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Phylogenetic Studies on Nuclear Large Subunit Ribosomal DNA Sequences of Smut Fungi and Related Taxar

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Phylogenetic Studies on Nuclear Large Subunit Ribosomal DNA Sequences of Smut Fungi and Related Taxar 2045 Phylogenetic studies on nuclear large subunit ribosomal DNA sequences of smut fungi and related taxar Dominik Begerow, Robert Bauer, and Franz Oberwinkler Abstract: To show phylogenetic relationships among the smut fungi and thcir relatives. we sequenced a part of the nuclear LSU rDNA from 43 different species of smut fungi and related taxa. Our data were combined with the existing sequences of seven further smut fungi and 17 other basidiomycetes. Two sets of sequences were analyzed. The first set with a representative number of simple septate basidiomycetes, complex scptate basidiomycetes, and smut fungi was analyzed with the neighbor-joining method to estimate the general topology of the basidiomycetes phylogeny and the positions of the smut fungi. The tripartite subclassification of the basidiomycetes into the Urediniomycetes, Ustilaginomycetes, and Hymcnomycetes was confirmed and two groups of smut fungi appeared. Thc smut genera Aurantiosporiurn, Microbotrl-unr, Fulvisporium, and Ustilentr-loma are members of the Urediniomycetes, whereas the other smut species tested are members of the Ustilaginomycetes wrth Entorrhiz.a as a basal taxon. The second set of 46 Ustilaginomycetes was analyzed using the neighbor-joining and the maximum parsimony methods to show the inner topology of the Ustilaginomycetes. The results indicated three major lineages among Ustilaginomycetes corresponding to the Entorrhizomycetidae, Exobasidiomycetidae, and Ustilaginomycetidae. The Entorrhizomycetidae are represented by Entorrhiza species. The Ustilaginomycctidae contain at least two groups, thc Urocystales and Ustilaginales. The Exobasidiomycetidae include five orders, i.e., Doassansiales, Entylomatales, Exobasidiales. Georgefischeriales. and Tilletiales, and Graphiola phoenicis and Microstroma juglandis. Our results support a classification mainly based on ultrastructure. The description of the Glomosporiaceae is emended. The Doassansiopsaceae, Mclanotaeniaceae, and Urocystaceae are proposed as new taxa. Key words'. basidiomycete systematics, LSU rDNA. Microbotryales, molecular phylogeny, smut fungi, Ustilaginomycetes. Rdsumd : Afin de ddmontrer les relations phylogdndtiques parmi les champignons du charbon et espöces apparentdes, les auteurs ont s6quenc6 une partie de la grande sous-unitd nucl6aire de 1'ADN ribosomique (LSU rDNA), chez 43 espöces dilTdrentes de champignons du charbon et taxons apparentds. Les donn6es ont 6td combin6es avec les s6quences d6jä connues de sept champignons du charbon et 17 autres basidiomycötes. Ils ont analysd deux groupes de s6quences. Le premier comporte un nombre repr6sentatif de basidiomycötes ä septations simples, de basidiomycötes ä septations complexes et de champignons du charbon, en utilisant la mdthodc de jonction avec les voisins pour estimer la topologie gönd,rale de la phylogdnie des basidiomycötes et les positions des champignons du charbon. La subclassification tripartite des basidiomycötes en Ur6dinomycötes, Ustilagoinomycötes et Hymdnomycötes est confirm6e et on ddtecte deux groupes de champignons du charbon. Les champignons du charbon des genres Aurantiosporiunt, Microbotn'tnt, Fulvisporium et Ustilent,,-loma sont membres des Ur6dinomycötes, alors que les autres espöces examin6es sont membres des Ustilaginomycötes, les Entorrhiz,a 6tant le taxon de base. Le second groupc de 46 Ustilaginomycötes a 6t6 analysd cn utilisant les m6thodes de jonction avec les voisins et de parscimonie maximum pour illustrer la topologie interne des Ustilaginomycdtes. Les rdsultats montrent trois lign6es majeures parmi lcs Ustilaginomycötcs, lesquellcs corrcspondent aux Entorrhizomycetidae, Exobasidiomycetidae et Ustilaginomycetidae. Les Entorrhizomycetidae sont repr6sent6s par les espöces d'Entorrhizo. Les Ustilaginomycetidae contiennent au moins deux groupes, les Urocystales et les Ustilaginales. Les Exobasidiomycetidae comportent cinq ordres, i.e., Doassansiales, Entylomatales, Exobasidiales, Georgefischeriales et Tilletiales ainsi quc le Graphiola phoenicis et le Microstroma .juglandis. Les r6sultats des auteurs supportent la classification basde principalement sur les ultrastructures. La description des Glomosporiaceae est amendde et les auteurs proposent les Doassansiopsaceae, les Melanotaeniaceae et les Urocystaceae comme nouveaux taxons. Mots c'lds : systdmatique des basidiomycötes, LSU rDNA, Microbotryales, phylogdnie mol6culaire. champignons du charbon, Ustilaginomycötes. [Traduit par la r6daction] Rcceived February 3, 1997. D. Begerow,2 R. Bauer, and F. Oberwinkler. Universität Tübingen, Institut für Biologie I, Lehrstuhl Spezielle Botanik und Mykologie, Auf der Morgenstelle I, D-'72076 Tübingen, Germany. I Part 141 of the series "studies in Heterobasidiomycetes". 2 Author to whom all correspondence should be addressed. e-mail: dominik.begerow@uni+uebingcn.de Can. J. Bot. 75:2045-2056 (19911 '9 1997 NRC Canada 2046 Can. J Bot Vol. 75,1997 lntroduction of 1000 replicates using SeqBoot and Consens of thc euvlte pack- age with defäult parameters (Felsenstcin 1993). Maxrmum parsi- A new system of smut fungi and allied taxa based on ultra- mony analysis was perforned by DNApars (urnble option: 100) structural studies was recently proposed by Bauer et al. (1997). and Consens. The alignments are available upon request. This system differs significantly from the traditional classifi- cation characterized by a basic dichotomy separating the Results phragmobasidiate Ustilaginaceae or Ustilaginales fionr the Sequence alignments holobasidiate Tilletiaceae or Tilletiales (e.g., Tulasne and Two sets of sequences were analyzed for phylogenetic dis- Tulasne 1847: Oberwinkler 1977, 1987). In the system of cussion of smut fungi and allied taxa. The flrst set with Bauer et al. (1997) six genera of smut fungi are grouped in sequences of 30 basidiomlicetes was analyzed to deterrnine the Microbotryales, whereas the other smut fungi are placed the general topology of the basidiomycetes, the positions of together with the Exobasidiales, Graphiolales. and Micro- smut fungi within this basidiomycetous topology and the root stromatales in the Ustila-einomycetcs. Owing to the profound of the Ustilaginomycetes. The second set with sequences of differences between traditional concepts and the systcm pro- 46 species was used to show the phylogenetic relationships posed Bauer et (1997), studies with independent by al. within the Ustilaginomycetes. The total consensus length of markers are required to test the classitications and to develop the first set was 518 bp, whereas the second set was 521 bp phylogenetic hypotheses. long. Although two small regions, positions 15-28 and Analyses of molecular sequence data have made impor- 465-413 of the alignment in the first set, 33-45 and462- tant contributions to the understanding of basidiomycetc 47 1 in the second set, respectively, included several ambigu- phylogeny (e.g., Berbee and Taylor 1993; Swann and Taylor ous positions owing to gap position. any manipulations were 1993, 1995; Berres et al. 1995; Boekhout et al. 1995). avoided to achieve highest reproducibility. Unfortunately. sequence data from smut fungi are available (Blanz only from a f'ew species and Gottschalk 1984; Swann Phylogenetic analysis of the first set and Taylor 1993, 1995; Boekhout et al. 1995; Berres et al. We analyzed a representative number of simple septate 1995). However. the previous results indicated the existence basidiomycetes, complex septate basidiomycetes. and smut of two distantly related groups of smut fungi. Because the fungi with allied taxa. Results of neighbor-joining analysis existing molecular sequence data base is too small to identify are shown in Fig 1. The three previously recognized classes natural groups among the smut fungi, we sequenced the 5' of basidiomycetes were confirmed. It was not the aim of this (LSU end of the large subunit of ribosomai DNA rDNA) of paper to study the origin of basidiomycetes. Analyses with presumptiveiy related species as a 38 smut fungi and five severai ascomycetes and zygorttycetes as outgroups led to (Qu Bruns et 1991) to semiconserved region et al. 1988; al. different arrangements of the three groups a-nd Entorrhi«t validate the system proposed by Bauer et al. (1997). Data was not always included in the Ustilaginomycetes (data not sets were completed with the sequences of seven further smut shown). Thus. the origin of basidiomycetes must be placed literature. fungi and l7 other basidiomycetes from somewhere close to the basal trifurcation. The first group, representing the Hymenomycetes, contains the heterobasid- Materials and methods iomycetes Tremella mesentericcr, Calocera liscosa, and Aurictrlaria auricula-jutlae, and the homobasidiomycetes Species studied for molecular analysis are listed in Tablc 1. DNA Ga nod e rm a mi c r o sp onon, Rus sul a mai r ei, B ol e t Lr s ntbine I I trs . was isolated from cultures or herbarium specimens fbllowing a Cortinarius stuntzii, Marasmius delectans. and Ag(tricLts modified version of the SDS method of Edwards ct al. (1991) and Henrion ct al. (1992): sanrples were ground in liquid nitrogen and arvensis. The second lineage representing the Urediniomy- incubated in 500 prl cxtraction buffer, tbr I h at 65"C. Thc extracts cetes is composed of the rusts (Melctmpsora lini, Put:c'inio werc centrifuged at 13.793 x g for 15 min and the supernatant was gruminis, and Puccinia recondita) together with some related transferred to a new Eppendorf tubc. RNA was digested with 10 U fungi (.Helicobasidium mompa, Eocronartium
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