Skip to main content

Advertisement

SpringerLink
Log in

Nucleotide sequence of the Schizosaccharomyces japonicus var. versatilis ribosomal RNA gene cluster and its phylogenetic implications

  • Original Paper
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

Fission yeasts form a small but heterogeneous group of ascomycetes and it is still unclear whether they should be subdivided into three genera (Schizosaccharomyces, Octosporomyces, Hasegawaea) or remain a single genus (Schizosaccharomyces). In order to decide whether a new genus Hasegawaea should be established for the species Schizosaccharomyces japonicus and Schizosaccharomyces versatilis, we have characterized the entire rDNA cluster in Schizosaccharomyces japonicus var. versatilis and compared it with the homologous region from Schizosaccharomyces pombe and with complete rRNA gene sequences from other yeast genera. From a phage genomic library a recombinant lambda phage containing the entire rDNA repeat unit was isolated. In this paper we report the primary sequence of the 18s, 5.8s and 25s rRNA coding regions. The S. japonicus var. versatilis rRNA genes are 1823 (18s), 158 (5.8s) and 3422 (25s) nucleotides long. The two sequences of the larger rRNA genes exhibit 95.7% (18s) and 93% (25s) similarity with the homologous genes from S. pombe. The differences between the rRNA genes of S. japonicus and S. pombe, however, are much smaller than the intrageneric differences within the rDNA sequences of other yeast genera. Therefore, subdivision of fission yeasts into the genera Schizosaccharomyces and Hasegawaea does not to seem to be justified. The sequence has been deposited in the EMBL data bank under the accession number Z 32848.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (1992) Current protocols in molecular biology. John Wiley and Sons, New York

    Google Scholar 

  • Barnitz JT, Cramer JH, Rownd RH, Cooley L, Söll D (1982) Arrangement of the ribosomal RNA genes in Schizosaccharomyces pombe. FEBS Lett 143:129–132

    Google Scholar 

  • Beijerinck AW (1894) Schizosaccharomyces octosporus, eine achtsporige Alkoholhefe. Zentralbl Bakteriol Parasitenk 16:49–58

    Google Scholar 

  • Benson S, Taylor RK (1984) A rapid small-scale procedure for isolation of phage lambda DNA. Biotechniques 2:126–127

    Google Scholar 

  • Berbee ML, Taylor JW (1992) Detecting morphological convergence in true fungi, using 18s rRNA gene-sequence data. Biosystems 28:117–125

    Google Scholar 

  • Bridge PD, May JW (1984) A numerical classification of fission yeasts of the genus Schizosaccharomyces Lindner. J Gen Microbiol 132:1921–1932

    Google Scholar 

  • Brosius J, Palmer ML, Poindexter JK, Noller HF (1978) The complete nucleotide sequence of a 16s ribosomal RNA gene from Escherichia coli. Proc Natl Acad Sci USA 75:4801–4805

    Google Scholar 

  • Campbell GR (1974) Methods of numerical taxonomy for various genera of yeasts. Adv Appl Microbiol 17:135–156

    Google Scholar 

  • Carbon P, Ehresmann C, Ehresmann B, Ebel JP (1979) The complete nucleotide sequence of the ribosomal 16s rRNA from Escherichia coli. Eur J Biochem 100:399–410

    Google Scholar 

  • Cedergren R, Gray MW, Abel Y, Sankoff D (1988) The evolutionary relationships among known life forms. J Mol Evol 28:98–112

    Google Scholar 

  • Cryer DR, Eccleshall R, Marmur J (1975) Isolation of yeast DNA. Methods Cell Biol 12:39–44

    Google Scholar 

  • Dams E, Hendriks L, Van de Peer Y, Neefs JM, Smits G, Vandenbempt I, De Wachter R (1988) Compilation of small ribosomal subunit RNA sequences. Nucleic Acids Res 1687–173

  • De Wachter R (1989) The nucleotide sequence of the small ribosomal subunit RNA of the yeast Candida albicans and the evolutionary position of the fungi among the eukaryotes. Syst Appl Microbiol 12:223–229

    Google Scholar 

  • Eckenrode VK, Arnold J, Meagher RB (1984) Comparison of the nucleotide sequence of soybean 18s rRNA with the sequences of other small-subunit rRNAs. J Mol Evol 21:259–269

    Google Scholar 

  • Enquist L, Sternberg N (1979) Packaging of bacteriophage lambda in vitro. Methods Enzymol 68:281–289

    Google Scholar 

  • Eriksson OE, Svedskog A, Landvik S (1993) Molecular evidence for the evolutionary hiatus between Saccharomyces cerevisiae and Schizosaccharomyces pombe. Systema Ascomycetorum 11:119–162

    Google Scholar 

  • Georgiev OI, Nikolaev N, Hadjiolov AA, Skryabin KG, Zakharyev VM, Bayev AA (1981) The structure of the yeast ribosomal RNA genes. 4. Complete sequence of the 25s rRNA gene from Saccharomyces cerevisiae. Nucleic Acids Res 9:6953–6958

    Google Scholar 

  • Hendriks L, Goris A, Neefs J, Van der Peer Y, Hennebert G, De Wachter R (1989) The nucleotide sequence of the small ribosomal subunit RNA of the yeast Candida albicans and the evolutionary position of the fungi among the eukaryotes. Syst Appl Microbiol 12:223–229

    Google Scholar 

  • Hendriks L, Goris A, Van de Peer Y, Neefs JM, Van Canneyt M, Kersters K, Berny JF, Hennebert G, De Wachter R (1992) The evolution of ascomycetes and ascomycete-like yeasts as inferred from small ribosomal subunit RNA sequences. Syst Appl Microbiol 15:98–104

    Google Scholar 

  • Henikoff S (1984) Unidirectional digestion with exonuclease III creates targeted break-points for DNA sequencing. Gene 28:351–359

    Google Scholar 

  • Henikoff S (1987) Unidirectional digestion with exonuclease III in DNA sequence analysis. Methods Enzymol 155:156–165

    Google Scholar 

  • Kock JLF, Van der Walt JP (1986) Fatty acid composition of Schizosaccharomyces Lindner. System Appl Microbiol 8:163–165

    Google Scholar 

  • Kudriavzev VI (1960) Die Systematik der Hefen. Akademie-Verlag, Berlin

    Google Scholar 

  • Kurtzman CP (1993) Systematics of the ascomycetous yeasts assessed from ribosomal RNA sequence divergence. Ant van Leeuwenhoek 63:165–174

    Google Scholar 

  • Kurtzman CP, Robnett CJ (1991) Phylogenetic relationships among species of Saccharomyces, Schizosaccharomyces, Debaryomyces and Schwanniomyces determined from partial ribosomal RNA sequences. Yeast 7:61–72

    Google Scholar 

  • Lapeyre B, Michot B, Feliu J, Bachellerie JP (1993) Nucleotide sequence of the Schizosaccharomyces pombe 25s ribosomal RNA and its phylogenetic implications. Nucleic Acids Res 21:3322

    Google Scholar 

  • Lindner P (1893) Schizosaccharomyces pombe nov. spec., ein neuer Gärungserreger. Wochenschr Brau 10:1298–1300

    Google Scholar 

  • Maleszka R, Clark-Walker GD (1990) Sequence of the gene for the cytoplasmic ribosomal RNA small subunit from Kluyveromyces lactis. Nucleic Acids Res 18:1889

    Google Scholar 

  • Martini AV (1991) Evaluation of phylogenetic relationships among fission yeasts by nDNA/nDNA reassociation and conventional taxonomic criteria. Yeast 7:73–78

    Google Scholar 

  • Mercure S, Rougeau N, Montplaisir S, Lemay G (1993a) The nucleotide sequence of the 25s rRNA-encoding gene from Candida albicans. Nucleic Acids Res 21:1490

    Google Scholar 

  • Mercure S, Rougeau N, Montplaisir S, Lemay G (1993b) Complete nucleotide sequence of Candida albicans 5.8s rRNA coding gene and flanking internal transcribed spacers. Nucleic Acids Res 21:4860

    Google Scholar 

  • Mifflin TE (1987) Comparison or radioactive (32P and 35S) and biotinylated probes for detection of Cytomegalovirus DNA. Clin Biochem 20:231–235

    Google Scholar 

  • Musters W, Boon K, Van der Sande CA, Van Heerikhuizen H, Planta RJ (1990) Functional analysis of transcribed spacers of yeast ribosomal DNA. EMBO J 9:3989–3996

    Google Scholar 

  • Olsen GJ, Woese CR (1993) Ribosomal RNA: a key to phylogeny. FASEB J 7:113–123

    Google Scholar 

  • Rankine BC, Fornachon JCM (1964) Schizosaccharomyces malidevorans sp. n., a yeast decomposing L-malic acid. Ant van Leeuwenhoek 30:73–75

    Google Scholar 

  • Raynal F, Michot B, Bachellerie JP (1984) Complete nucleotide sequence of mouse 18s rRNA gene: comparison with other available homologs. FEBS Lett 167:263–268

    Google Scholar 

  • Rubin GM (1973) The nucleotide sequence of Saccharomyces cerevisiae 5.8s ribosomal ribonucleic acid. J Biol Chem 248:3860–3875

    Google Scholar 

  • Rubtsov PM, Musakhanov MM, Zakharyev VM, Krayev AS, Skryabin KG, Bayev AA (1980) The structure of the yeast ribosomal RNA genes. I. The complete nucleotide sequence of the 18s ribosomal RNA gene from Saccharomyces cerevisiae. Nucleic Acids Res 8:5779–5794

    Google Scholar 

  • Schaak J, Mao JI, Söll DG (1982) The 5.8s rRNA gene sequence and the ribosomal repeat of Schizosaccharomyces pombe. Nucleic Acids Res 10:2851–2864

    Google Scholar 

  • Sloof WC (1970) Schizosaccharomyces Lindner. In: Lodder J (ed) The yeasts—a taxonomic study. North-Holland Publishing Co, Amsterdam, pp 733–755

    Google Scholar 

  • Van de Peer Y, Neefs JM, De Wachter R (1990) Small ribosomal subunit RNA sequences, evolutionary relationships among different life forms, and mitochondrial origins. J Mol Evol 30:436–476

    Google Scholar 

  • Veldman GM, Klootwijk J, De Regt VC, Planta RJ, Branlant C, Krol A, Ebel JP (1981a) The primary and secondary structure of yeast 26s rRNA. Nucleic Acids Res 9:4847–4862

    Google Scholar 

  • Veldman GM, Klootwijk J, Van Herikhuizen H, Planta RJ (1981b) The nucleotide sequence of the intergenic region between the 5.8s and 26s rRNA genes of the yeast ribosomal RNA operon. Possible implications for the interaction between 5.8s and 26s rRNA and the processing of primary transcript. Nucleic Acids Res 9:4847–4862

    Google Scholar 

  • Verbeet MP, Van Heerikhuizen H, Klootwijk J, Fontijn RD, Planta RJ (1984) Evolution of yeast ribosomal DNA: molecular cloning of the rDNA units of Kluyveromyces lactis and Hansenula wingei and their comparison with the rDNA units in other Saccharomycetaceae. Mol Gen Genet 195:116–125

    Google Scholar 

  • Wickerham LJ, Duprat E (1945) A remarkable fission yeast, Schizosaccharomyces versatilis nov. sp. J Bacteriol 50:597–607

    Google Scholar 

  • Yamada Y, 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 presence of linoleic acid in cellular fatty acid composition. J Gen Appl Microbiol 33:295–298

    Google Scholar 

  • Yamada Y, Banno I (1989) A proposal to divide the genus Schizosaccharomyces Lindner sensu Yarrow into three separate genera. 7th Int Symp Yeasts'. Yeast Special Issue pp 393–398

  • Yamada Y, Aizawa K, Matsumoto A, Nakagawa Y, Banno I (1987) An electrophoretic comparison of enzymes in strains of species in the fission yeast genera Schizosaccharomyces, Octosporomyces and Hasegawaea. J Gen Appl Microbiol 33:363–369

    Google Scholar 

  • Yamada Y, Arimoto M, Kondo K (1973) Coenzyme Q system in the classification of the ascosporogenous yeast genus Schizosaccharomyces and yeast-like genus Endomyces. J Gen Appl Microbiol 33:363–369

    Google Scholar 

  • Yukawa M, Maki T (1931) Schizosaccharomyces japonicus nov. spec. La Bull Sci Fakultato Terkultura, Kjusu Imp Univ, Fukuoka, Japan 4:218–226

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut für Biologie IV (Mikrobiologie), Rheinisch-Westfälische Technische Hochschule Aachen, Worringer Weg, D-52056, Aachen, Germany

    Joerg Naehring, Stefan Kiefer & Klaus Wolf

Authors
  1. Joerg Naehring
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stefan Kiefer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Klaus Wolf
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by F.K. Zimmermann

Rights and permissions

Reprints and permissions

About this article

Cite this article

Naehring, J., Kiefer, S. & Wolf, K. Nucleotide sequence of the Schizosaccharomyces japonicus var. versatilis ribosomal RNA gene cluster and its phylogenetic implications. Curr Genet 28, 353–359 (1995). https://doi.org/10.1007/BF00326433

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00326433

Key words

Search

Navigation