Skip to main content
Log in

The genes coding for subunit 3 of NADH dehydrogenase and for ribosomal protein S12 are present in the wheat and maize mitochondrial genomes and are co-transcribed

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

Summary

A region of about 2 kb which is almost identical in the wheat and maize mitochondrial genomes has been sequenced. It contains a tRNASer gene, a pseudo-tRNA gene and two open reading frames coding for subunit 3 of the NADH dehydrogenase (118 amino acids) and for ribosomal protein S12 (125 amino acids). The two protein genes are separated by 47 bp and are co-transcribed in wheat and maize. Two transcripts of about 0.9 kb and 3.0 kb, cach coding for both proteins, have been characterized, but no monocistronic transcript was detected. Each gene is preceded by a putative ribosome binding site. The pseudo-tRNA gene is interrupted by two insertion sequences in wheat and by one in maize. The origin of the additional interrupting sequence found in the wheat pseudo-tRNA gene, which is also present elsewhere in the mitochondrial genomes, is discussed.

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

References

  • Anderson S, Bankier AT, Barrell BG, De Bruijn MHL, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreir 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 

  • Bibb MJ, Von Etten RA, Wright CT, Walberg MW, Clayton DA (1981) Sequence and gene organization of mouse mitochondrial DNA. Cell 26:167–180

    Google Scholar 

  • Bland MM, Levings CSIII, Matzinger DF (1986) The tobacco mitochondrial ATPase subunit 9 gene is closely linked to an open reading frame for a ribosomal protein. Mol Gen Genet 204:8–16

    Google Scholar 

  • Bonen L (1987) The mitochondrial S13 ribosomal protein gene is silent in wheat embryos and seedlings. Nucleic Acids Res 15:10393–10404

    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 

  • Butow RA, Perlman PS, Grossman LI (1985) The unusual var1 gene of yeast mitochondrial DNA. Science 228:1496–1501

    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 

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

    Google Scholar 

  • Dale RMK, McClure BA, Houchins JP (1985) A rapid single-stranded cloning strategy for producing a sequential series of overlapping clones for use in DNA sequencing: Application to sequencing the corn mitochondrial 18 S rDNA. Plasmid 13:31–40

    Google Scholar 

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

    Google Scholar 

  • Dayhoff MO, Eck RV, Park CM (1972) A model of evolutionary change in proteins. In: Atlas of protein sequence and structure. Natl Biomed Res Fnd, Silver Spring, Md, pp 89–99

    Google Scholar 

  • Dewey RE, Levings CSIII, 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 

  • Falconet D, Lejeune B, Quetier F, Gray MW (1984) Evidence for homologous recombination between repeated sequences containing 18S and 5S ribosomal RNA genes in wheat mitochondrial DNA. EMBO J 3:297–302

    Google Scholar 

  • Falconet D, Sevignac M, Quetier F (1988) Nucleotide sequence and determination of the extremities of the 26 S ribosomal RNA gene in wheat mitochondria: evidence for sequence rearrangements in the ribosomal genes of higher plants. Curr Genet 13:75–82

    Google Scholar 

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

    Google Scholar 

  • Fromm H, Edelman M, Koller B, Goloubinoff P, Galun E (1986) The enigma of the gene coding for ribosomal protein S12 in the chloroplast of Nicotiana. Nucleic Acids Res 14:883–898

    Google Scholar 

  • Funatsu G, Wittman HG (1972) Ribosomal proteins: Location of amino-acid replacements in protein S12 isolated from E. coli mutants resistant to streptomycin. J Mol Biol 68:547–550

    Google Scholar 

  • Grabau EA (1985) Nucleotide sequence of the soybean mitochondrial 18S rRNA gene: evidence for a slow rate of divergence in the plant mitochondrial genome. Plant Mol Biol 5:119–124

    Google Scholar 

  • Grienenberger JM, Wintz H, Runeberg-Roos P, Marechal L, Jeannin G, Weil JH (1987) Localization of tRNA genes on maize and wheat mitochondrial genomes. In: von Wettstein D, Chua NH (eds) Plant molecular biology 1987. NATO ASI series A: life sciences. Plenum Publishing, New York, pp 149–161

    Google Scholar 

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

    Google Scholar 

  • Huh TY, Gray MW (1982) Conservation of ribosomal RNA gene arrangements in the mitochondrial DNA of angiosperms. Plant Mol Biol 1:245–249

    Google Scholar 

  • Joyce PBM, Spencer DF, Bonen L, Gray MW (1988) Genes for tRNAAsp, tRNAPro, tRNATyr and two tRNASer in wheat mitochondrial DNA. Plant Mol Biol 10:251–262

    Google Scholar 

  • Kimura M, Kimura J (1987) The complete aminoacid sequence of ribosomal protein S12 from Bacillus stearothermophilus. FEBS Lett 210:91–96

    Google Scholar 

  • Koller B, Fromm H, Galun E, Edelman M (1987) Evidence for the in vivo trans splicing of pre-mRNAs in tobacco chloroplasts. Cell 48:111–119

    Google Scholar 

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

    Google Scholar 

  • Lonsdale DM (1988) Plant mitochondrial genes and sequences. Plant Mol Biol Rep 6:266–273

    Google Scholar 

  • Lonsdale DM, Hodge TP, Fauron CMR (1984) The physical map and organisation of the mitochondrial genome from the fertile cytoplasm of maize. Nucleic Acids Res 12:9249–9261

    Google Scholar 

  • Maniatis T, Fritsch E, Sambrook J (1982) Molecular cloning: A laboratory manual., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Marechal L, Guillemaut P, Grienenberger JM, Jeannin G, Weil JH (1985) Sequence and codon recognition of bean mitochondria and chloroplast tRNAsTrp: evidence for a high degree of homology. Nucleic Acids Res 13:4411–4416

    Google Scholar 

  • Montandon PE, Stutz E (1984) The genes for the ribosomal proteins S12 and S7 are clustered with the gene for the Ef-Tu protein on the chloroplast genome of Euglena gracilis. Nucleic Acids Res 12:2851–2859

    Google Scholar 

  • Mulligan RM, Maloney AP, Walbot V (1988) RNA processing and multiple transcription initiation sites results in transcript size heterogeneity in maize mitochondria. Mol Gen Genet 211:373–380

    Google Scholar 

  • Ohyama K, Fukuzawa H, Kohchi T, Shirai H, Sano T, Sano S, Umesono K, Shiki Y, Takeuchi M, Chang Z, Aota S, Inokuchi H, Ozeki H (1986) Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322:572–574

    Google Scholar 

  • Post LE, Nomura M (1980) DNA sequences from the str operon of E. coli. J Biol Chem 255:4660–4666

    Google Scholar 

  • Quetier F, Lejeune B, Delorme S, Falconet D, Jubier MF (1985) Molecular form and function of the wheat mitochondrial genome. In: van Vloten-Doting L, Groot GSP, Hall TC (eds) Molecular form and function of the plant genomes. NATO ASI series A: life sciences 83. Plenum Press, New York London, pp 413–420

    Google Scholar 

  • Roe BA, Ma DP, Wilson RK, Wong JFH (1985) The complete nucleotide sequence of the Xenopus laevis mitochondrial genome. J Biol Chem 260:9759–9774

    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 

  • Schuster W, Brennicke A (1987) Plastid, nuclear and reverse transcriptase sequences in the mitochondrial genome of Oenothera:is genetic information transferred between organelles via RNA? EMBO J 6:2857–2863

    Google Scholar 

  • Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, Ohto C, Torazawa K, Meng BY, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimida H, Sugiura M (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5:2043–2049

    Google Scholar 

  • Stern DB, Newton KJ (1984) Isolation of intact plant mitochondrial RNA using aurintricarboxylic acid. Plant Mol Biol Rep 2:8–15

    Google Scholar 

  • Weiner AM, Deininger PL, Efstratiadis A (1986) Nonviral retroposons: Genes, pseudogenes, and transposable elements generated by the reverse flow of genetic information. Annu Rev Biochem 55:631–662

    Google Scholar 

  • Wintz H, Grienenberger JM, Weil JH, Lonsdale DM (1988) Location and nucleotide sequence of two tRNA genes and a tRNA pseudo-gene in the maize mitochondrial genome: evidence for the transcription of a chloroplast gene in mitochondria. Curr Genet 13:247–254

    Google Scholar 

  • Wissinger B, Hiesel R, Schuster W, Brennicke A (1988) The NADH-dehydrogenase subunit 5 gene in Oenothera mitochondria contains two introns and is co-transcribed with the 5S rRNA gene. Mol Gen Genet 212:56–65

    Google Scholar 

  • Wittmann-Liebold B (1986) Ribosomal proteins: their structure and evolution. In: Hardesty B, Kramer G (eds) Structure, function and genetics of ribosomes. Springer, New York Heidelberg Berlin, pp 326–361

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by D.M. Lonsdale

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gualberto, J.M., Wintz, H., Weil, JH. et al. The genes coding for subunit 3 of NADH dehydrogenase and for ribosomal protein S12 are present in the wheat and maize mitochondrial genomes and are co-transcribed. Mol Gen Genet 215, 118–127 (1988). https://doi.org/10.1007/BF00331312

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00331312

Key words

Navigation