Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

The rapeseed mitochondrial gene encoding a homologue of the bacterial protein Ccl1 is divided into two independently transcribed reading frames

  • 60 Accesses

  • 16 Citations


In the rapeseed mitochondrial genome we identified sequences that have a high similarity to those of a bacterial gene involved in the biogenesis of cytochromesc designatedccl1. The structure of this gene is quite unusual. In rapeseed mitochondria, theccl1-homologous (orf577) sequence is divided into two parts, which are at least 45 kb apart. These two parts are transcribed separately and their transcripts are edited similarly to the homologous transcripts of wheat andOenothera. However it was impossible to identify a mature transcript covering the whole coding region, a result that excludes a trans-splicing event. No other copy of this gene was found in either the nuclear genome or the mitochondrial genome. The protein product oforf577 is present in rapeseed mitochondria. These results raise the possibility that this divided gene might be functional and active in rapeseed mitochondria through a novel mechanism of gene expression.

This is a preview of subscription content, log in to check access.


  1. Aubert D, Bisanz-Seyer C, Herzog M (1992) Mitochondrialrps14 is a transcribed and edited pseudogene inArabidopsis thaliana. Plant Mol Biol 20:1169–1174

  2. Beckman DL, Trawick DR, Kranz RG (1992) Bacterial cytochromesc biogenesis. Genes Dev 6:268–283

  3. Binder S, Marchfelder A, Brennicke A, Wissinger B (1992) RNA editing in trans-splicing intron sequences ofnad2 mRNAs inOenothera mitochondria. J Biol Chem 267:7615–7623

  4. Binder S, Brennicke A (1993) Transcription initiation sites in mitochondria ofOenothera berteriana. J Biol Chem 268:7849–7855

  5. Bland MM, Levings CS III, 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

  6. Bock H, Brennicke A, Schuster W (1994)Rps3 andrpl16 genes do not overlap inOenothera mitochondria: GTG as a potential translation initiation codon in plant mitochondria? Plant Mol Biol 24:811–818

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

  8. Bonhomme S, Budar F, Lancelin D, Small I, Defrance M-C, Pelletier G (1992) Sequence and transcript analysis of theNco2.5 Ogura-specific fragment correlated with cytoplasmic male sterility inBrassica cybrids. Mol Gen Genet 235:340–348

  9. Bonnard G, Grienenberger JM (1995) A gene proposed to encode a transmembrane domain of an ABC transporter is expressed in wheat mitochondria. Mol Gen Genet 246:91–99

  10. Brandt P, Unseld M, Eckert-Ossenkopp U, Brennicke A (1993) Anrps14 pseudogene is transcribed and edited inArabidopsis mitochondria. Curr Genet 24:330–336

  11. Burke-Agüero DH, Hearst JE (1990) An RNA Holliday junction? Structural and dynamic consideration of the bacteriophage T4 gene 60 interruption. J Mol Biol 213:199–201

  12. Chapdelaine Y, Bonen L (1991) The wheat mitochondrial gene for subunit I of the NADH dehydrogenase complex: atrans-splicing model for this gene-in-pieces. Cell 65:465–472

  13. Clary DO, Wolstenholme DR (1983) Nucleotide sequence of a segment ofDrosophila mitochondrial DNA that contains the genes for cytochromec oxidase subunits II and III and ATPase subunit 6. Nucleic Acids Res 11:4211–4227

  14. Cooper AA, Stevens TH (1995) Protein splicing: self-splicing of genetically mobile elements at the protein level. Trends Biochem Sci 20:351–356

  15. Covello PS, Gray MW (1992) Silent mitochondrial and active nuclear genes for subunit 2 of cytochromec oxidase (cox2) in soybean: evidence for RNA-mediated gene transfer. EMBO J 11:3815–3820

  16. Davis EO, Jenner PJ, Brooks PC, Colston MJ, Sedgwick SG (1992) Protein splicing in the maturation ofMycobacterium tuberculosis RecA protein. Cell 71:201–210

  17. de Bruijn MH (1983)Drosophila melanogaster mitochondrial DNA: a novel organization and genetic code. Nature 304:234–241

  18. Folkerts O, Hanson MR (1989) Three copies of a single recombination repeat occur on the 443 kb mastercircle of thePetunia hybrida 3074 mitochondrial genome. Nucleic Acids Res 17:7345–7357

  19. Gonzalez DH, Bonnard G, Grienenberger JM (1993) A gene involved in the biogenesis ofc-type cytochromes is co-transcribed with a ribosomal protein gene in wheat mitochondria. Curr Genet 21:248–255

  20. Grabau E, Havlik M, Gesteland R (1988) Chimeric organization of two genes for the soybean mitochondrial ATPase subunit 6. Curr Genet 13:83–89

  21. Grohmann L, Brennicke A, Schuster W (1992) The mitochondrial gene encoding ribosomal protein S12 has been translocated to the nuclear genome inOenothera. Nucleic Acids Res 20:5641–5646

  22. Gruska I, Jekabsons W, Schuster W (1995)Oenothera mitochondrialorf454, a gene involved in cytochromec biogenesis corresponds toorf169 andorf322 ofMarchantia. Mol Gen Genet 247:529–536

  23. Handa H, Nakajima K (1992a) Different organization and altered transcription of the mitochondrialatp6 gene in the male-sterile cytoplasm of rapeseed (Brassica napus L.). Curr Genet 21:153–159

  24. Handa H, Nakajima K (1992b) RNA editing ofatp6 transcripts from the male-sterile and normal cytoplasms of rapeseed (Brassica napus L.). FEBS Lett 310:111–114

  25. Hodges RA, Perler FB, Noren CJ, Jack WE (1992) Protein splicing removes the intervening sequence in an Archaean DNA polymerase. Nucleic Acids Res 20:6153–6157

  26. Huang WM, Ao S-Z, Casjens S, Orlandi R, Zeikus R, Weiss R, Winge D, Fang M (1988) A persistent untranslated sequence within bacteriophage T4 DNA topoisomerase gene 60. Science 239:1005–1011

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

  28. Kane PM, Yamashiro CT, Wolczyk DF, Goebl M, Neff N, Stevens TH (1990) Protein splicing converts the yeastTFP1 gene product to the 69 kDa subunit of the vacuolar H+-adenosine triphosphatase. Science 250:651–657

  29. Knoop V, Schuster W, Wissinger B, Brennicke A (1991)Trans splicing integrates an exon of 22 nucleotides into thenad5 mRNA in higher plant mitochondria. EMBO J 10:3483–3493

  30. Knoop V, Kloska S, Wissinger B, Brennicke A (1994) On the identification of group II introns in nucleotide sequence data. J Mol Biol 242:389–396

  31. Kozak M (1983) Comparison of initiation of protein synthesis in procaryotes, eucaryotes, and organelles. Microbiol Rev 47:1–45

  32. Kranz RG (1989) Isolation of mutants and genes involved in cytochromes c biosynthesis inRhodobacter capsulatus. J Bacteriol 171:456–464

  33. Kranz RG, Beckman DL (1994) Cytochrome biogenesis. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer Academic, Amsterdam, pp 1368

  34. Le S-Y, Chen J-H, Maizel JV Jr (1993) Identification of unusual RNA folding patterns by bacteriophage T4 gene 60. Gene 124:21–28

  35. Michel F, Umesono K, Ozeki H (1989) Comparative and functional anatomy of group II catalytic introns — a review. Gene 82:5–30

  36. Newton KJ (1988) Plant mitochondrial genomes: organization, expression and variation. Annu Rev Plant Physiol Plant Mol Biol 39:503–532

  37. Nugent JM, Palmer JD (1991) RNA-mediated transfer of thecoxII from the mitochondrion to the nucleus during flowering plant evolution. Cell 66:473–481

  38. 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 liver-wortMarchanta polymorphia mitochondrial DNA. J Mol Biol 223:1–7

  39. Palmer JD, Herbon LA (1988) Plant mitochondrial DNA evolves rapidly in structure, but slowly in sequence. J Mol Evol 28:87–97

  40. Patell V, Bonnard G, Lamattina L, Gualberto JM, Grienenberger JM (1992)Trans-, cis-splicing and RNA editing fornad2 gene expression in wheat mitochondria. In Brennicke A (ed) Proceedings of the HFSP Workshop on RNA Editing in Plant Mitochondria. Berlin, pp 69

  41. Pruitt KD, Hanson MR (1989) Cytochrome oxidase subunit II sequences inPetunia mitochondria: two intron-containing genes and an intron-less pseudogene associated with cytoplasmic male sterility. Curr Genet 16:281–291

  42. Rochaix J-D, Kuchka M, Mayfield S, Schirmer-Rahire M, Girard-Bascou J, Bennoun P (1989) Nuclear and chloroplast mutations affect the synthesis or stability of the chloroplastpsbC gene product inChlamydomonas reinhardtii. EMBO J 8:1013–1021

  43. Rothenberg M, Hanson MR (1987) Different transcript abundance of two divergent ATP synthase subunit 9 genes in the mitochondrial genome ofPetunia hybrida. Mol Gen Genet 209:21–27

  44. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

  45. Sanger F, Nicklen S, Coulson A (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467

  46. Schuster W (1994) The highly editedorf206 inOenothera mitochondria may encode a component of a heme transporter involved in cytochromec biogenesis. Plant Mol Biol 25:33–42

  47. Schuster W, Brennicke A (1991) RNA editing makes mistakes in plant mitochondria: editing loses sense in transcripts ofrps19 pseudogene and in creating stop codons incoxI andrps3 mRNAs ofOenothera. Nucleic Acids Res 19:6923–6928

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

  49. Senda M, Harada T, Mikami T, Sugiura M, Kinoshita T (1991) Genomic organization and sequence analysis of the cytochrome oxidase subunit II gene from normal and male-sterile mitochondria in sugar beet. Curr Genet 19:175–181

  50. Sutton CA, Conklin PL, Pruitt KD, Jay Calfee A, Cobb AG, Hanson MR (1993) Editing ofrps3/rpl16 transcripts creates a premature truncation of therpl16 open reading frame. Curr Genet 23:472–476

  51. Thomson MC, Macfarlane JL, Beagley CT, Wolstenholme DR (1994) RNA editing ofmat-r transcripts in maize and soybean increases similarity of the encoded protein to fungal and bryophyte group II intron maturases: evidence thatmat-r encodes a functional protein. Nucleic Acids Res 22:5745–5752

  52. Wahleithner JA, Wolstenholme DR (1988) Ribosomal protein S14 genes in broad bean mitochondrial DNA. Nucleic Acids Res 16:6897–6913

  53. Wissinger B, Schuster W, Brennicke A (1991)Trans splicing inOenothera mitochondria:nad1 mRNAs are edited in exon andrans-splicing group II intron sequences. Cell 65:473–482

Download references

Author information

Correspondence to H. Handa.

Additional information

Communicated by A. Kondorosi

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Handa, H., Bonnard, G. & Grienenberger, J.-. The rapeseed mitochondrial gene encoding a homologue of the bacterial protein Ccl1 is divided into two independently transcribed reading frames. Molec. Gen. Genet. 252, 292–302 (1996). https://doi.org/10.1007/BF02173775

Download citation

Key words

  • Rapeseed
  • Plant mitochondria
  • Cytochromec biogenesis
  • RNA editing
  • ccl1