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Oenothera mitochondrial orf454, a gene involved in cytochrome c biogenesis corresponds to orf169 and orf322 of Marchantia

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Abstract

We have characterized a mitochondrial gene in Oenothera, designated orf454, capable of encoding a component of the cytochrome c biogenesis system. This open reading frame is interrupted by an intron of 941 nucleotides showing high similarity to a group II intron residing in the rpl2 gene. RNA editing, which is observed at 18 cytidine positions within the orf454 reading frame, improves the similarity to protein-coding sequences in bacteria and higher plants and removes the last 16 amino acids. orf454 also shows high sequence similarity to two overlapping reading frames (orf169 and orf322) of Marchantia mitochondria. These ORFs belong to an operon-like cluster of genes in the liverwort that is not conserved in Oenothera mitochondria. However, in bacteria these reading frames are organized like the Marchantia gene cluster. It has been shown by genetical analysis in Rhodobacter capsulatus that these genes are essential for cytochrome c biogenesis. Genes of bacterial operons — ccl1 in Rhodobacter and yejR and nrfE in Escherichia coli — show high sequence similarity to the mitochondrial reading frames orf577 and orf454 of Oenothera. orf454, which we describe here, is homologous to the C-terminal region of these bacterial genes, while the previously described orf577 is homologous to the N-terminal region.

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References

  • Ames GF-L (1986) Bacterial periplasmic transport systems: structure, mechanism, and evolution. Annu Rev Biochem 55:397–425

    Google Scholar 

  • Beckman DL, Kranz RG (1993) Cytochrome c biogenesis in a photosynthetic bacterium requires a periplasmic thioredoxinlike protein. Proc Natl Acad Sci USA 90 2179–2183

    Google Scholar 

  • Beckman DL, Trawick DR, Kranz RG (1992) Bacterial cytochrome c biogenesis. Genes Dev 6 268–283

    Google Scholar 

  • Blattner FR, Burland V, Plunkett G III, Sofia HJ, Daniels DL (1993) Analysis of the Escherichia coli genome. IV. DNA sequence of the region from 89.2 to 92.8 minutes. Nucleic Acids Res 21:5408–5417

    Google Scholar 

  • Chanut FA, Grabau EA, Gesteland RF (1993) Complex organization of the soybean mitochondrial genome: recombination repeats and multiple transcripts at the atpA loci. Curr Genet 23:234–247

    Google Scholar 

  • Covello PS, Gray MW (1989) RNA editing in plant mitochondria. Nature 341:662–666

    Google Scholar 

  • Darwin A, Hussain H, Griffiths L, Grove J, Sambongi Y, Busby S, Cole J (1993) Regulation and sequence of the structural gene for cytochrome c552 from Escherichia coli: not a hexahaem but a 50 kDa tetrahaem nitrite reductase. Mol Microbiol 9:1255–1265

    Google Scholar 

  • Gonzalez DH, Bonnard G, Grienenberger J-M (1993) A gene involved in the biogenesis of cytochromes is co-transcribed with a ribosomal protein gene in wheat mitochondria. Curr Genet 24:248–255

    Google Scholar 

  • Gualberto JM, Lamattina L, Bonnard G, Weil J-H, Grienenberger J-M (1989) RNA editing in wheat mitochondria results in the conservation of protein sequences. Nature 341:660–662

    Google Scholar 

  • Hiesel R, Wissinger B, Schuster W, Brennicke A (1989) RNA editing in plant mitochondria. Science 246:1632–1634

    Google Scholar 

  • Higgins CF (1992) ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8:67–113

    Google Scholar 

  • Jekabsons W, Schuster W (1995) orf250 encodes a second subunit of an ABC-type heme transporter in Oenothera mitochondria. Mol Gen Genet 246:166–173

    Google Scholar 

  • Lipman DJ, Pearson WR (1985) Rapid and sensitive similarity searches. Science 227: 1435–1441

    Google Scholar 

  • Michel F, Umesono K, Ozeki H (1989) Comparative and functional anatomy of group II catalytic introns — a review. Gene 82: 530

    Google Scholar 

  • Nicholson DW Neupert W (1989) Import of cytochrome c into mitochondria: reduction of heme, mediated by NADH and flavin nucleotides, is obligatory for its covalent linkage to apocytochrome c. Proc Natl Acad Sci USA 86:4340–4344

    Google Scholar 

  • Nicholson DW, Stuart RA, Neupert W (1989) Biogenesis of cytochrome c1. J Biol Chem 264:10156–10168

    Google Scholar 

  • Oda K, Yamato K, Ohta E, Nakamura Y, Takemura M, Nozato N, Akashi K, Kanegae T, Ogura Y, Kohchi T, Ohyama K (1992) Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA. J Mol Biol 223: 1–7

    Google Scholar 

  • Pearson WR, Lipman DJ (1988) Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 85:2444–2448

    Google Scholar 

  • Ramseier TM, Winteler HV, Hennecke H (1991) Discovery and sequence analysis of bacterial genes involved in the biogenesis of c-type cytochromes. J Biol Chem 266:7793–7803

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    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 (1994) The highly edited orf206 in 0enothera mitochondria may encode a component of a heme transporter involved in cytochrome c biogenesis. Plant Mol Biol 25: 33–42

    Google Scholar 

  • Schuster W, Hiesel R, Wissinger B, Schobel W, Brennicke A (1989) Isolation and analysis of plant mitochondria and their genomes. In: Shaw CH (ed) Plant molecular biology. IRL Press, Oxford, Washington DC, pp 79–1020

    Google Scholar 

  • Schuster W Combettes B, Flieger K, Brennicke A (1993) A plant mitochondrial gene encodes a protein involved in cytochrome c biogenesis. Mol Gen Genet 239:49–57

    Google Scholar 

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Communicated by R. Hagemann

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Gruska, I., Jekabsons, W. & Schuster, W. Oenothera mitochondrial orf454, a gene involved in cytochrome c biogenesis corresponds to orf169 and orf322 of Marchantia . Molec. Gen. Genet. 247, 529–536 (1995). https://doi.org/10.1007/BF00290343

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  • DOI: https://doi.org/10.1007/BF00290343

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