Skip to main content
SpringerLink
Log in

A gene proposed to encode a transmembrane domain of an ABC transporter is expressed in wheat mitochondria

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

Abstract

In a study of transcribed regions of the wheat mitochondrial genome, we identified an open reading frame of 720 bp, which was consequently designated orf240. The amino acid sequence deduced from orf240 shows a high level of similarity with HelC, a protein essential for c-type cytochrome biogenesis in the photosynthetic purple bacterium Rhodobacter capsulatus. HelC is part of a putative heme ABC transporter. An open reading frame homologous to orf240 is present in the mitochondrial genome of Marchantia polymorpha. The wheat gene is expressed as an mRNA of 2.8 kb, which is further processed to smaller transcripts. The transcript is highly edited, with 36 C to U modifications found in the coding region of all cDNAs sequenced. RNA editing is responsible for changes in 14% of the amino acids specified by the transcript.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

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

    Google Scholar 

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

    Google Scholar 

  • Blattner FR, Burland V, Plunkett III G, 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 

  • Bonen L (1991) The mitochondrial genome: so simple yet so complex. Curr Opin Genet Dev 1:515–522

    Google Scholar 

  • Braun HP, Emmermann M, Kruft V, Schmitz UK (1992) Cytochrome c 1 from potato: a protein with a presequence for targeting to the mitochondrial intermembrane space. Mol Gen Genet 231:217–225

    Google Scholar 

  • Covello PS, Gray MW (1991) Sequence analysis of wheat mitochondrial transcripts capped in vitro — definitive identification of transcription initiation sites. Curr Genet 20:245–251

    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 c 552 from Escherichia coli: not a hexahaem but a 50 kDa tetrahaem nitrite reductase. Mol Microbiol 9:1255–1265

    Google Scholar 

  • Devereux J, Haeberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395

    Google Scholar 

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

    Google Scholar 

  • Gray MW, Hanic-Joyce PJ, Covello PS (1992) Transcription, processing and editing in plant mitochondria. Annu Rev Plant Physiol Plant Mol Biol 43:145–175

    Google Scholar 

  • Gualberto JM, Domon C, Weil JH, Grienenberger JM (1990) Structure and transcription of the gene coding for subunit 3 of cytochrome oxidase in wheat mitochondria. Curr Genet 17:41–47

    Google Scholar 

  • Gualberto JM, Wintz H, Weil JH, Grienenberger JM (1988) 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

    Google Scholar 

  • Gualberto JM, Bonnard G, Lamattina L, Grienenberger JM (1991) Expression of the wheat mitochondrial nad3-rps12 transcription unit: correlation between editing and mRNA maturation. Plant Cell 3:1109–1120

    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 

  • Hartl FU, Neupert W (1990) Protein sorting to mitochondria: Evolutionary conservations of folding and assembly. Science 247:930–938

    Google Scholar 

  • Hartl FU, Ostermann J, Guiard B, Neupert W (1987) Successive translocations into and out of the mitochondrial matrix: targetting of proteins to the intermembrane space by a bipartite signal peptide. Cell 51:1027–1037

    Google Scholar 

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

    Google Scholar 

  • Hiratsuka J, Shimada H, Whittier R, Ishibashi T, Sakamoto M, Mori M, Kondo C, Honji Y, Sun CR, Meng BY, Li YQ, Kanno A, Nishikawa Y, Hirai A, Shinozaki K, Sugiura M (1989) The complete sequence of the rice (Oryza sativa) chloroplast genome: Intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of cereals. Mol Gen Genet 217:185–194

    Google Scholar 

  • Hyde SC, Emsley P, Hartshorn M, Mimmack MM, Gileadi U, Pearce SR, Gallagher MP, Gill DR, Hubbard RE, Higgins CF (1990) Structural model of ATP-binding proteins associated with cystic fibrosis, multidrug resistance and bacterial transport. Nature 346:362–365

    Google Scholar 

  • Kerppola RE, Shyamala UK, Klebba P, Ames GF-L (1991) The membrane-bound proteins of periplasmic permeases form a complex. J Biol Chem 266:9857–9865

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132

    Google Scholar 

  • Lamattina L, Grienenberger JM (1991) RNA editing of the transcript coding for subunit-4 of NADH dehydrogenase in wheat mitochondria — uneven distribution of the editing sites among the 4 exons. Nucleic Acids Res 19:3275–3282

    Google Scholar 

  • Lamattina L, Gonzalez D, Gualberto JM, Grienenberger JM (1993) Higher plant mitochondria encode an homologue of the nuclear-coded 30 kDa subunit of bovine mitochondrial complex I. Eur J Biochem 217:831–838

    Google Scholar 

  • Lill R, Stuart RA, Drygas NE, Nargang FE, Neupert W (1992) Import of cytochrome c heme lyase into mitochondria: a novel pathway into the intermembrane space. EMBO J 11:449–456

    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 

  • 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 c 1. Role of cytochrome c 1 heme lyase and of the two proteolytic processing steps during import into mitochondria. J Biol Chem 264:10156–10168

    Google Scholar 

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

    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 — a primitive form of plant mitochondrial genome. J Mol Biol 223:1–7

    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 

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

    Google Scholar 

  • Pritchard AE, Seilhamer JJ, Mahalingam R, Sable CL, Venuti SE, Cummings DJ (1990) Nucleotide sequence of the mitochondrial genome of Paramecium. Nucleic Acids Res 18:173–180

    Google Scholar 

  • Quétier 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 plant genomes. (NATO ASI series A: Life sciences) Plenum Press, New York-London, pp 413–420

    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 

  • 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 

  • Valentin K, Maid U, Emich A, Zetsche K (1992) Organization and expression of a phycobiliprotein gene cluster from the unicellular alga Cyanidium caldarium. Plant Mol Biol 20:267–276

    Google Scholar 

  • Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut de Biologie Moléculaire des Plantes du CNRS, Université Louis Pasteur, 12 rue du Général Zimmer, F-67084, Strasbourg, France

    Géraldine Bonnard & Jean Michel Grienenberger

Authors
  1. Géraldine Bonnard
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jean Michel Grienenberger
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by R. Hagemann

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bonnard, G., Grienenberger, J.M. A gene proposed to encode a transmembrane domain of an ABC transporter is expressed in wheat mitochondria. Molec. Gen. Genet. 246, 91–99 (1995). https://doi.org/10.1007/BF00290137

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00290137

Key words

Search

Navigation