Abstract
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.
Similar content being viewed by others
References
Aubert D, Bisanz-Seyer C, Herzog M (1992) Mitochondrialrps14 is a transcribed and edited pseudogene inArabidopsis thaliana. Plant Mol Biol 20:1169–1174
Beckman DL, Trawick DR, Kranz RG (1992) Bacterial cytochromesc biogenesis. Genes Dev 6:268–283
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
Binder S, Brennicke A (1993) Transcription initiation sites in mitochondria ofOenothera berteriana. J Biol Chem 268:7849–7855
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
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
Bonen L (1987) The mitochondrial S13 ribosomal protein gene is silent in wheat embryos and seedlings. Nucleic Acids Res 15:10393–10404
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
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
Brandt P, Unseld M, Eckert-Ossenkopp U, Brennicke A (1993) Anrps14 pseudogene is transcribed and edited inArabidopsis mitochondria. Curr Genet 24:330–336
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
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
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
Cooper AA, Stevens TH (1995) Protein splicing: self-splicing of genetically mobile elements at the protein level. Trends Biochem Sci 20:351–356
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
Davis EO, Jenner PJ, Brooks PC, Colston MJ, Sedgwick SG (1992) Protein splicing in the maturation ofMycobacterium tuberculosis RecA protein. Cell 71:201–210
de Bruijn MH (1983)Drosophila melanogaster mitochondrial DNA: a novel organization and genetic code. Nature 304:234–241
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
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
Grabau E, Havlik M, Gesteland R (1988) Chimeric organization of two genes for the soybean mitochondrial ATPase subunit 6. Curr Genet 13:83–89
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
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
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
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
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
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
Jekabsons W, Schuster W (1995)orf250 encodes a second subunit of an ABC-type heme transporter inOenothera mitochondria. Mol Gen Genet 246:166–173
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
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
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
Kozak M (1983) Comparison of initiation of protein synthesis in procaryotes, eucaryotes, and organelles. Microbiol Rev 47:1–45
Kranz RG (1989) Isolation of mutants and genes involved in cytochromes c biosynthesis inRhodobacter capsulatus. J Bacteriol 171:456–464
Kranz RG, Beckman DL (1994) Cytochrome biogenesis. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer Academic, Amsterdam, pp 1368
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
Michel F, Umesono K, Ozeki H (1989) Comparative and functional anatomy of group II catalytic introns — a review. Gene 82:5–30
Newton KJ (1988) Plant mitochondrial genomes: organization, expression and variation. Annu Rev Plant Physiol Plant Mol Biol 39:503–532
Nugent JM, Palmer JD (1991) RNA-mediated transfer of thecoxII from the mitochondrion to the nucleus during flowering plant evolution. Cell 66:473–481
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
Palmer JD, Herbon LA (1988) Plant mitochondrial DNA evolves rapidly in structure, but slowly in sequence. J Mol Evol 28:87–97
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
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
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
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
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
Sanger F, Nicklen S, Coulson A (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467
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
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
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
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
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
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
Wahleithner JA, Wolstenholme DR (1988) Ribosomal protein S14 genes in broad bean mitochondrial DNA. Nucleic Acids Res 16:6897–6913
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
Author information
Authors and Affiliations
Additional information
Communicated by A. Kondorosi
Rights and permissions
About this article
Cite this article
Handa, H., Bonnard, G. & Grienenberger, J.M. 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
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02173775