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EMBO J. Nov 1992; 11(11): 3815–3820.
PMCID: PMC556890

Silent mitochondrial and active nuclear genes for subunit 2 of cytochrome c oxidase (cox2) in soybean: evidence for RNA-mediated gene transfer.


In most plants and other eukaryotes investigated, the mitochondrial genome carries the gene encoding subunit 2 of cytochrome c oxidase (cox2). In this paper, we show that the previously reported mitochondrial cox2 of soybean is actually silent, and that there is an expressed, single-copy, nucleus-encoded cox2. Molecular cloning and sequence analysis of cox2 cDNA and genomic clones show that the soybean nuclear gene encodes an N-terminal extension that resembles a signal sequence for mitochondrial import and whose coding sequence is separated by an intron from that corresponding to mtDNA-encoded cox2. Comparison of soybean mitochondrial and nuclear cox2 sequences clearly indicates that in an ancestor of soybean, cox2 was transferred from the mitochondrion to the nucleus via a C-to-U edited RNA intermediate.

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Selected References

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  • Baldauf SL, Palmer JD. Evolutionary transfer of the chloroplast tufA gene to the nucleus. Nature. 1990 Mar 15;344(6263):262–265. [PubMed]
  • Bogorad L. Evolution of organelles and eukaryotic genomes. Science. 1975 May 30;188(4191):891–898. [PubMed]
  • Bonen L, Gray MW. Organization and expression of the mitochondrial genome of plants I. The genes for wheat mitochondrial ribosomal and transfer RNA: evidence for an unusual arrangement. Nucleic Acids Res. 1980 Jan 25;8(2):319–335. [PMC free article] [PubMed]
  • Bonen L, Boer PH, Gray MW. The wheat cytochrome oxidase subunit II gene has an intron insert and three radical amino acid changes relative to maize. EMBO J. 1984 Nov;3(11):2531–2536. [PMC free article] [PubMed]
  • Brown TA, Waring RB, Scazzocchio C, Davies RW. The Aspergillus nidulans mitochondrial genome. Curr Genet. 1985;9(2):113–117. [PubMed]
  • Cattaneo R. Different types of messenger RNA editing. Annu Rev Genet. 1991;25:71–88. [PubMed]
  • Cavalier-Smith T. The simultaneous symbiotic origin of mitochondria, chloroplasts, and microbodies. Ann N Y Acad Sci. 1987;503:55–71. [PubMed]
  • Corpet F. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 1988 Nov 25;16(22):10881–10890. [PMC free article] [PubMed]
  • Covello PS, Gray MW. RNA editing in plant mitochondria. Nature. 1989 Oct 19;341(6243):662–666. [PubMed]
  • Covello PS, Gray MW. Differences in editing at homologous sites in messenger RNAs from angiosperm mitochondria. Nucleic Acids Res. 1990 Sep 11;18(17):5189–5196. [PMC free article] [PubMed]
  • Covello PS, Gray MW. RNA sequence and the nature of the CuA-binding site in cytochrome c oxidase. FEBS Lett. 1990 Jul 30;268(1):5–7. [PubMed]
  • Farrelly F, Butow RA. Rearranged mitochondrial genes in the yeast nuclear genome. Nature. 1983 Jan 27;301(5898):296–301. [PubMed]
  • Gantt JS, Baldauf SL, Calie PJ, Weeden NF, Palmer JD. Transfer of rpl22 to the nucleus greatly preceded its loss from the chloroplast and involved the gain of an intron. EMBO J. 1991 Oct;10(10):3073–3078. [PMC free article] [PubMed]
  • Gellissen G, Michaelis G. Gene transfer. Mitochondria to nucleus. Ann N Y Acad Sci. 1987;503:391–401. [PubMed]
  • Grabau EA. Cytochrome oxidase subunit II gene is adjacent to an initiator methionine tRNA gene in soybean mitochondrial DNA. Curr Genet. 1987;11(4):287–293. [PubMed]
  • Gray MW. The evolutionary origins of organelles. Trends Genet. 1989 Sep;5(9):294–299. [PubMed]
  • Gray MW. Origin and evolution of mitochondrial DNA. Annu Rev Cell Biol. 1989;5:25–50. [PubMed]
  • Gray MW, Doolittle WF. Has the endosymbiont hypothesis been proven? Microbiol Rev. 1982 Mar;46(1):1–42. [PMC free article] [PubMed]
  • Gualberto JM, Lamattina L, Bonnard G, Weil JH, Grienenberger JM. RNA editing in wheat mitochondria results in the conservation of protein sequences. Nature. 1989 Oct 19;341(6243):660–662. [PubMed]
  • Helms C, Dutchik JE, Olson MV. A lambda DNA protocol based on purification of phage on DEAE-cellulose. Methods Enzymol. 1987;153:69–82. [PubMed]
  • Hiesel R, Wissinger B, Schuster W, Brennicke A. RNA editing in plant mitochondria. Science. 1989 Dec 22;246(4937):1632–1634. [PubMed]
  • Hoch B, Maier RM, Appel K, Igloi GL, Kössel H. Editing of a chloroplast mRNA by creation of an initiation codon. Nature. 1991 Sep 12;353(6340):178–180. [PubMed]
  • Holm L, Saraste M, Wikström M. Structural models of the redox centres in cytochrome oxidase. EMBO J. 1987 Sep;6(9):2819–2823. [PMC free article] [PubMed]
  • Horwich AL, Cheng M, West A, Pollock RA. Mitochondrial protein import. Curr Top Microbiol Immunol. 1991;170:1–42. [PubMed]
  • Jacobs HT, Posakony JW, Grula JW, Roberts JW, Xin JH, Britten RJ, Davidson EH. Mitochondrial DNA sequences in the nuclear genome of Strongylocentrotus purpuratus. J Mol Biol. 1983 Apr 25;165(4):609–632. [PubMed]
  • Joyce PB, Gray MW. Chloroplast-like transfer RNA genes expressed in wheat mitochondria. Nucleic Acids Res. 1989 Jul 25;17(14):5461–5476. [PMC free article] [PubMed]
  • Jukes TH, Osawa S. The genetic code in mitochondria and chloroplasts. Experientia. 1990 Dec 1;46(11-12):1117–1126. [PubMed]
  • Kudla J, Igloi GL, Metzlaff M, Hagemann R, Kössel H. RNA editing in tobacco chloroplasts leads to the formation of a translatable psbL mRNA by a C to U substitution within the initiation codon. EMBO J. 1992 Mar;11(3):1099–1103. [PMC free article] [PubMed]
  • Maréchal L, Guillemaut P, Grienenberger JM, Jeannin G, Weil JH. Sequence and codon recognition of bean mitochondria and chloroplast tRNAsTrp: evidence for a high degree of homology. Nucleic Acids Res. 1985 Jun 25;13(12):4411–4416. [PMC free article] [PubMed]
  • Mogen BD, MacDonald MH, Graybosch R, Hunt AG. Upstream sequences other than AAUAAA are required for efficient messenger RNA 3'-end formation in plants. Plant Cell. 1990 Dec;2(12):1261–1272. [PMC free article] [PubMed]
  • Nugent JM, Palmer JD. RNA-mediated transfer of the gene coxII from the mitochondrion to the nucleus during flowering plant evolution. Cell. 1991 Aug 9;66(3):473–481. [PubMed]
  • Obar R, Green J. Molecular archaeology of the mitochondrial genome. J Mol Evol. 1985;22(3):243–251. [PubMed]
  • Palmer JD. Contrasting modes and tempos of genome evolution in land plant organelles. Trends Genet. 1990 Apr;6(4):115–120. [PubMed]
  • Pratje E, Mannhaupt G, Michaelis G, Beyreuther K. A nuclear mutation prevents processing of a mitochondrially encoded membrane protein in Saccharomyces cerevisiae. EMBO J. 1983;2(7):1049–1054. [PMC free article] [PubMed]
  • Schuster W, Brennicke A. Plastid, nuclear and reverse transcriptase sequences in the mitochondrial genome of Oenothera: is genetic information transferred between organelles via RNA? EMBO J. 1987 Oct;6(10):2857–2863. [PMC free article] [PubMed]
  • Stanford A, Bevan M, Northcote D. Differential expression within a family of novel wound-induced genes in potato. Mol Gen Genet. 1989 Jan;215(2):200–208. [PubMed]
  • Stern DB, Lonsdale DM. Mitochondrial and chloroplast genomes of maize have a 12-kilobase DNA sequence in common. Nature. 1982 Oct 21;299(5885):698–702. [PubMed]
  • Thorsness PE, Fox TD. Escape of DNA from mitochondria to the nucleus in Saccharomyces cerevisiae. Nature. 1990 Jul 26;346(6282):376–379. [PubMed]
  • Lau CS, McLaren M, Saniabadi A, Scott N, Belch JJ. The pharmacological effects of cicaprost, an oral prostacyclin analogue, in patients with Raynaud's syndrome secondary to systemic sclerosis--a preliminary study. Clin Exp Rheumatol. 1991 May-Jun;9(3):271–273. [PubMed]
  • van den Boogaart P, Samallo J, Agsteribbe E. Similar genes for a mitochondrial ATPase subunit in the nuclear and mitochondrial genomes of Neurospora crassa. Nature. 1982 Jul 8;298(5870):187–189. [PubMed]
  • von Heijne G. Why mitochondria need a genome. FEBS Lett. 1986 Mar 17;198(1):1–4. [PubMed]
  • Wolfe KH, Li WH, Sharp PM. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci U S A. 1987 Dec;84(24):9054–9058. [PMC free article] [PubMed]

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