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Early Diverging Ascomycota: Phylogenetic Divergence and Related Evolutionary Enigmas

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Early Diverging Ascomycota: Phylogenetic Divergence and Related Evolutionary Enigmas Mycologia, 98(6), 2006, pp. 996–1005. # 2006 by The Mycological Society of America, Lawrence, KS 66044-8897 Early diverging Ascomycota: phylogenetic divergence and related evolutionary enigmas Junta Sugiyama1 Key words: basal Ascomycota, classification, Tokyo Office, TechnoSuruga Co. Ltd., Ogawamachi evolution, molecular phylogeny Kita Building 4F, Kanda Ogawamachi 1-8-3, Chiyoda- ku, Tokyo 101-0052, Japan INTRODUCTION Kentaro Hosaka Department of Botany, The Field Museum, 1400 S. The ascomycete subphylum Taphrinomycotina sensu Lake Shore Drive, Chicago, Illinois 60605-2496 Eriksson and Winka (1997) was based on the pro- Sung-Oui Suh visional class ‘‘Archiascomycetes’’ proposed by Nishida and Sugiyama (1993, 1994b). The taxon was Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana 70803 based on nuclear small subunit (nSSU) rDNA sequence analyses, and it is an assemblage of the diverse early diverging Ascomycota. The group Abstract: The early diverging Ascomycota lineage, includes taxa that have been central to evolutionary detected primarily from nSSU rDNA sequence-based theories concerning the origin of the Ascomycota and phylogenetic analyses, includes enigmatic key taxa Basidiomycota. Among numerous phylogenetic hy- important to an understanding of the phylogeny and potheses one by Savile (1955, 1968) on the phylogeny evolution of higher fungi. At the moment six of higher fungi has attracted the attention of representative genera of early diverging ascomycetes mycologists for more than 50 y; it is a logical (i.e. Taphrina, Protomyces, Saitoella, Schizosaccharo- hypothesis based on phenotypic characters, particu- myces, Pneumocystis and Neolecta) have been assigned larly those of comparative morphology (Kramer 1987, to ‘‘Archiascomycetes’’ sensu Nishida and Sugiyama Sugiyama and Nishida 1995, Sugiyama 1998, Kurtz- (1994) or the subphylum ‘‘Taphrinomycotina’’ sensu man and Sugiyama 2001). Savile (1955, 1968) pro- Eriksson and Winka (1997). The group includes fungi posed that Taphrina Fr. represented an early di- that are ecologically and morphologically diverse, and vergence within the higher Fungi (i.e. the present-day it is difficult therefore to define the group based on Taphrina was the closest survivor of ‘‘Prototaphrina,’’ common phenotypic characters. Bayesian analyses of a hypothetical genus and common ancestor of the nSSU rDNA or combined nSSU and nLSU rDNA Ascomycota and Basidiomycota). One major lineage sequences supported previously published Ascomy- led to the present day Taphrina and the Ascomycota, cota frameworks that consist of three major lineages whereas another line led to the Basidiomycota (i.e. (i.e. a group of early diverging Ascomycota [Taphri- the Uredinales line and the parasitic Auriculariaceae nomycotina], Saccharomycotina and Pezizomyco- via a ‘‘Protobasidiomycete’’). Cavalier-Smith (1987) tina); Taphrinomycotina is the sister group of proposed another hypothesis on the basis of ultra- Saccharomycotina and Pezizomycotina. The 50% structural and molecular (5S ribosomal RNA se- majority rule consensus of 18 000 Bayesian quences) data; he suggested that the Taphrinomy- MCMCMC-generated trees from multilocus gene cetes (including Taphrinales, Schizosaccharo- sequences of nSSU rDNA, nLSU rDNA (D1/D2), mycetales and Protomycetales) evolved independent- RPB2 and b-tubulin also showed the monophyly of ly from a Saccharomycetes-Mucorales-Entomophtho- the three subphyla and the basal position of rales group by the total loss of chitin, and he placed Taphrinomycotina in Ascomycota with significantly the Taphrinomycetes and Saccharomycetes in the higher statistical support. However to answer contro- phylum Endomycota. Cavalier-Smith (2001) subse- versial questions on the origin, monophyly and quently accommodated the Taphrinomycetes and evolution of the Taphrinomycotina, additional in- Saccharomycetes as classes within the Hemiascomy- tegrated phylogenetic analyses might be necessary cotina. The existence of chitinous walls in species of using sequences of more genes with broader taxon Taphrina (Nishida and Sugiyama 1994a, Nishida sampling from the early diverging Ascomycota. 2005) and Schizosaccharomyces (e.g. Bowen et al 1992) had been shown with molecular techniques and refuted a hypothesis based on loss of chitin. Accepted for publication 19 September 2006. Additional historical background on the phylogenetic 1 Corresponding author. E-mail: [email protected] and evolutionary theories related to Taphrina and the 996 SUGIYAMA ET AL:EARLY DIVERGING ASCOMYCOTA 997 TABLE I. Characteristics of the early diverging ascomycetes compared to other ascomycetes a, b Taphrinomycotina Schizosaccharo- Pneumo- Saccharomy- Pezizomy- Character Taphrina Protomyces Saitoella myces cystis Neolecta cotina cotina Lifestyle PP PP S S PA Sc S PP/S Culturable YES YES YES YES NO NO YES YES Ascoma 222 2 2 + 2 + Ascogenous hyphae 222 2 2 + 2 + Enveloping membrane I?2 IVVIV system Forcible ascospore +/2 +/22 2 2 + 2 +/2 discharge Anamorph Y Y Y Y ? ? Y H Woronin bodies ? ? 22 2++/2 + Simple septal pore + ? 22 2++/2 + Ploidy of somatic cells n+n 2n n n n/2n n n/2n n Major ubiquinone Q-10 Q-10 Q-10 Q-10 ? ? Q-6,9 Q-9, 10, system 10(H2), 10(H4) a Compiled from Alexopoulos et al (1996), Sugiyama (1998) and Landvik et al (2003). b Exceptional data are omitted. c N. vitellina is possibly a weak parasite on the host conifer, the ecology of three species is little known (Landvik et al 2001). Abbreviations 5 PP: phytopathogenic; PA: pathogenic for animals; S: saprobic; +: present; 2: lacking; ?: unknown or no data; I: associated with individual nuclei; V: enclosing all nuclei; Y: yeast/yeastlike; H: hyphal. definition and circumscription of the Taphrinomyco- attracted great interest from mycologists, centering tina were reviewed by Sugiyama and Nishida (1995), on the major question whether the early diverging Alexopoulos et al (1996), Sugiyama (1998) and ascomycetes comprise a monophyletic or a paraphy- Kurtzman and Sugiyama (2001). letic group. Eriksson (1999) first suggested that the As stated above Nishida and Sugiyama (1993, 1994b) subphylum might be paraphyletic, and subsequent initially treated their provisional class ‘‘Archiascomy- analyses have not resolved the question. A phylogeny cetes’’ as monophyletic, accommodating five genera based on the gene sequences encoding the second Taphrina, Protomyces, Saitoella, Schizosaccharomyces and largest subunit RNA polymerase II (RPB2, Liu et al Pneumocystis. The common characters of the five 1999) supported the view that the Ascomycota is genera are: (i) A sexually reproductive state (not composed of monophyletic groups of Taphrinomy- present in Saitoella) is ascogenous but ascogenous cotina (5Archiascomycetes), Saccharomycotina hyphae are not formed; (ii) asexual reproduction is by (5Saccharomycetes) and Pezizomycotina (5Euasco- budding or fission; (iii) neither ascomata nor con- mycetes); however only two early diverging species, idiomata are formed; and (iv) the vegetative state is Schizosaccharomyces pombe and Neolecta vitellina, were hyphal or yeast-like (TABLE I). On the basis of nSSU included in their study. On the other hand a phylog- rDNA sequence analyses Landvik et al (1993) and eny from b-tubulin genes (Landvik et al 2001) showed Landvik (1996) subsequently included the apothecial that the early diverging ascomycetes are not mono- ascomycete genus Neolecta in the early diverging phyletic but supported the hypotheses of an early ascomycete lineage defined by Berbee and Taylor divergence of Neolecta from superficially similar (1993, 1995), and Sjamsuridzal et al (1997) confirmed filamentous ascomycetes (5 euascomycetes). The the addition of Neolecta into the group based on the respective RPB2 and b-tubulin genes did not give same gene, thus causing an evolutionary enigma. a clear answer for the monophyly vs. paraphyly of the Characteristics of all the representative genera and Taphrinomycotina. Taxonomically de Hoog et al other ascomycete yeasts and filamentous ascomycetes (2000) and Sugiyama (2005) treated the group as are compared (TABLE I); these phenotypic characters the class Archiascomycetes in the phylum Ascomy- used to circumscribe the Taphrinomycotina are un- cota, in which the remaining phyla were Hemiasco- clear with the inclusion of Neolecta in the group. mycetes (ascomycetous yeasts) and Euascomycetes The discovery of Neolecta as a member of the (filamentous ascomycetes), corresponding to the already diverse early diverging ascomycetes has subphyla Taphrinomycotina, Saccharomycotina and 998 MYCOLOGIA Pezizomycotina, respectively (Eriksson and Winka Biological and cultural properties of Protomyces 1997, Eriksson 2005). Kirk et al (2001) reclassified inouyei, P. lactucae-debilis Sawada and P. pachydermus the early diverging ascomycetes into four classes, the von Thu¨men have been characterized by Tubaki Taphrinomycetes, Schizosaccharomycetes, Pneumo- (1957). nSSU rDNA sequence phylogeny demonstrat- cystidomycetes and Neolectomycetes. Eriksson (2005) ed that these three Protomyces spp. and P. macro- treated these as ‘‘classes of uncertain positions in the sporus Unger form a monophyletic group (Sjamsur- subphylum Taphrinomycotina’’ because of poor idzal et al 1997). In addition a core group comprising support for Taphrinomycotina as a monophyletic Taphrina (including T. vestergrenii) and Protomyces group, corresponding to the classification used in this spp. always appeared to be monophyletic with strong volume (Blackwell et al
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