Skip to main content
SpringerLink
Log in

The complete nucleotide sequence and multipartite organization of the tobacco mitochondrial genome: comparative analysis of mitochondrial genomes in higher plants

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

Abstract

Tobacco is a valuable model system for investigating the origin of mitochondrial DNA (mtDNA) in amphidiploid plants and studying the genetic interaction between mitochondria and chloroplasts in the various functions of the plant cell. As a first step, we have determined the complete mtDNA sequence of Nicotiana tabacum. The mtDNA of N. tabacum can be assumed to be a master circle (MC) of 430,597 bp. Sequence comparison of a large number of clones revealed that there are four classes of boundaries derived from homologous recombination, which leads to a multipartite organization with two MCs and six subgenomic circles. The mtDNA of N. tabacum contains 36 protein-coding genes, three ribosomal RNA genes and 21 tRNA genes. Among the first class, we identified the genes rps1 and ψrps14, which had previously been thought to be absent in tobacco mtDNA on the basis of Southern analysis. Tobacco mtDNA was compared with those of Arabidopsis thaliana, Beta vulgaris, Oryza sativa and Brassica napus. Since repeated sequences show no homology to each other among the five angiosperms, it can be supposed that these were independently acquired by each species during the evolution of angiosperms. The gene order and the sequences of intergenic spacers in mtDNA also differ widely among the five angiosperms, indicating multiple reorganizations of genome structure during the evolution of higher plants. Among the conserved genes, the same potential conserved nonanucleotide-motif-type promoter could only be postulated for rrn18-rrn5 in four of the dicotyledonous plants, suggesting that a coding sequence does not necessarily move with the promoter upon reorganization of the mitochondrial genome.

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

Fig. 1a–f
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abdelnoor RV, Yule R, Elo A, Christensen AC, Meyer-Gausen G, Mackenzie SA (2003) Substoichiometric shifting in the plant mitochondrial genome is influenced by a gene homologous to MutS. Proc Natl Acad Sci USA 100:5968–5973

    Article  CAS  PubMed  Google Scholar 

  • Adams KL, Daley DO, Qui Y, Whelan J, Palmer JD (2000) Repeated, recent and diverse transfers of a mitochondrial gene to the nucleus in flowering plants. Nature 408:354–357

    Article  CAS  PubMed  Google Scholar 

  • Adams KL, Robenblueth M, Qiu Y, Palmer JD (2001) Multiple losses and transfers to the nucleus of two mitochondrial succinate dehydrogenase genes during angiosperm evolution. Genetics 158:1289–1300

    CAS  PubMed  Google Scholar 

  • Adams KL, Qui Y, Stroutemyer M, Palmer JD (2002) Punctuated evolution of mitochondrial gene content: high and variable rates of mitochondrial gene loss and transfer to the nucleus during angiosperm evolution. Proc Natl Acad Sci USA 99:9905–9912

    Article  CAS  PubMed  Google Scholar 

  • Backert S, Börner T (2000) Phage T4-like intermediates of DNA replication and recombination in the mitochondria of the higher plant Chenopodium album (L.). Curr Genet 37:304–314

    Article  CAS  PubMed  Google Scholar 

  • Bergman P, Sdqvist J, Farbos I, Glimelius K (2000) Male-sterile tobacco displays abnormal mitochondrial atp1 transcript accumulation and reduced floral ATP/ADP ratio. Plant Mol Biol 42:531–544

    Article  CAS  PubMed  Google Scholar 

  • Bland MM, Matzinger DF, Levings CS III (1985) Comparison of the mitochondrial genome of Nicotiana tabacum with its progenitor species. Theor Appl Genet 69:535–541

    CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bland MM, Levings CS III, Matzinger DF (1987) The ATPase subunit 6 gene of tobacco mitochondria contains an unusual sequence. Curr Genet 12:475–481

    Article  CAS  PubMed  Google Scholar 

  • Burger G, Franz Lang B, Braun H-P, Marx S (2003) The enigmatic mitochondrial ORF ymf39 codes for ATP synthase chain b. Nucleic Acids Res 31:2353–2360

    Article  CAS  PubMed  Google Scholar 

  • Caoile AGFS, Stern DB (1997) A conserved core element is functionally important for maize mitochondrial promoter activity in vitro. Nucleic Acids Res 25:4055–4060

    Article  CAS  PubMed  Google Scholar 

  • Chen HC, Wintz H, Weil JH, Pillay DT (1989) Three mitochondrial tRNA genes from Arabidopsis thaliana: evidence for the conversion of a tRNAPhe gene to a tRNATyr gene. Nucleic Acids Res 17:2613–2621

    CAS  PubMed  Google Scholar 

  • Ewing B, Hillier L, Wendl M, Green P (1998) Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8:175–185

    CAS  PubMed  Google Scholar 

  • Fauron C, Casper M, Gao Y, Moor B (1995) The maize mitochondrial genome: dynamic, yet functional. Trends Genet 11:228–235

    Google Scholar 

  • Giegé P, Knoop V, Brennicke A (1998) Complex II subunit 4 (sdh4) homologous sequences in plant mitochondrial genomes. Curr Genet 34:313–317

    Article  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Gordon D, Abajian C, Green P (1998) Consed: a graphical tool for sequence finishing. Genome Res 8:195–202

    CAS  PubMed  Google Scholar 

  • Graham LE, Cook ME, Busse JS (2000) The origin of plants: body plan changes contributing to a major evolutionary radiation. Proc Natl Acad Sci USA 97:4535–4540

    Article  CAS  PubMed  Google Scholar 

  • Gray MW (1999) Evolution of organellar genomes. Curr Opin Genet Dev 9:678–687

    Article  CAS  PubMed  Google Scholar 

  • Handa H (2003) The complete nucleotide sequence and RNA editing content of the mitochondrial genome of rapeseed ( Brassica napus L.): comparative analysis of the mitochondrial genomes of rapeseed and Arabidopsis thaliana. Nucleic Acids Res 31:5907–5916

    Article  CAS  PubMed  Google Scholar 

  • Hirose T, Sugiura M (2001) Involvement of a site-specific trans -acting factor and a common RNA-editing protein in the editing of chloroplast mRNAs: development of a chloroplast in vitro RNA editing system. EMBO J 16:6804–6811

    Article  Google Scholar 

  • Hoffmann M, Binder S (2002) Functional importance of nucleotide identities within the pea atp9 mitochondrial promoter sequence. J Mol Biol 320:943–950

    Article  CAS  PubMed  Google Scholar 

  • Janska H, Sarria R, Woloszynska M, Arrieta-Montiel M, Mackenzie SA (1998) Stoichiometric shifts in the common bean mitochondrial genome leading to male sterility and spontaneous reversion to fertility. Plant Cell 10:1163–1180

    Article  CAS  PubMed  Google Scholar 

  • Joyce PBM, Gray MW (1989) Nucleotide sequence of a wheat mitochondrial glutamine tRNA gene. Nucleic Acids Res 17:5461–5476

    CAS  PubMed  Google Scholar 

  • Kadowaki K, Ozawa K, Kazama S, Kubo N, Akihama T (1995) Creation of an initiation codon by RNA editing in the coxI transcript from tomato mitochondria. Curr Genet 28:415–422

    Article  CAS  PubMed  Google Scholar 

  • Kanazawa A, Tsutsumi N, Hirai A (1994) Reversible changes in the composition of the population of mtDNAs during dedifferentiation and regeneration in tobacco. Genetics 138:865–870

    CAS  PubMed  Google Scholar 

  • Kenton A, Parokonny AS, Gleba YY, Bennett MD (1993) Characterization of the Nicotiana tabacum L. genome by molecular cytogenetics. Mol Gen Genet 240:159–169

    Article  CAS  PubMed  Google Scholar 

  • Klein M, Eckert-Ossenkopp U, Schmiedeberg I, Brandt P, Unseld M, Brennicke A, Schuster W (1994) Physical mapping of the mitochondrial genome of Arabidopsis thaliana by cosmid and YAC clones. Plant J 6:447–455

    Article  CAS  PubMed  Google Scholar 

  • Kubo T, Nishizawa S, Sugawara A, Itchoda N, Estiati A, Mikami T (2000) The complete nucleotide sequence of the mitochondrial genome of sugar beet ( Beta vulgaris L.) reveals a novel gene for tRNAcys (GCA). Nucleic Acids Res 28:2571–2576

    Article  CAS  PubMed  Google Scholar 

  • Kurland CG, Andersson SGE (2000) Origin and evolution of the mitochondrial proteome. Microbiol Mol Biol Rev 64:786–820

    Google Scholar 

  • Kurtz S, Choudhuri JV, Ohlebusch E, Schleiermacher C, Stoye J, Giegerich R (2001) REPUTER: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res 29:4633–4642

    Article  CAS  PubMed  Google Scholar 

  • Lelandais C, Gutierres S, Mathieu C, Vedel F, Remacle C, Maréchal-Drouard L, Brennicke A, Binder S, Chétrit P (1996) A promoter element active in run-off transcription controls the expression of the two cistrons of nad and rps genes in Nicotiana sylvestris mitochondria. Nucleic Acids Res 24:4789-4804

    Article  Google Scholar 

  • Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964

    Article  CAS  PubMed  Google Scholar 

  • Margulis L, Bermudes D (1985) Symbiosis as a mechanism of evolution: status of cell symbiosis theory. Symbiosis 1:101–124

    CAS  PubMed  Google Scholar 

  • Marienfeld J, Unseld M, Brennicke A (1999) The mitochondrial genome of Arabidopsis is composed of both native and immigrant information. Trends Plant Sci 4:495–502

    Article  PubMed  Google Scholar 

  • Mundel C, Schuster W (1996) Loss of RNA editing of rps1 sequences in Oenothera mitochondria. Curr Genet 30:455–460

    Article  CAS  PubMed  Google Scholar 

  • Notsu Y, Masood S, Nishikawa T, Kubo N, Akiduki G., Nakazono M, Hirai A, Kadowaki K (2002) The complete sequence of the rice ( Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol Genet Genomics 268:434–445

    Article  CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Oldenberg DJ, Bendich AJ (1996) Size and structure of replicating mitochondrial DNA in cultured tobacco cells. Plant Cell 8:447–461

    Article  PubMed  Google Scholar 

  • Ortega VM, Bohner JG, Chase CD (2000) The tobacco apocytochrome b gene predicts sensitivity to the respiratory inhibitors antimycin A and myxothiazol. Curr Genet 37:315–321

    Article  CAS  PubMed  Google Scholar 

  • Palmer JD, Adams KL, Cho Y, Parkinson CL, Qiu Y, Song K (2000) Dynamic evolution of plant mitochondrial genomes: mobile genes and introns and highly variable mutation rates. Proc Natl Acad Sci USA 97:6960–6966

    Article  CAS  PubMed  Google Scholar 

  • Quiñones V, Zanlungo S, Holuigue L, Litvak S, Jordana X (1995) The cox1 initiation codon is created by RNA editing in potato mitochondria. Plant Physiol 108:1327–1328

    Article  PubMed  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual (3rd edn). Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.

    Google Scholar 

  • Satoh M, Nemoto Y, Kawano S, Nagata T, Hirokawa H, Kuroiwa T (1993) Organization of heterologous mitochondrial DNA molecules in mitochondrial nuclei of cultured tobacco cells. Protoplasma 175:112–120

    CAS  Google Scholar 

  • Shinozaki K, et al (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5:2043–2049

    CAS  Google Scholar 

  • Siqueira SF, Dias SMG, Hardouin P, Pereira FRS, Lejeune B, de Souza AP (2002) Transcription of succinate dehydrogenase subunit 4 ( sdh4) gene in potato: detection of extensive RNA editing and co-transcription with cytochrome oxidase III ( cox3) gene. Curr Genet 41:282–289

    Article  CAS  PubMed  Google Scholar 

  • Soltis PS, Soltis DE, Chase MW (1999) Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402:402–404

    Article  CAS  PubMed  Google Scholar 

  • Stamper SE, Dewey RE, Bland MM, Levings CS III (1987) Characterization of the gene urf13 -T and unidentified reading frame, ORF25, in maize and tobacco mitochondria. Curr Genet 12:457–463

    Article  CAS  PubMed  Google Scholar 

  • Sugiyama Y, Watase Y, Nagase M, Hirai A, Sugiura M (2004) Timing of tRNA gene transfer from chloroplast to mitochondrion revealed by genomic analysis of dicotyledonous plant mitochondria. Endocytobiosis Cell Res 15:77–86

    Google Scholar 

  • Svab Z, Maliga P (1993) High-frequency plastid transformation in tobacco by selection for a chimeric aadA gene. Proc Natl Acad Sci USA 90:913–917

    CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed  Google Scholar 

  • Turmel M, Otis C, Lemieux C (2002) The chloroplast and mitochondrial genome sequences of the charophyte Chaetosphaeridium globosum: insights into the timing of the events that restructured organelle DNAs within the green algal lineage that led to land plants. Proc Natl Acad Sci USA 99:11275-11280

    Article  CAS  PubMed  Google Scholar 

  • Turmel M, Otis C, Lemieux C (2003) The mitochondrial genome of Chara vulgaris: insights into the mitochondrial DNA architecture of the last common ancestor of green algae and land plants. Plant Cell 15:1888–1903

    Article  CAS  PubMed  Google Scholar 

  • Unseld M, Marienfeld JR, Brandt P, Brennicke A (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nature Genet 15:57–61

    CAS  PubMed  Google Scholar 

  • Weber F, Dietrich A, Weil J-H, Marechal-Drouard L (1990) A potato mitochondrial isoleucine tRNA is coded for by a mitochondrial gene possessing a methionine anticodon. Nucleic Acids Res 18:5027–5030

    CAS  PubMed  Google Scholar 

  • Zanlungo S, Quiñones V, Moenne A, Holuigue L, Jordana X (1995). Splicing and editing of rps10 transcripts in potato mitochondria. Curr Genet 27:565–571

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Ms. M. Shigemori for help with the preparation of tobacco mitochondria. This work was in part supported by a Grant-in-Aid for Scientific Research (B) (No. 15370025) to M.S., and a grant from Takeda Science Foundation to Y.S.

Author information

Authors and Affiliations

  1. Center for Gene Research, Nagoya University, Chikusa-ku, 464-0812, Nagoya , Japan

    Y. Sugiyama, Y. Watase, M. Nagase & S. Yagura

  2. Graduate School of Natural Sciences, Nagoya City University, Mizuho-ku, 467-8501, Nagoya, Japan

    N. Makita & M. Sugiura

  3. Faculty of Agriculture, Meijo University, Tempaku-ku, 468-8502, Nagoya, Japan

    A. Hirai

Authors
  1. Y. Sugiyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Y. Watase
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Nagase
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. N. Makita
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. Yagura
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A. Hirai
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. Sugiura
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Y. Sugiyama.

Additional information

Communicated by R. Hagemann

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sugiyama, Y., Watase, Y., Nagase, M. et al. The complete nucleotide sequence and multipartite organization of the tobacco mitochondrial genome: comparative analysis of mitochondrial genomes in higher plants. Mol Genet Genomics 272, 603–615 (2005). https://doi.org/10.1007/s00438-004-1075-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-004-1075-8

Keywords

Search

Navigation