Skip to main content
Log in

Evolutionary relationships of membrers of the generaTaphrina, Protomyces, Schizosaccharomyces, and related taxa within the archiascomycetes: Integrated analysis of genotypic and phenotypic characters

  • Original Papers
  • Published:
Mycoscience

Abstract

To study the phylogeny and evolution of archiascomycetes, we determined the full sequence of the nuclear 18S rRNA gene from 14Taphrina species and 2Protomyces species, and the partial sequence ofSchizosaccharomyces japonicus var.japonicus. The sequences were phylogenetically analyzed by the neighbor-joining, maximum parsimony, and maximum-likelihood methods. We also looked at their principal phenotypic characters and genotypic character. Relationships within the Ascomycota are concordant with the previously published phylogenies inferred from 18S rDNA sequence divergence and divide the archi-, hemi-and euascomycetes into distinct major lineages. All the trees show that, within the archiascomycete lineage, 11 of the 14Taphrina species and the 2Protomyces species are monophyletic. A core groups ofTaphrina andProtomyces is always monophyletic. The evidence from molecular and phenotypic characters such as cell wall sugar composition, ubiquinone, cell wall ultrastructure, and mode of conidium ontogeny, strongly suggests that ‘T’. californica CBS 374.39, ‘T’. maculans CBS 427.69 and ‘T’. farlowii CBS 376.39 should be excluded from the archiascomycete lineage. ‘Taphrina’ farlowii CBS 376.39 groups withCandida albicans in the Saccharomycetales, whereas ‘T’. californica CBS 374.39 and ‘T’. maculans CBS 427.69 have a basidiomycete affinity and group with Tremellalean members in the hymenomycete lineage.Schizosaccharomyces is monophyletic. The strictly anamorphic yeastSaitoella complicata groups with the apothecial ascomyceteNeolecta vitellina rather than theTaphrina/Protomyces branch.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Literature cited

  • Alexopoulos, C. J., Mims, C. W. and Blackwell, M. 1996. Introductory mycology, 4th ed. John Wiley & Sons, New York.

    Google Scholar 

  • Andres, D. A., Seabra, M. C., Brown, M. S., Armstrong, S. A., Smeland, T. E., Cremers, F. P. M. and Goldstein, J. L. 1993. cDNA cloning of component A of rab geranylgeranyl transferase and demonstration of its role as a rab escort protein. Cell73: 1091–1099.

    Article  PubMed  CAS  Google Scholar 

  • Barnett, J. A., Payne, R. W. and Yarrow, D. 1990. Yeasts: Characteristics and identification, 2nd ed. Cambridge Univ. Press, Cambridge.

    Google Scholar 

  • Berbee, M. L. and Taylor, J. W. 1993. Dating the evolutionary radiations of the true fungi. Can. J. Bot.71: 1114–1127.

    Google Scholar 

  • Cronquist, A. 1988. The evolution and classification of flowering plants, 2nd ed. The New York Botanical Garden, New York.

    Google Scholar 

  • Delanoë, P. and Delanoë, M. 1912. Sur les rapports des kystes de Carini du poumon des rats avec leTrypanosoma lewisi. C.R. Acad. Sci. Paris155: 658–660.

    Google Scholar 

  • Edman, J. C., Kovacs, J. A., Masur, H., Santi, D. V., Elwood, H. J. and Sogin, M. L. 1988. Ribosomal RNA sequence showsPneumocystis carinii to be a member of the fungi. Nature334: 519–522.

    Article  PubMed  CAS  Google Scholar 

  • Eriksson, O. E. 1994.Pneumocystis carnii, a parasite in lungs of mammals, referred to a new family and order (Pneumocystidaceae, Pneumocystidales, Ascomycota). Systema Ascomycetum13: 165–180.

    Google Scholar 

  • Eriksson, O. E. 1995. DNA and ascomycete systematics. Can. J. Bot.73 (Suppl. 1): S784-S789.

    CAS  Google Scholar 

  • Eriksson, O. E. and Hawksworth, D. L. 1995. Notes on ascomycete systematics-Nos 1885–2023. Systema Ascomycetum14: 41–77.

    Google Scholar 

  • Eriksson, O. E., Svedskog, A. and Landvik, S. 1993. Molecular evidence for the evolutionary hiatus betweenSaccharomyces cerevisiae andSchizosaccharomyces pombe. Systema Ascomycetum11: 119–162.

    Google Scholar 

  • Felsenstein, J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol.17: 368–376.

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution39: 783–791.

    Article  Google Scholar 

  • Felsenstein, J. 1993. PHYLIP (Phylogeny Inference Package) version 3.5c. Distributed by the author. Department of Genetics, University of Washington, Seattle, USA.

    Google Scholar 

  • Gams, W. and von Arx, J. A. 1980. Validation ofSymbiotaphrina (imperfect yeasts). Persoonia10: 542–543.

    Google Scholar 

  • Goto, S. and Sugiyama, J. 1970. Studies on Himalayan yeasts and moulds. IV. Several asporogenous yeasts including two new taxa ofCryptococcus. Can. J. Bot.48: 2097–2101.

    Google Scholar 

  • Goto, S., Sugiyama, J., Hamamoto, M. and Komagata, K. 1987.Saitoella, a new anamorphic genus in the Cryptococcaceae to accommodate two Himalayan yeast isolates formally identified asRhodotorula glutinis. J. Gen. Appl. Microbiol.33: 75–85.

    Google Scholar 

  • Hasegawa, T., Takizawa, M. and Tanida, S. 1983. A rapid analysis for chemical grouping of aerobic actinomycetes. J. Gen. Appl. Microbiol.29: 319–322.

    CAS  Google Scholar 

  • Hawksworth, D. L., Kirk, P. M., Sutton, B. C. and Pegler, D. N. 1995. Ainsworth & Bisby's dictionary of the fungi, 8th ed. C.A.B. International, Wallingford.

    Google Scholar 

  • Heath, I. B., Ashton, M. L. and Kaminskyi, S. G. W. 1987. Mitosis as a phylogenetic marker among the yeasts: review and observations on novel mitotic systems in freeze substituted cells of the Taphrinales. In: The expanding realm of yeast-like fungi, (ed. by de Hoog, G. S., Smith, M. T. and Weijman, A. C. M.), pp. 279–297. Elsevier, Amsterdam.

    Google Scholar 

  • Heath, I. B., Ashton, M. L., Rethoret, K. and Heath, M. C. 1982. Mitosis and the phylogeny ofTaphrina. Can. J. Bot.60: 1696–1725.

    Google Scholar 

  • Jones, K. G. and Blackwell, M. 1996. Ribosomal DNA sequence analysis places the yeast-like genusSymbiotaphrina within filamentous ascomycetes. Mycologia88: 212–218.

    CAS  Google Scholar 

  • Kimura, M. 1980. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol.16: 111–120.

    Article  PubMed  CAS  Google Scholar 

  • Korf, R. P. 1973. Discomycetes and Tuberales. In: The fungi, vol. 4A, (ed. by Ainsworth, G. C., Sparrow, F. K. and Sussman, A. S.), pp. 249–319. Academic Press, New York.

    Google Scholar 

  • Kramer, C. L. 1973. Protomycetales and Taphrinales. In: The fungi, vol. 4A, (ed. by Ainsworth, G. C., Sparrow, F. K. and Sussman, A. S.), pp. 33–41. Academic Press, New York.

    Google Scholar 

  • Kramer, C. L. 1987. The Taphrinales. In: The expanding realm of yeast-like fungi, (ed. by de Hoog, G. S., Smith, M. T. and Weijman, A. C. M.), pp. 151–166. Elsevier, Amsterdam.

    Google Scholar 

  • Kreger-van Rij., N. J. W. (ed.) 1984. The yeasts, a taxonomic study, 3rd ed. Elsevier, Amsterdam.

    Google Scholar 

  • Kuraishi, H., Katayama-Fujimura, Y., Sugiyama, J. and Yokoyama, T. 1985. Ubiquinone systems in fungi I. Distribution of ubiquinones in the major families of ascomycetes, basidiomycetes, and deuteromycetes, and their taxonomic implications. Trans. Mycol. Soc. Japan26: 383–395.

    Google Scholar 

  • Kuraishi, H., Sugiyama, J. and Yamada, Y. 1991. Distribution of ubiquinone systems in fungi. Bull. JFCC7: 111–133.

    Google Scholar 

  • Kurtzman, C. P. 1993. Systematics of the ascomycetous yeasts assessed from ribosomal RNA sequence divergence. Antonie van Leeuwenhoek63: 165–174.

    Article  PubMed  CAS  Google Scholar 

  • Kurtzman, C. P. and Robnett, C. J. 1991. Phylogenetic relationships among species ofSaccharomyces, Schizosaccharomyces, Debaryomyces andSchwaniomyces determined from partial ribosomal RNA sequence. Yeast7: 61–72.

    Article  PubMed  CAS  Google Scholar 

  • Kurtzman, C. P. and Robnett, C. J. 1994. Orders and families of ascosporogenous yeasts and yeast-like taxa compared from ribosomal RNA sequence similarities. In: Ascomycete systematics: Problems and perspectives in the nineties, (ed. by Hawksworth, D. L.), pp. 249–258. Plenum Press, New York.

    Google Scholar 

  • Landvik, S. 1996.Neolecta, a fruit-body-producing genus of the basal ascomycetes, as shown by SSU and LSU rDNA sequences. Mycol. Res.100: 199–202.

    CAS  Google Scholar 

  • Landvik, S., Eriksson, O. E., Gargas, A. and Gustafsson, P. 1993. Relationships of the genusNeolecta (Neolectales ordo nov., Ascomycotina) inferred from 18S rDNA sequences. Systema Ascomycetum11: 107–118.

    Google Scholar 

  • Mesbah, M., Premachandran, U. and Whitman, W. B. 1989. Precise measurement of the G+C content of deoxyribonucleic acid by high-performance liquid chromatography. Int. J. Syst. Bacteriol.39: 159–167.

    Article  CAS  Google Scholar 

  • Minet, M., Nurse, P., Thuriaux, P. and Mitchison. 1979. Uncontrolled septation in a cell division cycle mutant of the fission yeastSchizosaccharomyces pombe. J. Bacteriol.137: 440–446.

    PubMed  CAS  Google Scholar 

  • Mix, A. J. 1949. A monograph of the genusTaphrina. Univ. Kansas Sci. Bull.33: 1–167.

    Google Scholar 

  • Moore, R. T. 1990. The genusLalaria gen. nov.: Taphrinales anamorphosum. Mycotaxon38: 315–330.

    Google Scholar 

  • Moore, R. T. and Flinn, A. M. 1991. Ubiquinone and urease distribution inTaphrina andSymbiotaphrina. Antonie van Leeuwenhoek59: 45–47.

    Article  PubMed  CAS  Google Scholar 

  • Naehring, J., Kiefer, S. and Wolf, K. 1995. Nucleotide sequence of theSchizosaccharomyces Japonicus var.versatilis ribosomal RNA gene cluster and its phylogenetic implications. Curr. Genet.28: 353–359.

    Article  PubMed  CAS  Google Scholar 

  • Nishida, H. and Sugiyama, J. 1993. Phylogenetic relationships amongTaphrina, Saitoella, and other fungi. Mol. Biol. Evol.10: 431–436.

    PubMed  CAS  Google Scholar 

  • Nishida, H. and Sugiyama, J. 1994. Archiascomycetes: detection of a major new lineage within the Ascomycota. Mycoscience35: 361–366.

    Article  Google Scholar 

  • Nishida, H., Blanz, P. A. and Sugiyama, J. 1993. The higher fungusProtomyces inouyei has two group I introns in the 18S rRNA gene. J. Mol. Evol.37: 25–28.

    Article  PubMed  CAS  Google Scholar 

  • Nishida, H., Tajiri, Y. and Sugiyama, J. 1997. Multiple origins of fungal group I introns located in the same position of nuclear SSU rRNA gene. J. Mol. Evol. (In press.)

  • Noda, H. and Kodama, K. 1996. Phylogenetic position of yeastlike endosymbionts of Anobiid beetles. Appl. Environ. Microbiol.62: 162–167.

    PubMed  CAS  Google Scholar 

  • Prillinger, H., Dorfler, Ch., Laaser, G., Eckerlein, B. and Lehle, L. 1990. Ein Betrag zur Systematik und Entwicklungsbiologie Hoherer Pilze: Hefe-Typen der Basidiomyceten, Teil I: Schizosaccharomycetales,Protomyces-Typ. Z. Mykol.56: 219–250.

    Google Scholar 

  • Prillinger, H., Oberwinkler, F., Umile, C., Tlachac, K., Bauer, R., Dorfler, C. and Taufrathofer, E. 1993. Analysis of cell wall carbohydrates (neurtral sugars) from ascomycetous and basidiomycetous yeasts with and without derivation. J. Gen. Appl. Microbiol.39: 1–34.

    CAS  Google Scholar 

  • Reddy, M. S. and Kramer, C. L. 1975. A taxonomic revision of the Protomycetales. Mycotaxon3: 1–50.

    Google Scholar 

  • Redhead, S. A. 1977. The genusNeolecta (Neolectaceae fam. nov., Lecanorales, Ascomycetes) in Canada. Can. J. Bot.55: 301–306.

    Article  Google Scholar 

  • Saiki, R. K., Gelfand, D. H., Stoffel, S., Scharf, S. J., Higuchi, R., Horn, G. T., Mullis, K. B. and Erlich, H. A. 1988. Primerdirected enzymatic amplification of DNA with a thermotable DNA polymerase. Science239: 487–491.

    PubMed  CAS  Google Scholar 

  • Saitou, N. and Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol.4: 406–425.

    PubMed  CAS  Google Scholar 

  • Sugiyama, J. and Nishida, H. 1994. Phylogenetic divergence of Taphrinalean fungi: Evidence from molecules and morphology. Fifth Int. Mycol. Congr., Vancouver, Canada, August 14–21, p. 213.

  • Sugiyama, J. and Nishida, H. 1995. The higher fungi: their evolutionary relationships and implications for fungal systematics. In: Biodiversity and evolution, (ed. by Arai, R., Kato, M. and Doi, Y), pp. 177–195. The National Science Museum Foundation, Tokyo.

    Google Scholar 

  • Sugiyama, J., Nagahama, T. and Nishida, H. 1996a. Fungal diversity and phylogeny with emphasis on 18S ribosomal DNA sequence divergence. In: Microbial diversity in time and space, (ed. by Colwell, R. R., Simidu, U. and Ohwada, K.), pp. 41–51. Plenum Press, New York.

    Google Scholar 

  • Sugiyama, J., Nishida, H. and Suh, S-O. 1993. The paradigm of fungal diagnoses and descriptions in the era of molecular systematics:Saitoella complicata as an example. In: The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics, (ed. by Reynolds, D. R. and Taylor, J. W.), pp. 261–269. C.A.B. International, Wallingford.

    Google Scholar 

  • Sugiyama, J., Fukagawa, M., Chiu, S-W. and Komagata, K. 1985. Cellular carbohydrate composition, ubiquinone systems, and Diazonium Blue B color test in the generaRhodosporidium, Leucosporidium, Rhodotorula, and related basidiomycetous yeasts. J. Gen. Appl. Microbiol.31: 519–550.

    CAS  Google Scholar 

  • Sugiyama, J., Tajiri, Y., Sjamsuridzal, W. and Nishida, H. 1996b. Phylogeny and evolution of archiascomycetes as yeasts. Ninth Int. Symp. on Yeasts, Sydney, Australia, August 25–30, p. 9.

  • Suh, S.-O., Hirata, A., Sugiyama, J. and Komagata, K. 1993. Septal ultrastructure of basidiomycetous yeasts and their taxonomic implication with observations on the ultrastructure ofErythrobasidium hasegawianum andSympodiomycopsis paphiopedili. Mycologia85: 30–37.

    Google Scholar 

  • Swofford, D. L. 1993. PAUP: Phylogenetic analysis using parsimony, version 3.1. Illinois Natural History Survey, Champaign, Illinois.

    Google Scholar 

  • Taylor, J. W. and Bowman, B. H. 1993.Pneumocystis carinii and the ustomycetous red yeast fungi. Mol. Microbiol.8: 425–426.

    PubMed  CAS  Google Scholar 

  • Taylor, J. W., Swann, E. C. and Berbee, M. L. 1994. Molecular evolution of ascomycete fungi: Phylogeny and conflict. In: Ascomycete systematics: Problems and perspectives in the nineties, (ed. by Hawksworth, D. L.), pp. 201–212. Plenum Press, New York.

    Google Scholar 

  • Thompson, J. D., Higgins, D. G. and Gibson, T. J. 1994. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position spoecific gap penalties and weight matrix choice. Nucleic Acids Res.22: 4673–4680.

    PubMed  CAS  Google Scholar 

  • Tubaki, K. 1957. Biological and cultural studies of three species ofProtomyces. Mycologia49: 44–54.

    Google Scholar 

  • Vancanneyt, M., Coopman, R., Tytgat, R., Berny, J. F., Hennebert, G. L. and K. Kersters. 1992. A taxonomic study of the basidiomycetous yeast generaRhodosporidium Banno andRhodotorula Harrison based on whole cell protein patterns, DNA base composition and coenzyme Q types. J. Gen. Appl. Microbiol.38: 363–377.

    CAS  Google Scholar 

  • van Eijk, G. W. and Roeymans, H. J. 1982. Distribution of carotenoids and sterols in relation to the taxonomy ofTaphrina andProtomyces. Antonie van Leeuwenhoek48: 257–264.

    Article  PubMed  Google Scholar 

  • von Arx, J. A. 1981. The genera of fungi sporulating in pure culture, 3rd ed. J. Cramer, Lehre.

    Google Scholar 

  • Wakefield, A. E., Hopkin, J. M., Bridge, P. D. and Hawksworth, D. L. 1993.Pneumocystis carinii and the ustomycetous red yeast fungi. Mol. Microbiol.8: 426–427.

    CAS  Google Scholar 

  • Yamada, Y. and Banno, I. 1987.Hasegawaea gen. nov., an ascosporogenous yeast genus for the organisms whose asexual reproduction is by fission and whose ascospores have smooth surfaces without papillae and which are characterized by the absence of coenzyme Q and by the preseace of linoleic acid in cellular fatty acid composition. J. Gen. Appl. Microbiol.33: 295–298.

    CAS  Google Scholar 

  • Yamada, Y. and Kondo, K. 1972. Taxonomic significance of coenzyme Q system in yeasts and yeast-like fungi. In: Yeasts, models in science and technics, (ed. by Kocková-Kratochvilová, A. and Minárik, E.), pp. 363–373. House of Slovak Academy of Science, Bratislava.

    Google Scholar 

  • Yamada, Y., Ohishi, T. and Kondo, K. 1983. The coenzyme Q system in strains of some yeasts and yeast-like fungi. J. Gen. Appl. Microbiol.29: 51–57.

    CAS  Google Scholar 

  • Yamada, Y., Asahi, T., Maeda, K. and Mikata, K. 1993. The phylogenetic relationships of fission yeasts based on the partial sequences of 18S and 26S ribosomal RNAs: the recognition ofHasegawaea Yamada et Banno along withSchizosaccharomyces Lindner. Bull. Fac. Agric. Shizuoka43: 29–38.

    CAS  Google Scholar 

  • Yamada, Y., Banno, I., von Arx, J. A. and van der Walt, J. P. 1987. Taxonomic significance of the coenzyme Q system in yeasts and yeast-like fungi. In: The expanding realm of yeast-like fungi, (ed. by de Hoog, G. S., Smith, M. T. and Weijman, A. C. M.), pp. 299–308. Elsevier, Amsterdam.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Junta Sugiyama.

About this article

Cite this article

Sjamsuridzal, W., Tajiri, Y., Nishida, H. et al. Evolutionary relationships of membrers of the generaTaphrina, Protomyces, Schizosaccharomyces, and related taxa within the archiascomycetes: Integrated analysis of genotypic and phenotypic characters. Mycoscience 38, 267–280 (1997). https://doi.org/10.1007/BF02464084

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02464084

Key Words

Navigation