The Simple-Septate Basidiomycetes: a Synopsis
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Mycol Progress DOI 10.1007/s11557-006-0502-0 ORIGINAL PAPER Robert Bauer . Dominik Begerow . José Paulo Sampaio . Michael Weiß . Franz Oberwinkler The simple-septate basidiomycetes: a synopsis Received: 22 December 2005 / Revised: 2 February 2006 / Accepted: 3 February 2006 # German Mycological Society and Springer-Verlag 2006 Abstract The simple-septate basidiomycetes comprise Taxonomical Novelties Agaricomycotina . more than 8,000 species that show a high morphological Agaricostilbomycetes . Atractiellomycetes . and ecological heterogeneity. To gain insight in the Classiculomycetes . Cryptomycocolacomycetes . phylogenetic relationships within this group, we compared Cystobasidiales . Cystobasidiomycetes . several ultrastructural features such as septal pore appara- Erythrobasidiales . Helicobasidiales . Kondoaceae . tus, form and behavior of the spindle pole bodies, types of Microbotryomycetes . Mixiales . Mixiomycetes . host–parasite interaction, presence or absence of colaco- Naohideales . Pachnocybales . Pucciniomycetes . somes, symplechosomes, atractosomes and cystosomes as Pucciniomycotina . Spiculogloeales . Ustilaginomycotina well as nuclear rDNA sequences coding for small- and large-subunit rRNA. Based on our integrated analysis, we Keywords Basidiomycetes . Fungal systematics . propose a new classification system for the simple-septate Molecular phylogenetics . Ultrastructure . Taxonomy basidiomycetes with the subphylum Pucciniomycotina and the classes Agaricostilbomycetes, Atractiellomycetes, Classiculomycetes, Cryptomycocolacomycetes, Cystoba- Introduction sidiomycetes, Microbotryomycetes, Mixiomycetes and Pucciniomycetes. We also propose the pucciniomycotinous BasedonestimatesbyKirketal.(2001), simple-septate taxa Cystobasidiales, Erythrobasidiales, Helicobasidiales, basidiomycetes (Urediniomycetes sensu Swann and Mixiales, Naohideales, Pachnocybales, Spiculogloeales Taylor 1995) consist of approximately 8,000 described and Kondoaceae and the new subphyla Agaricomycotina species. The Pucciniales (Uredinales) with ca. 7,000 (equivalent to the current Hymenomycetes) and Ustilagi- species is the largest order in this group, followed by the nomycotina (equivalent to the current Ustilaginomycetes). Septobasidiales and Microbotryales. Most simple-septate basidiomycetes have phragmobasidia. Holobasidia are extremely rare and occur only in Pachnocybe, Chiono- sphaera and Curvibasidium and possibly also in Colacosiphon (Kirschner et al. 2001; Sampaio et al. 2004; Oberwinkler and Bandoni 1982; Oberwinkler and Part 229 of the series ‘Studies in heterobasidiomycetes’ from the Bauer 1989). Morphologically and ecologically, the Botanical Institute, Tübingen University, Tübingen, Germany. simple-septate basidiomycetes exhibit a high degree of divergence. They comprise plant parasites as well as *) . R. Bauer ( D. Begerow M. Weiß F. Oberwinkler mycoparasites, saprobes and some human pathogens, Universität Tübingen, Botanisches Institut, Lehrstuhl für Spezielle Botanik und Mykologie, but mutualistic symbionts are not known in this group so Auf der Morgenstelle 1, far (Weiß et al. 2004). Sporulation ranges from scattered 72076 Tübingen, Germany basidia (as in Kriegeria) to resupinate fructifications e-mail: [email protected] (as in Saccoblastia) to complex stilboid or pycnidioid Tel.: +49-07071-2973212 Fax: +49-07071-295344 basidiomes (as in Pachnocybe and Heterogastridium, respectively). This tremendous morphological and ecolog- J. P. Sampaio ical diversity is reflected by a great genetic heterogeneity Centro de Recursos Microbiológicos, (Weiß et al. 2004). We assume that the simple-septate Secção Autónoma de Biotecnologia, Faculdade de Ciências e Tecnologia, basidiomycetes represent old basidiomycetous lineages, Universidade Nova de Lisboa, and that the current number of species may only represent 2829-516 Caparica, Portugal the tip of the iceberg. Although attempts have been made (e.g., Swann et al. performed stepwise: 30% resin in acetone at 4°C for 7 h, 2001; Weiß et al. 2004), a supraordinal classification of the 70 and 100% resin at 8 C for 20 h each and 100% resin at simple-septate basidiomycetes is far from settled. Thus, 18°C for approximately 12 h. Samples were then trans- only one higher subgroup, the Microbotryomycetidae, has ferred to fresh medium and polymerized at 60°C for 10 h. been described (Swann et al. 1999). This paper therefore Finally, samples were processed as described above for focuses on the evolution and supraordinal classification of chemically fixed samples, except that the sections were this heterogeneous group of basidiomycetes. To gain additionally stained with 1% aqueous uranyl acetate for 1 h. insight into the phylogenetic relationships within this Specimens used in the transmission electron microscopy group, we evaluated ultrastructural characters such as are specified in the figure legends using the following septal pore apparatus, form and behavior of the spindle acronyms: ATCC, American Type Culture Collection; BM, pole bodies (SPBs), host–parasite interactions, colaco- private herbarium Bernhard Müller; CCM, Czech Collec- somes, symplechosomes, atractosomes, and cystosomes as tion of Microorganisms; F, culture collection of the well as nuclear genes coding for rRNA of the small and Botanical Institute, University of Tübingen; FO, private large ribosomal subunits (SSU and LSU, respectively). herbarium F. Oberwinkler; GD, private herbarium G. This paper is influenced to a great extent by the so far Deml; GEL, private herbarium G. and E. Langer; HUV, more than 200 contributions of the series “Studies in Herbarium Ustilaginales Vánky; RB, private herbarium R. heterobasidiomycetes” published by the Lehrstuhl Spe- Bauer; RJB, private herbarium R.-J. Bandoni; and TUB, zielle Botanik und Mykologie, Universität Tübingen, Herbarium of the Botanical Institute, University of during the past 30 years. Tübingen. Materials and methods Molecular phylogenetic analyses Transmission electron microscopy DNA was isolated from cultures or herbarium specimens using a sodium dodecyl sulfate (SDS) method as described For conventional chemical fixation, samples were fixed previously (Begerow et al. 1997). The D1/D2 region of the with 2% glutaraldehyde in 0.1 M sodium cacodylate buffer nuclear gene coding for the LSU rRNA was amplified (pH 7.2) at room temperature overnight. Following six using polymerase chain reaction and the primers NL1/NL4 transfers in 0.1 M sodium cacodylate buffer, samples were (O’Donnell 1993). The nuclear gene coding for the SSU postfixed in 1% osmium tetroxide in the same buffer for 1 h rRNA was amplified using several primer combinations to in the dark, washed in distilled water and stained in 1% cover the whole gene (Gargas and Taylor 1992). The PCR aqueous uranyl acetate for 1 h in the dark. After five products were purified using the QIAquick protocol washes in distilled water, samples were dehydrated in (Qiagen). The dsDNA was directly sequenced using an acetone, using 10-min changes at 25, 50, 70, 95% and ABI PRISM Dye-Termination Cycle Sequencing Kit three times in 100% acetone. Samples were embedded in (Applied Biosystems) on automated sequencers (ABI Spurr’s plastic and sectioned with a diamond knife. 373A and ABI 3100, Applied Biosystems). The sequences Ultrathin serial sections were mounted on formvar-coated, were manually edited and assembled with Sequencher 4.1 single-slot copper grids, stained with lead citrate at room (Gene Codes Corporation). temperature for 5 min, and washed with distilled water. The first data set consisted of LSU sequences of 87 They were examined using a Zeiss transmission electron species of simple-septate basidiomycetes and three asco- microscope operating at 80 kV. mycetes as outgroup. The second set combined partial LSU For high-pressure freezing and freeze substitution, and nearly complete SSU sequences of 61 basidiomycetes samples were removed with a 2-mm cork borer. To remove and three ascomycetes as outgroup. For both data sets, we air from intercellular spaces, samples were infiltrated with followed a multiple-analysis strategy (Lee 2001) and distilled water containing 6% (v/v) (2.5 M) methanol for aligned the sequences with four different alignment meth- approximately 5 min at room temperature. Single samples ods and programs, namely, DIALIGN 2.2.1, using the −n were placed in an aluminum holder (one half with a hollow option (Morgenstern 1999); MAFFT, using the FFT-NS-i of 0.3 mm depth for the sample and the other with a flat option (Katoh et al. 2002); MUSCLE 3.2 (Edgar 2004); and top) and frozen immediately in the high-pressure freezer POA (Lee et al. 2002). For the combined analysis of LSU HPM 010 (Balzers Union, Lichtenstein) as described in and SSU sequences, each region was aligned separately. detail by Mendgen et al. (1991). Substitution medium The different alignments of the first data set were then (1.5 ml per specimen) consisted of 2% osmium tetroxide in analyzed according to different methods of phylogenetic acetone, which was dried over calcium chloride. Freeze reconstruction. Positions where most sequences contained substitution was performed at −90, −60 and −30°C (8 h for leading or trailing gaps were excluded before inferring each step) using a Balzers freeze substitution apparatus phylogenetic trees. For neighbor-joining analysis (Saitou (FSU 010). The temperature was then raised to approxi- and Nei 1987), the data were first analyzed with Modeltest mately 0°C over a 30-min period, and samples were version 3.04