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Morphological and DNA Sequence Evidence for Synonymy with the Gasteromycete Genus Pyrenogaster

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Morphological and DNA Sequence Evidence for Synonymy with the Gasteromycete Genus Pyrenogaster Mycologia, 97(1), 2005, pp. 139±149. q 2005 by The Mycological Society of America, Lawrence, KS 66044-8897 The myxomycete genus Schenella: morphological and DNA sequence evidence for synonymy with the gasteromycete genus Pyrenogaster Arturo Estrada-Torres INTRODUCTION Centro de Investigaciones en Ciencias BioloÂgicas, Universidad AutoÂnoma de Tlaxcala, Apdo. Postal Schenella simplex was described and illustrated as a 183. Tlaxcala 90000, MeÂxico new genus and species by Thomas H. Macbride (1911). A single collection gathered in Aug 1903 on Thomas W. Gaither a decaying pine log in Yosemite Valley, California, was Department of Biology, Slippery Rock University, designated as the holotype. Macbride expressed Slippery Rock, Pennsylvania 16507-1325 doubt about this taxon in the ®rst sentence of his Dennis L. Miller1 brief paper: ``This following description and accom- panying ®gures are submitted to mycologists partly Department of Molecular and Cell Biology F03.1, University of Texas at Dallas, Richardson, for the sake of eliciting information.'' Macbride fur- Texas 75080 ther noted that, ``If a slime-mould, the species is re- ferable to the family Dianemaceae and is akin to Carlos Lado those in which the capillitial threads pass from side Real JardõÂn BotaÂnico, CSIC. Plaza de Murillo 2, to side of the fructi®cation, attached at each end.'' 28014 Madrid, EspanÄa This unique combination of charactersÐaethalioid Harold W. Keller fructi®cations, simple capillitial threads twisted to- gether to form vertical columns attached to the outer Department of Biology, Central Missouri State University, Warrensburg, Missouri 64093 peridium and at the base of the fructi®cation along with tiny, smooth, spherical spores, 5±6 mm diamÐ were the stated hallmarks of this enigmatic taxon. Abstract: The genus Schenella has proven dif®cult to The status of Schenella simplex as a myxomycete was classify since its description as a new genus in 1911. so doubtful that Macbride omitted the taxon from Macbride placed it with the Myxomycetes but it was his 1922 monograph (Macbride 1922), nor was it in- unclear with which myxomycete, if any, it should be cluded in the Lister monograph (Lister 1925). grouped. Recent identi®cation of abundant samples In the 1934 monograph by Macbride and Martin of Schenella has aided a re-evaluation of its classi®ca- (1934) Schenella simplex again was included. Com- tion as a myxomycete. Morphological evidence based mentary after the species description again casts on light and scanning electron microscopy of re- doubt on the status of this taxon: ``A very curious cently collected specimens and on the type specimen form, of somewhat doubtful af®nities and placed in of Macbride suggested that it might be synonymous the Stemonitaceae on the basis of the dark violet with the gasteromycete Pyrenogaster. Analysis of DNA brown spores and the dark capillitium. There is no sequences from freshly isolated samples indicates that suggestion of columellae in the pillar-like columns. the genus Schenella is related closely to an anciently To the naked eye it suggests an amaurochaete.'' diverged, monophyletic group of fungi that includes Spores were described as ``rather coarsely tubercu- several gasteromycete genera, among them Geastrum, late'' and not smooth. Sphaerobolus and Pseudocolus. Comparisons of the Hagelstein (1944) made reference to Schenella sim- morphology and DNA sequences of authentically plex in the Amaurochaetaceae but again expressed identi®ed specimens of Pyrenogaster atrogleba indicate doubt about its status: ``. might appropriately be that it is synonymous with Schenella simplex. The no- placed in this family if conclusively proven to be a menclatural implications of this discovery are dis- form of Mycetozoa. The original description and ®g- cussed. ures are not impressive, and clearly indicate the au- Key words: Eumycetozoa, gasteromycete, molec- thor was uncertain.'' Schenella was not included in his ular systematics, Myxomycetes, plasmodial slime key to the genera. molds, Pyrenogaster, Schenella Martin (1949) included a note about Schenella in the Stemonitaceae that, ``if it is a myxomycete, (it) Accepted for publication 20 August 2004. would be placed in this family close to Amaurochae- 1 Corresponding author. E-mail: [email protected] te.'' A dichotomous key to 10 genera in the family 139 140 MYCOLOGIA fails to include Schenella. Martin (1961) described a tical to the S. simplex type. Morphological data, as second species of Schenella, S. microspora, after re- well as DNA sequence evidence from the Mexican examination of the type of S. simplex. He concluded specimens, also indicate that S. simplex is related to that Schenella was a valid genus in the Stemonitaceae, an anciently diverged group of gasteromycete fungi closely allied to Amaurochaete. Martin re-interpreted and should not be classi®ed as a myxomycete. Fur- the morphology of this taxon as a pseudoaethalium, ther, morphological characterization indicates that S. not an aethalium, with the sporangia arranged ver- simplex is synonymous with the gasteromycete fungus, tically much as in Dictydiaethalium. Each column Pyrenogaster atrogleba (Zeller) L.S. DomõÂnguez & Cas- (sporangium) appeared to have a distinct top with tellano. In support of this, DNA sequences obtained an individual peridium and a coiled, twisted mass of from authentically identi®ed P. atrogleba specimens pseudocapillitial threads attached also at the base of are identical to DNA sequences from the Mexican the fructi®cation. There was no trace of a columella. specimens of S. simplex. The capillitial system consisted of a bundle of threads Preliminary work on the status of Schenella has within each sporangium. Martin (1961) emended the been published as abstracts (Gaither and Keller 1997, generic and species description, emphasizing the Estrada-Torres et al 2002, Gaither and Keller 2002). dark capillitium and dark spores as the salient mor- phological characters for assignment to the Stemon- MATERIALS AND METHODS itaceae close to Amaurochaete. Spore diameter of S. simplex was given as 5±6 mm and for S. microspora 3.5± Recent ®eld collections of S. simplex were examined from 4(4.5) mm. Martin (1961) also noted that spores were two Mexican states, Tlaxcala and Veracruz. Representative small for a myxomycete but no smaller than other specimens are deposited in the TLXM herbarium with some duplicates at MA-Fungi. Specimens were washed with well known species. This statement is supported by alcohol and distilled water to eliminate as many spores as examples such as Stemonitis microsperma B. Ing, and possible. Freehand transverse sections were made of perid- S. smithii Macbr., with the smallest spore diameters ial fragments for microscopic examination and then rinsed known in the Myxomycetes (Martin and Alexopoulos and stained with a 1% aqueous solution of methylene blue 1969). following the technique described by Largent et al (1977). Nannenga-Bremekamp (1967) used capillitial Permanent slides of these sections or of complete fruiting characteristics to transfer Schenella from the Stemon- bodies were made in Hoyer's medium. Microscopic exami- itaceae to its own monogeneric family, the Schenel- nation was made with a light microscope equipped with dif- laceae. This transfer was based exclusively on the lit- ferential interference contrast imaging (Nomarski optics) erature because no specimens were examined. or with bright ®eld light microscopy. Fruiting bodies were The description of a second species in the genus, mounted in either distilled water, clear lactophenol or Hoy- er's medium. Selected specimens were photographed un- Schenella microspora, by Martin (1961) seems to have der 6003 or 10003 under the oil immersion lens using convinced other authors as to its identity as a myxo- either a Nikon E-600 microscope or an Olympus PM10 pho- mycete and recognition of a separate family, Sche- tomicrographic system. All SEM preparations used the crit- nellaceae (Martin and Alexopolous 1969, Nannenga- ical point drying technique. SEM images were recorded on Bremekamp 1974, Farr 1976, Martin et al 1983, Polaroid 55 ®lm using either of these SEMs: AMRAY 1200 Hawksworth et al 1995). at 35 kV, a JEOL JSM-35C, or a JEOL T-300 at 15 kV. Color Rammeloo (1985) examined spores of the type standards followed the ISCC-NBS Color Name Charts Illus- specimen of S. simplex using scanning electron mi- trated with Centroid Colors (Anon. 1976). croscopy, expressing doubt that the taxon was a Spore germination was observed using a suspension of myxomycete because the spores possessed a pore sim- spores in sterile distilled water placed in a depression mi- ilar to that of some taxa in the fungal order Agari- croscope slide. Hanging drop spore preparations using sealed cover glasses over a depression microscope slide were cales. One ®eld collection from Mexico more re- observed periodically up to 1 wk. Spore cultures were pre- cently was identi®ed as Schenella simplex and com- pared by spreading spores uniformly using a sterile glass pared with the type of S. simplex. RodrõÂguez-Palma rod with 0.1 ml aliquots of a spore suspension on the sur- and Estrada-Torres (1996) collected this specimen in face of these culture media: 2% water agar, potato-dextrose the Abies religiosa forest in Malintzi National Park, agar and a modi®cation of Melin & Norkrans medium for Tlaxcala, MeÂxico. ectomycorrhizal fungi (Marx 1969). This paper reports comparisons of additional spec- Specimens examined.ÐSchenella simplex T.H. Macbr., Type
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