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The tobacco mitochondrial ATPase subunit 9 gene is closely linked to an open reading frame for a ribosomal protein

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Summary

A transcribed segment of mitochondrial DNA (mtDNA) from Nicotiana tabacum contains the F0-ATPase subunit 9 gene, an open reading frame with homology to the E. coli small subunit ribosomal protein S13 and an open reading frame with homology to a portion of the mammalian “URF 1” protein, recently shown to be a component of the NADH:ubiquinone reductase complex (NADH:Q 1). The transcriptional patterns of the tobacco ATPase 9 gene and S13-like open reading frame share eight RNA species indicating the two sequences are part of the same transcriptional unit. A maize mtDNA fragment contains the S13 homologous sequence and the NADH:Q 1 homologous sequence in an orientation similar to tobacco. The S13-like sequence is present as a single copy in maize and tobacco, as two copies in wheat, and is absent in pea and bean. We discuss the distribution and orientation of the S13-like and “URF 1”-like sequences and the possibility that they are active genes.

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References

  • Anderson S, Bankier AT, Barrell BG, de Bruijn MHL, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJH, Staden R, Young IG (1981) Sequence and organization of the human mitochondrial genome. Nature 290:457–465

    Google Scholar 

  • Anderson S, de Bruijn MHL, Coulson AR, Eperon IC, Sanger F, Young IG (1982) Complete sequence of bovine mitochondrial DNA, conserved features of the mammalian mitochondrial genome. J Mol Biol 156:683–717

    Google Scholar 

  • Bedwell D, Davis G, Gosink M, Post L, Nomura M, Kestler H, Zengel JM, Lindahl L (1985) Nucleotide sequence of the alpha ribosomal protein operon of Escherichia coli. Nucleic Acids Res 13:3891–3903

    Google Scholar 

  • Bland MM, Matzinger DF, Levings CS III (1985) Comparison of the mitochondrial genome of Nicotiana tabacum with its progenitor species. Theor Appl Genet 69:535–541

    Google Scholar 

  • Braun CJ, Levings CS III (1985) Nucleotide sequence of the F1-ATPase α subunit gene from maize mitochondria. Plant Physiol 79:571–577

    Google Scholar 

  • Brennicke A, Möller S, Blanz PA (1985) The 18S and 5S ribosomal RNA genes in Oenothera mitochondria: sequence rearrangements in the 18S and 5S rRNA genes of higher plants. Mol Gene Genet 198:404–410

    Google Scholar 

  • Brown TA, Davies RW, Ray JA, Waring RB, Scazzocchio C (1983) The mitochondrial genome of Aspergillus nidulans contains reading frames homologous to the human URFs 1 and 4. EMBO J 2:427–435

    Google Scholar 

  • Burger G, Werner S (1983) Nucleotide sequence and transcript mapping of a mtDNA segment comprising CO 1, tRNAarg, and several unidentified reading frames in Neurospora crassa. In: Schweyen RJ, Wolf K, Kaudewitz F (eds) Mitochondria 1983: nucleo-mitochondrial interactions. de Gruyter, Berlin, pp 331–342

    Google Scholar 

  • Burger G, Helmer Citterich M, Nelson MA, Werner S, Macino G (1985) RNA processing in Neurospora crassa mitochondria: transfer RNAs punctuate a large precursor transcript. EMBO J 4:197–204

    Google Scholar 

  • Barke JM, RajBhandary UL (1982) Intron within the large rRNA gene of N. crassa mitochondria: a long open reading frame and a consensus sequence possibly important in splicing. Cell 31:509–520

    Google Scholar 

  • Chomyn A, Mariottini P, Cleeter MWJ, Ragan CI, Matsuno-Yagi A, Hatefi Y, Doolittle RF, Attardi G (1985) Six unidentified reading frames of human mitochondrial DNA encode components of the respiratory-chain NADH dehydrogenase. Nature 314:592–597

    Google Scholar 

  • Clary DO, Goddard JM, Martin SC, Fauron CM-R, Wolstenholme DR (1982) Drosophila mitochondrial DNA: a novel gene order. Nucleic Acids Res 10:6619–6637

    Google Scholar 

  • Dale RMK, Mendu N, Ginsburg H, Kridl JC (1984) Sequence analysis of the maize mitochondrial 26S rRNA gene and flanking regions. Plasmid 11:141–150

    Google Scholar 

  • Dawson AJ, Jones VP, Leaver CJ (1984) The apocytochrome b gene in maize mitochondria does not contain introns and is preceded by a potential ribosome binding site. EMBO J 3:2107–2113

    Google Scholar 

  • Dewey RE, Levings CS III, Timothy DH (1985a) Nucleotide sequence of ATPase subunit 6 gene of maize mitochondria. Plant Physiol 79:914–919

    Google Scholar 

  • Dewey RE, Schuster AM, Levings CS III, Timothy DH (1985b) Nucleotide sequence of Fo-ATPase proteolipid (subunit 9) gene of maize mitochondria. Proc Natl Acad Sci USA 82:1015–1019

    Google Scholar 

  • Dewey RE, Levings CS III, Timothy DH (1986) Novel recombinations in the maize mitochondrial genome produce a unique transcriptional unit in the texas male-sterile cytoplasm. Cell 44:439–449

    Google Scholar 

  • Drake JW, Glickman BW, Ripley LS (1983) Updating the theory of mutation. Am Scientist 71:621–630

    Google Scholar 

  • Edwards JC, Christianson T, Mueller D, Biswas TK, Levens D, Li D, Wettstein J, Rabinowitz M (1983) Initiation and transcription of yeast mitochondrial RNA. In: Schweyen RJ, Wolf K, Kaudewitz F (eds) Mitochondria 1983: nucleo-mitochondrial interactions. de Gruyter, Berlin, pp 69–78

    Google Scholar 

  • Fox TD, Leaver CJ (1981) The Zea mays mitochondrial gene codding cytochrome oxidase subunit II has an intervening sequence and does not contain TGA codons. Cell 26:315–323

    Google Scholar 

  • Hack E, Leaver CJ (1983) The α-subunit of the maize F1-ATPase is synthesised in the mitochondrion. EMBO J 2:1783–1789

    Google Scholar 

  • Hensgens LAM, 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

    Google Scholar 

  • Hensgens LAM, Brakenhoff J, de Vries BF, Sloof P, Tromp MC, van Boom JH, Benne R (1984) The sequence of the gene for cytochrome c oxidase subunit II a frameshift containing gene for cytochrome c oxidase subunit II and seven unassigned reading frames in Trypanosoma brucei mitochondrial maxi-circle DNA. Nucleic Acids Res 12:7327–7344

    Google Scholar 

  • Hiesel R, Brennicke A (1983) Cytochrome oxidase subunit II gene in mitochondria of Oenothera has no intron. EMBO J 2:2173–2178

    Google Scholar 

  • Ise W, Haiker H, Weiss H (1985) Mitochondrial translation of subunits of the rotenone-sensitive NADH:ubiquinone reductase in Neurospora crassa. EMBO J 4:2075–2080

    Google Scholar 

  • Khoury G, Gruss P (1983) Enhancer elements. Cell 33:313–314

    Google Scholar 

  • Lambowitz AM, LaPolla RJ, Collins RA (1979) Mitochondrial ribosome assembly in Neurospora, two-dimensional gel electrophoretic analysis of mitochondrial ribosomal proteins. J Cell Biol 82:17–31

    Google Scholar 

  • Leaver CJ, Dixon LK, Hack E, Fox TD, Dawson AJ (1983) Mitochondrial genes and their expression in higher plants. In: Ciferri O, Dure L III (eds) Structure and function of plant genomes. Plenum Press, New York, pp 347–361

    Google Scholar 

  • Lelong JC, Gros D, Gros F, Bollen A, Maschler R, Stöffler G (1974) Function of individual 30S subunit proteins of Escherichia coli. Effect of specific immunoglobulin fragments (Fab) on activities of ribosomal decoding sites. Proc Natl Acad Sci USA 71:248–252

    Google Scholar 

  • Lindemann H, Wittmann-Liebold B (1977) Primary structure of protein S13 from the small subunit of Escherichia coli ribosomes. Hoppe-Seyler's Z Physiol Chem 358:843–863

    Google Scholar 

  • Maniatis T, Fritsch EF, Sambrook J (1982) In: Molecular cloning, a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, pp 1–545

    Google Scholar 

  • Michel F, Cummings DJ (1985) Analysis of class I introns in a mitochondrial plasmid associated with senescence of Podospora anserina reveals extraordinary resemblance to the Tetrahymena ribosomal intron. Curr Genet 10:69–79

    Google Scholar 

  • Nomura M (1984) The control of ribosome synthesis. Sci Am 250:102–114

    Google Scholar 

  • Norrander J, Kempe T, Messing J (1983) Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene 26:101–106

    Google Scholar 

  • Pratje E, Schnierer S, Dujon B (1984) Mitochondrial DNA of Chlamydomonas reinhardtii: the DNA sequence of a region showing homology with mammalian URF2. Curr Genet 9:75–82

    Google Scholar 

  • Pring DR, Levings CS III (1978) Heterogeneity of maize cytoplasmic genomes among male-sterile cytoplasms. Genetics 89:121–136

    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 

  • Scazzocchio C, Brown TA, Waring RB, Ray JA, Davies RW (1983) Organisation of the Aspergillus nidulans mitochondrial genome. In: Schweyen RJ, Wolf K, Kaudewitz F (eds) Mitochondria 1983: nucleo-mitochondrial interactions. de Gruyter, Berlin, pp 303–312

    Google Scholar 

  • Schieber GL, O'Brien TW (1983) Cytoplasmic synthesis of proteins of the mammalian mitochondrial ribosome. In: Schweyen RJ, Wolf K, Kaudewitz F (eds) Mitochondria 1983: nucleo-mitochondrial interactions, de Gruyter, Berlin, pp 469–480

    Google Scholar 

  • Schuster AM, Sisco RU, Levings CS III (1983) Two unique RNAs in cms-S and RU maize mitochondria. In: Goldberg RB (ed) Plant molecular biology. Alan R Liss, New York, pp 437–444

    Google Scholar 

  • Sebald W, Hoppe J, Wachter E (1979) Amino acid sequence of the ATPase proteolipid from mitochondria, chloroplasts and bacteria (wild type and mutants). In: Quagliarello E (ed) Function and molecular aspects of biomembrane transport, Elsevier/North-Holland Biomedical, Amsterdam, pp 63–74

    Google Scholar 

  • Terpstra P, Zanders E, Butow RA (1979) The association of var1 with the 38S mitochondrial ribosomal subunit in yeast. J Biol Chem 254:12653–12661

    Google Scholar 

  • Thomas PS (1980) Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci USA 77:5201–5205

    Google Scholar 

  • van den Boogaart P, Samallo J, van Dijk S, Agsteribbe E (1982) Structural and functional analyses of the genes for subunit II of cytochrome aa3 and for a dicyclohexylcarbodiimide-binding protein in Neurospora crassa mitochondrial DNA. In: Slonimski P, Borst P, Attardi G (eds) Mitochondrial genes. Cold Spring Harbor Laboratory, Cold Spring Harbor, pp 375–380

    Google Scholar 

  • Vieira J, Messing J (1982) The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene 19:259–268

    Google Scholar 

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Communicated by R.B. Goldberg

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Bland, M.M., Levings, C.S. & Matzinger, D.F. The tobacco mitochondrial ATPase subunit 9 gene is closely linked to an open reading frame for a ribosomal protein. Molec Gen Genet 204, 8–16 (1986). https://doi.org/10.1007/BF00330180

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