Abstract
The purpose of this work was to compare mitochondrial DNA restriction endonuclease patterns in strains of the yeast Kluyveromyces lactis, from different sources, to see how conserved is the organization of this organellar genome. The mitochondrial DNA of five independently-isolated strains and one of unknown origin were compared. Strains NRRL Y-1205, NRRL Y-8279 and NRRL Y-1140 gave identical patterns. Strain NRRL Y-1564 showed an insertion, with respect to the other three, of approximately 1250 bp. Strain W600B had also an insertion with extra restriction sites for EcoRI, HpaI, HaeIII, HincII and XbaI. On the other hand, strain Y-123 showed a restriction pattern quite different from the others.
Sequences putatively encoding apocytochrome b, ATPase subunit 9 and ribosomal RNA large subunit, were localized on the physical maps of three strains. Results demonstrated that the order of these three genes shows a common feature in strains W600B and WM37 (auxotroph of Y-1140) but a different distribution in WM27 (auxotroph derived from Y-123). All these facts explain the extensive intraspecific polymorphism observed in the mtDNA of this yeast.
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References
Attardi G & Schatz G (1988) Biogenesis of Mitochondria. Ann. Rev. Cell. Biol. 4: 289–333
Bernardi G, Prunell A, Fonty GH, Kopecka H & Straus F (1976) The mitochondrial genome of yeast. Organization, evolution and the petite mutation. In: Saccone C & Kroon AM (Eds) The Genetic Function of Mitochondrial DNA (pp 185–198). North Holland Publishing Co., Amsterdam
Bogler SA, Zarley CD, Burianek LL, Fuerst PA & Byers TJ (1983) Interstrain mitochondrial DNA polymorphism detected in Acanthamoeba by restriction endonuclease analysis. Mol. Biochem. Parasitol. 8: 145–163
Brown GG & Simpson MV (1981) Intra- and interspecific variation of the mitochondrial genome in Rattus norvergicus and Rattus rattus. Restriction enzyme analysis of variant mitochondrial DNA molecules and their evolutionary relationships. Genetics 97: 125–143
Brown TA, Ray JA, Waring RB, Scazzocchio C & Davis RW (1984) A mitochondrial reading frame which may code for a second form of ATPase subunit 9 in Aspergillus nidulans. Curr. Genet. 8: 489–492
Brown WM (1980) Polymorphism in mitochondrial DNA of humans as revealed by restriction endonuclease analysis. Proc. Natl. Acad. Sci. USA 77: 3605–3609
Brunner A & Coria R (1989) Cloning and sequencing of the gene for apocytochrome b of the yeast Kluyveromyces lactics strains WM27 (NRRL Y-17066) and WM37 (NRRL Y-1140). Yeast 5: 209–218
Buzzo K, Foute LD & Wolstenholme DR (1978) EcoRI cleavage site variants of mitochondrial DNA molecules from rats. Proc. Natl. Acad. Sci. USA 75: 909–913
Case TJ & Wallace DC (1981) Maternal inheritance of mitochondrial DNA polymorphisms in cultured human fibroblasts. Somatic Cell Genet. 7: 103–108
Clark-Walker GD (1989) In vivo rearrangement of mitochondrial DNA in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 86: 8847–8851
Costas M, Edwards SW, Lloyd D, Griffiths AJ & Turner G (1983) Restriction enzyme analysis of mitochondrial DNA of members of the genus Acanthamoeba as an aid in taxonomy. FEMS Microbiol Lett. 17: 231–234
Denaro M, Blanc H, Johnson MJ, Chen KH, Wilmsen E, Cavalli-Sforza LL & Wallace DC (1981) Ethnic variation in HpaI endonuclease cleavage patterns of human mitochondrial DNA. Proc. Natl. Acad. Sci. USA 78: 5768–5772
Duell EA, Inoue S & Utter MF (1964) Isolation and properties of intact mitochondria from spheroplasts of yeasts. J. Bacteriol. 88: 1762–1773
Dujon B (1981) Mitochondrial genetics and functions. In: Strathern JN, Jones WE & Broach JR (Eds) The Molecular Biology of the Yeast Saccharomyces. Life cycle and inheritance (pp 505–635). Cold Spring Harbor Laboratory. Cold Spring Harbor, NY
Fitch WM, Smith TF & Ralph WW (1983) Mapping the order of DNA restriction fragments. Gene 22: 19–29
Francisco JF, Brown GG & Simpson MV (1979) Further studies on types A and B rat mtDNAs: Cleavage maps and evidence for cytoplasmic inheritance in mammals. Plasmid 2: 426–436
Groot GSP & Van Harten-Loosbroek N (1980) The organization of the genes for ribosomal RNA on mitochondrial DNA of Kluyveromyces lactis. Curr. Genet. 1: 133–135
Grossman LT & Hudspeth MES (1985) Fungal mitochondrial genomes. In: Bennett JW & Lasure IL (Eds) Gene Manipulations in Fungi. (pp 60–103). Academic Press, NY
Hayashi JI, Tagashira Y, Moriwaki K & Yosida YH (1981) Polymorphisms of mitochondrial DNAs in Norway rats (Rattus norvegicus). Cleavage site variations and length polymorphisms of restriction fragments. Molec. gen. Genet. 184: 337–341
Hensgens ALM, Grivell LA, Borst P & Bos JL (1979) Nucleotide sequence of the mitochondrial structural gene for subunit 9 of yeast ATPase complex. Proc. Natl. Acad. Sci. USA 76: 1663–1667
Hudspeth MES, Shumrad DS, Tatti KM & Grossman LT (1980) Rapid purification of yeast mitochondrial DNA in high yield. Biochim. Biophys. Acta 610: 221–228
Hutchinson III C, Newbold JE, Potter SS & Edgell MH (1974) Maternal inheritance of mammalian mitochondrial DNA. Nature 251: 536–538
Johnson MJ, Wallace DC, Ferris SD, Rattazzi MC & Cavalli-Sforza LL (1983) Radiation of human mitochondrial DNA types analyzed by restriction endonuclease cleavage patterns. J. Mol. Evol. 19: 255–271
Kurtzman CP (1985) Molecular taxonomy of the fungi. In: Bennett JW & Lasure IL (Eds) Gene Manipulations in Fungi (pp 35–63). Academic Press, NY
Kurtzman CP, Phaff HJ & Meyer SA (1983) Nucleic acid relatednes among yeasts. In: Spencer JFT, Spencer DM & Smith ARW (Eds) Yeast Genetics. Fundamental and Applied Aspects (pp 139–166). Springer Verlag, NY
Lachance MA (1985) Current views on the yeast species. Microbiol. Sci. 2: 122–126
Lansman RA, Avise JC, Aquadro CF, Shapira JF & Daniel WS (1983) Extensive genetic variation in mitochondrial DNAs among geographic populations in the deer mouse, Peromyscus maniculatus. Evolution 37: 1–16
Macino G & Tzagoloff A (1979) Assembly of the mitochondrial membrane system. The DNA sequence of a mitochondrial ATPase gene in Saccharomyces cerevisiae. J. Biol. Chem. 254: 4617–4623
Maniatis T, Fritsch EF & Sambrook J (1982) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
Massardo D, Wolf K, Manna F & DelGiudice L (1981) Divergenze nel DNA mitochondriale de ceppi differenti del lievito Schizosaccharomyces pombe. ATTI Associazione Genetica Italiana 28: 265–268
McArthur CR & Clark-Walker GD (1983) Mitochondrial DNA size diversity in the Dekkera-Brettanomyces yeasts. Curr. Genet. 7: 29–35
Reilly JG & Thomas CA (1980) Length polymorphisms, restriction site variation and maternal inheritance of mitochondrial DNA of Drosophila melanogaster. Plasmid 3: 109–115
Sanders JPM, Weijers PJ, Groot GSP & Borst P (1974) Properties of mitochondrial DNA from Kluyveromyces lactis. Biochim. Biophys. Acta 374: 136–144
Sanders JPM, Heyting C, Verbeet MPh, Meijlink CPW & Borst P (1977) The organization of genes in yeast mitochondrial DNA. III. Comparison of the physical maps of the mitochondrial DNAs from three wild-type Saccharomyces Strains. Molec. gen. Genet. 157: 239–261
Sebald W & Hoppe J (1981) On the structure and genetics of the proteolipid subunit of the ATP synthase complex. Curr. Topics Bioenerg. 12: 1–64
Shah DM & Langley CH (1979) Inter- and intraspecific variation in restriction maps of Drosophila mitochondrial DNAs. Nature 281: 696–699
Sheetz RM & Dickson RC (1980) Mutations affecting synthesis of β-galactosidase activity in the yeast Kluyveromyces lactis. Genetics 95: 877–890
Tzagoloff A & Meyers AM (1986) Genetics of mitochondrial biogenesis. Ann. Rev. Biochem. 55: 249–285
Van den Boogaart P, Samallo J & Agsterribe E (1982) Similar genes for a mitochondrial ATPase subunit in the nuclear and mitochondrial genomes of Neurospora crassa. Nature 298: 187–189
Wallace DC (1982) Structure and evolution of organelle genomes. Microbiol. Rev. 46: 208–240
Wesołowski M, Algeri A & Fukuhara H (1981) Gene organization of the mitochondrial DNA of yeasts: Kluyveromyces lactis and Saccharomycopsis lipolytica. Curr. Genet. 3: 157–162
Wesołowski M & Fukuhara H (1981) Linear mitochondrial deoxyribonucleic acid from the yeast Hansenula mrakii. Mol. Cell. Biol. 1: 387–393
Yonekawa H, Moriwaki K, Gotoh O, Hayashi JI, Watanabe J, Miyashita N, Petras ML & Tagashira Y (1981) Evolutionary relationships among five subspecies of mus musculus based on restriction enzyme cleavage patterns of mitochondrial DNA. Genetics 98: 801–816
Zimmer M, Welser F, Oraler G & Wolf K (1987) Distribution of mitochondrial introns in the species Schizosaccharomyces pombe and the origin of the group II intron in the gene encoding apocytochrome b. Curr. Genet. 12: 329–336
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Roberto, C.O., María, E.Z.O., Valentín, M.R. et al. Restriction site variation, length polymorphism and changes in gene order in the mitochondrial DNA of the yeast Kluyveromyces lactics . Antonie van Leeuwenhoek 58, 227–234 (1990). https://doi.org/10.1007/BF00399333
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DOI: https://doi.org/10.1007/BF00399333