Skip to main content
Log in

Putative target sites for mobile G+C rich clusters in yeast mitochondrial DNA: Single elements and tandem arrays

  • Published:
Molecular and General Genetics MGG Aims and scope Submit manuscript

Summary

GC clusters constitute the major repetitive elements in the mitochondrial (mt) genome of the yeast Saccharomyces cerevisiae. Many of these clusters are optional and thus contribute much to the polymorphism of yeast mtDNAs. We have made a systematic search for polymorphic sites by comparing mtDNA sequences of various yeast strains. Most of the 26 di- or polymorphic sites found differ by the presence or absence of a GC cluster of the majority class, here referred to as the M class, which terminate with an AGGAG motif. Comparison of sequences with and without the GC clusters reveal that elements of the subclasses M1 and M2 are inserted 3′ to a TAG, flanked by A+T rich sequences. M3 elements, in contrast, only occur in tandem arrays of two to four GC clusters; they are consistently inserted 3′ to the AGGAG terminal sequence of a preexisting cluster. The TAG or the terminal AGGAG, therefore, are regarded as being part of the target sites for M1 and M2 or M3 elements, respectively. The dinucleotide AG is in common to both target sites; it also occurs at the 3′ terminus (AGGAG). This suggests its duplication during GC cluster insertion. This notion is supported by the observation that GC clusters of the minor classes G and V similarily repeat at their 3′ terminus a GT or an AA dinucleotide, respectively, from their putative target sites.

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.

Institutional subscriptions

Similar content being viewed by others

References

  • Berlani RE, Pentella C, Macino G, Tzagoloff A (1980a) Assembly of the mitochondrial membrane system: Isolation of mitochondrial transfer ribonucleic acid mutants and characterization of transfer ribonucleic acid genes of Saccharomyces cerevisiae. J Bacteriol 141:1086–1097

    Google Scholar 

  • Berlani RE, Bonitz SG, Coruzzi G, Nobrega M, Tzagoloff A (1980b) Transfer RNA genes in the cap-oxi1 region of yeast mitochondrial DNA. Nucleic Acid Res 8:5017–5030

    Google Scholar 

  • Blanc H, Dujon B (1980) Replicator, regions of the yeast mitochondrial DNA responsible for suppressiveness. Proc Natl Acad Sci USA 77:3942–3946

    Google Scholar 

  • Blanc H (1984) Two modules from the hypersuppressive rho- mitochondrial DNA are required for plasmid replication in yeast. Gene 30:47–61

    Google Scholar 

  • Bonitz SG, Tzagoloff A (1980) Assembly of the mitochondrial membrane system; Sequences of yeast mitochondrial tRNA genes. J Biol Chem 255:9075–9081

    Google Scholar 

  • Bonitz SG, Coruzzi G, Thalenfeld BE, Tzagoloff A (1980) Assembly of the mitochondrial membrane system: Structure and nucleotide sequence of the gene for subunit 1 of yeast cytochrome oxidase. J Biol Chem 225:11927–11941

    Google Scholar 

  • Bordonne R (1987) Structure et expression de gènes mitochondriaux de la levure Saccharomyces cerevisiae. Etude de la maturation des produits de transcription de DNA mitochondrial. PhD thesis, Strasbourg

  • Bordonne R, Dirheimer G, Martin R (1987) Transcription initiation and RNA processing of a yeast mitochondrial tRNA gene cluster. Nucleic Acids Res 15:7381–7394

    Google Scholar 

  • Butow RA, Ainley WM, Zassenhaus HP, Hudspeth ME, Grossmann LI (1983) The unusual organization of the yeast mitochondrial VAR1 gene. In: Nagley P, Linnane AW, Peacock AW, Pateman JA (eds) Manipulation and Expression of Genes in Eukaryotes. Academic Press, Sydney, pp 269–277

    Google Scholar 

  • Butow RA, Perlman PS, Grossman LI (1985) The unusual VAR1 gene of yeast mitochondrial DNA. Science 228:1496–1501

    Google Scholar 

  • Colin Y, Baldacci G, Bernardi G (1985) A new putative gene in the mitochondrial genome of Saccharomyces cerevisiae. Gene 36:1–13

    Google Scholar 

  • Coruzzi G, Bonitz SG, Thalenfeld BE, Tzagoloff A (1981) Assembly of the mitochondrial membrane system: Analysis of the nucleotide sequence and transcripts in the oxi1 region of yeast mitochondrial DNA. J Biol Chem 256:12780–12787

    Google Scholar 

  • de Zamaroczy M, Bernardi G (1985) Sequence organisation of the mitochondrial genome of yeast — a review. Gene 41:1–22

    Google Scholar 

  • de Zamaroczy M, Bernardi G (1986a) The GC clusters of the mitochondrial genome of yeast and their evolutionary origin. Gene 41:1–22

    Google Scholar 

  • de Zamaroczy M, Bernardi G (1986b) The primary structure of the mitochondrial genome of Saccharomyces cerevisiae — a review. Gene 47:155–177

    Google Scholar 

  • de Zamaroczy M, Faugeron-Fonty G, Bernardi G (1983) Excision sequences in the mitochondrial genome of yeast. Gene 21:193–202

    Google Scholar 

  • de Zamaroczy M, Faugeron-Fonty G, Baldacci G, Goursot R, Bernardi G (1984) The ORI sequences of the mitochondrial genome of a wild-type yeast strain: number; location; orientation and structure. Gene 32:439–457

    Google Scholar 

  • Dieckmann CL, Gandy B (1987) Preferential recombination between GC clusters in yeast mitochondrial DNA. EMBO J 6:4197–4203

    Google Scholar 

  • Dobres M, Gerbl-Rieger S, Schmelzer C, Mueller MW, Schweyen RJ (1985) Deletions in the COB gene of yeast mtDNA and their phenotypic effect. Curr Genet 10:283–290

    Google Scholar 

  • Dujon B (1980) Sequence of the intron and flanking exons of the mitochondrial 21S rRNA gene of yeast strains having different alleles at the omega and rib-1 loci. Cell 20:185–197

    Google Scholar 

  • Faugeron-Fonty G, Goyon C (1985) Polymorphic variations in the ORI sequences from the mitochondrial genomes of different wild-type yeast strains Curr Genet 10:269–282

    Google Scholar 

  • Faugeron-Fonty G, Le Van Kim C, de Zamaroczy M, Goursot R, Bernardi G (1984) A comparative study of the ORI sequences from the mitochondrial genome of twenty wild-type yeast strains. Gene 32:459–473

    Google Scholar 

  • Gough J, Murray NE (1983) Sequence diversity among related genes for recognition of specific targets in DNA molecules. J Mol Biol 166:1–19

    Google Scholar 

  • Goursot R, Mangin M, Bernardi G (1982) Surrogate origins of replication in the mitochondrial genomes of ORIs petite mutants of yeast. EMBO J 1:705–711

    Google Scholar 

  • Hensgens LAM, Bonen L, de Haan M, van der Horst G, Grivell LA (1983) Two intron sequences in yeast mitochondrial COX1 gene: Homology among URF-containing introns and strain dependent variation in flanking exons. Cell 32:379–389

    Google Scholar 

  • Holl J, Schmidt C, Schweyen RJ (1985) COB intron 3 in yeast mtDNA: Nucleotide sequence and mutations in a novel RNA domain. In: Quagliariello E, Slater EC, Palmieri F, Saccone C, Kroon AM (eds) Achievements and perspectives of Mitochondrial Research, vol. 2, Biogenesis. Elsevier Science Publishers B. V. Amsterdam, pp 227–236

    Google Scholar 

  • Hudspeth MES, Ainley WM, Shumard DS, Butow RA, Grossman LJ (1982) Location and structure of the VAR1 gene on yeast mitochondrial DNA: Nucleotide sequence of the 40.0 allele. Cell 30:617–626

    Google Scholar 

  • Hudspeth MES, Vicent RD, Perlman PS, Shumard DS, Treisman L, Grossman LI (1984) Expandable VAR1 gene of yeast mitochondrial DNA: In-frame insertions can explain the strain-specific protein size polymorphisms. Proc Natl Acad Sci USA 81:3148–3152

    Google Scholar 

  • Johnson DA, Gautsch JW, Sportsman JR, Elder JH (1984) Improved technique utilizing nonfat dry milk for analysis of proteins and nucleic acids transferred to nitrocellulose. Gene Anal Technique 1:3–8

    Google Scholar 

  • Kleckner N (1981) Transposable elements in prokaryotes. Annu Rev Genet 15:341–404

    Google Scholar 

  • Lang FB, Burger G, Thomas D, Bandlow W, Kaudewitz F (1977) A simple method for large scale preparation of mitochondria from microorganisms. Anal Biochem 77:110–121

    Google Scholar 

  • Li M, Tzagoloff A, Underbrink-Lyon K, Martin NC (1982) Identification of the paromomycin-resistance mutation in the 15 S RNA gene of yeast mitochondria. J Biol Chem 257:5921–5928

    Google Scholar 

  • Macino G, Tzagoloff A (1980) Assembly of the mitochondrial membrane system: Sequence analysis of a yeast mitochondrial ATPase gene containing the OLI2 and OLI4 loci. Cell 20:507–517

    Google Scholar 

  • Martin RP, Bordonné R, Dirheimer G (1982) The paromomycin region in the yeast mitochondrial genome. In: Akoyounoglou G, Evangelopoulos EA, Georgatsos J, Palaiologos G, Trakatellis A, Tsiganos CP (eds) Cell function and differentiation; part B. A.R. Liss, Inc. New York, pp 355–365

    Google Scholar 

  • Messing J, Crea R, Seeburg PH (1981) A system for shotgun DNA sequencing. Nucleic Acids Res 9:309–321

    Google Scholar 

  • Michel F (1984) A maturase-like coding sequence downstream of the OXI2 gene of yeast mitochondrial DNA is interrupted by two GC clusters and a putative end-of-messenger signal. Curr Genet 8:307–317

    Google Scholar 

  • Miller DL, Underbrink-Lyon K, Najarian DR, Krupp J, Martin NC (1983) Transcription of yeast mitochondrial tRNA genes and processing of tRNA gene transcripts. In: Schweyen RJ, Wolf K, Kaudewitz F (eds) Mitochondria 1982. Walter de Gruyter, Berlin New York, pp 151–164

    Google Scholar 

  • Nobrega FG, Tzagoloff A (1980) Assembly of the mitochondrial membrane system: DNA sequence and organisation of the cytochrome b gene in Saccharomyces cerevisiae D273-10B. J Biol Chem 255:9829–9837

    Google Scholar 

  • Novitski CE, Macreadie JG, Maxwell RJ, Lukins HB, Linnane AW, Nagley P (1984) Biogenesis of mitochondria: Genetic and molecular analysis of the OLI2 region of mitochondrial DNA in Saccharomyces cerevisiae. Curr Genet 8:135–146

    Google Scholar 

  • Osinga KA, Vries EDE, Van der Horst GTJ, Tabak HF (1984) Initiation of transcription in yeast mitochondria: Analysis of origins of replication and of genes coding for a messenger RNA and a transfer RNA. Nucleic Acids Res 12:1889–1900

    Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467

    Google Scholar 

  • Séraphin B, Simon M, Faye G (1985) A mitochondrial reading frame which may code for a maturase-like protein in Saccharomyces cerevisiae. Nucleic Acids Res 13:3005–3014

    Google Scholar 

  • Séraphin B, Simon M, Faye G (1987) The mitochondrial reading frame rf3 is a functional gene in Saccharomyces cerevisiae. J Biol Chem 262:10146–10153

    Google Scholar 

  • Sor F, Fukihara H (1982a) Nature of an inserted sequence in the mitochondrial gene coding for 15 S ribosomal RNA of yeast. Nucleic Acids Res 10:1626–1633

    Google Scholar 

  • Sor F, Fukihara H (1982b) Nucleotide sequence of the small ribosomal RNA gene from the mitochondria of Saccharomyces cerevisiae. In: Slonimski P, Borst P, Attardi G (eds) Mitochondrial Genes. Cold Spring Harbor Laboratory Press, New York, pp 255–267

    Google Scholar 

  • Sor F, Fukuhara H (1983) Complete DNA sequence coding for the large ribosomal RNA of yeast mitochondria. Nucleic Acids Res 11:339–348

    Google Scholar 

  • Tzagoloff A, Nobrega M, Akai A, Macino G (1980) Assembly of the mitochondrial membrane system: Organisation of yeast mitochondrial DNA in the OLI1 region. Curr Genet 2:149–157

    Google Scholar 

  • Wakabayashi K, Mabuchi T (1984) Nucleotide sequence involved in the replication of cloned yeast mitochondrial DNA. J Biochem 96:171–177

    Google Scholar 

  • Weiller G (1987) Mobile Elemente im mitochondrialen Genom der Hefe. PhD thesis, University of Munich

  • Zinn RA, Pohlman JK, Perlman PS, Butow RA (1987) In vivo double-strand breaks occur at recombinogenic G+C rich sequences in the yeast mitochondrial genome. Proc Natl Acad Sci USA 85:2686–2690

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by C.P. Hollenberg

Rights and permissions

Reprints and permissions

About this article

Cite this article

Weiller, G., Schueller, C.M.E. & Schweyen, R.J. Putative target sites for mobile G+C rich clusters in yeast mitochondrial DNA: Single elements and tandem arrays. Molec Gen Genet 218, 272–283 (1989). https://doi.org/10.1007/BF00331278

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00331278

Key words

Navigation