DNA se- classification of this group. Members of the Pezizales quence data from the 18S rRNA gene. The strict con- have a dehiscence mechanism that typically involves sensus tree based upon these data shows both the an apical circumscissile rupture of the ascus wall to Sarcoscyphineae and the Pezizineae as paraphyletic. produce a lid, the operculum. Some pezizalean spe- These data suggest that the subordinal taxa currently cies, however, have asci in which the operculum has recognized within the Pezizales should be abandoned been lost or reduced (Trappe 1979), or in which the and the taxonomy revised to reflect phylogenetic re- ascus ruptures by a slit. Asci with opercula are also lationships. Strongly supported clades (i.e., greater found in taxa outside the Pezizales, such as Orcadia than 95% bootstrap value, 1500 replicates) include: (Kohlmeyer and Kohlmeyer 1979), but these fungi the Pezizaceae, the Morchellaceae, the Sarcoscypha- have never been classified within Pezizales and their ceae, the Helvellaceae, and a clade that includes the relationship to other Ascomycota is uncertain. Sarcosomataceae (which is paraphyletic), and the The significance of the operculum (FIGS. 2, 3) for Otidiaceae (represented only by 2 taxa). The genus discomycete classification was first recognized by Pindara, formerly placed in the Sarcoscyphaceae, is Boudier (1879, 1885, 1907). He divided the disco- nested within the Helvellaceae, and Wynnea, assigned mycetes by the mode of dehiscence. Two series were to the Sarcosomataceae by some authors, is posi- recognized, those with an operculum and those with- tioned in the Sarcoscyphaceae. out. Many of Boudier's peers (e.g., Cooke 1892, Kar- Key Words: cladistics, Pezizineae, Sarcoscyphi- sten 1885, Rehm 1895, Saccardo 1889, Schroeter neae 1893) however, did not agree with this division. Seav- Accepted for publication August 6, 1998. er's classic treatments (1927, 1928, 1942, 1951) divide 1 Email: [email protected] the discomycetes along Boudier's lines. Two French 41 This content downloaded from 140.247.98.12 on Mon, 03 Oct 2016 15:04:27 UTC All use subject to http://about.jstor.org/terms 42 MYCOLOGIA 1 2 3 FIGS. 1-3. Ascal apices according to Boudier and LeGal. 1. Apical chamber seen from different perspectives in Sarcosoma X 1500. The stippled structure is LeGal's coussinet or suboperculum (redrawn from LeGal 1946b). 2. Boudier's interpretation of Ascobolus asci and paraphyses with an empty ascus on the left showing an operculum X450 (redrawn from Schroeter, J. 1893). 3. Boudier's interpretation of the lid on the ascus of Ascobolus X 1200 (redrawn from Schr6eter, J. 1893). workers (Chadefaud 1942, 1943, 1946, Le Gal 1946a, ened eccentric opercula but other taxa, traditionally b, 1953) focused their observations on the mecha- placed in the family, had no such structures. The sub- nisms of ascal dehiscence in the Pezizales (operculate operculate ascus became the locus for ultrastructural discomycetes). Using light microscopic observations studies; details of its structure interpreted from light on the ascal apex morphology, Le Gal distinguished microscopy were questioned by investigators using an ascal apex that was characterized by having a TEM (van Brummelen 1975, 1978, 1994, Samuelson thickened sub-apical pad ("coussinet") in the apical 1975, Samuelson and Kimbrough 1978). Structurally chamber-the suboperculum (FIG. 1). In 1953, she some of the taxa show two thickened apical sublayers presented the view that this was a link between those (Bellemere 1994, Bellem&re et al 1990). This inter- taxa she considered the Pezizales, and the evolution- pretation differed from Le Gal's original concept arily primitive inoperculate Helotiales. She described (1946b) and Samuelson's (1975) revised version, but the family Sarcoscyphaceae as the "natural" inter- is similar to that of Samuelson et al (1980). Numer- mediary group for these species with subopercula. Le ous researchers (Das and Pant 1984, Denison 1963, Gal (1947) proposed two tribes, the Sarcoscypheae 1965, 1967, 1969, 1972, Gamundi 1957, 1959, 1971, for species with brightly-colored apothecia and the Korf 1957, 1963, 1970, 1972, Korf and Waraitch 1971, Urnulae for those with brown to black apothecia. Korf and Zhuang 1991, Paden and Tylutki 1968, Many classification schemes (Nannfeldt 1949, Korf 1969, Paden 1983, Pant and Tewari 1970, Rifai 1968, 1957, 1958, 1970, 1972, 1973, Dennis 1953, 1960, Wang and Zhuang 1997, Zhuang 1991, 1993) how- 1978, Denison 1963, 1965, 1972) followed Le Gal's ever, have used the term suboperculate without de- separation of the suboperculate from the operculate scribing it or fully accounting for the range of vari- taxa. Eckblad (1968) was the first to raise issue with ability seen with the light microscope. When Rifai the definition and the structure of the suboperculate (1968) proposed a suborder for the operculate taxa ascus. He noted (1968, 1972) that some taxa includ- (Pezizineae) and one for the suboperculates (the Sar- ed in the Sarcoscyphaceae did indeed have the thick- coscyphineae), he was codifying the commonly held This content downloaded from 140.247.98.12 on Mon, 03 Oct 2016 15:04:27 UTC All use subject to http://about.jstor.org/terms HARRINGTON ET AL: PHYLOGENY WITHIN THE PEZIZALES 43 view that ascus morphology was fundamentally differ- reactions. The 18S rRNA gene was either amplified as a sin- ent between the two groups and that it was an im- gle fragment with primer pairs PNS1 and NS8, or as two portant character in the classification of Pezizales. At overlapping fragments with the primer pairs PNS1/NS41 and NS 51/ITS 2 (http://www.botany.duke.edu/fungi/mycolab). the time Korf (1970)
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