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Journal of Plant Research

, Volume 106, Issue 1, pp 89–99 | Cite as

Organization and post-transcriptional modification of mitochondrial genes in higher plants

  • Koh-ichi Kadowaki
JPR Symposium

Abstract

Recent topics regarding higher plant mitochondria are briefly reviewed, such as gene organization, the genes associated with mutants, and the maturation of transcripts. The estimated genome size of higher plant mitochondrial DNA varies from about 200 kb to 2,500 kb. Most of the mitochondrial genomes are organized as complex multiple circular molecules, generated from recombinations between repeated sequences. Several protein-encoding genes unique to plant mitochondria are identified but gene contents are not identical among the plant species. Gene transfer of cytochrome oxidase subunit II, generally mitochondrially encoded gene, is found to move from mitochondrion to nucleus via RNA molecules and the event is limited in a single genus of legume. Genes associated with mitochondrial mutants, CMS-T and NCS3, are isolated and characterized in detail. Plant mitochondria have two types of notable post-transcriptional RNA modifications. One is RNA editing that alters a cytidine residue in DNA to a uridine residue in RNA, and results in an evolutionally more conservative polypeptide. The other istrans-splicing of transcripts of NADH dehydrogenase subunit 1 and 5 genes, that fuses the physically scattered mRNAs and makes a mature mRNA.

Key words

Gene organization Gene transfer Mitochondrial mutants Mitochondrion Transcript modification 

Abbreviations

(atpA, atp6 andatp9)

ATPase subunit α, 6, and 9 genes

(coxI andcoxII)

cytochrome oxidase subunit I and II genes

(C)

cytidine

(CMS)

cytoplasmic male sterillity

(E.coli)

Escherichia coli

(nad1 andnad5)

NADH dehydrogenase subunit 1 and 5 genes

(NCS3 and NCS5)

nonchromosomal stripe mutants 3 and 5

(Rf1 andRf2)

restorer fertillity 1 and 2 genes

(rrn26)

26S ribosomal RNA gene

(rps3,rps13, andrpl16)

ribosomal protein S3, S13, and L16 genes

(U)

uridine

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References

  1. Bailey-Serres, J., Hanson, D.K., Fox, T.D. andLeaver, C.J. 1986. Mitochondrial genome rearrangement leads to extension and relocation of the cytochrome c oxidase subunit I gene in Sorghum. Cell47: 567–576.CrossRefPubMedGoogle Scholar
  2. Bartnik, E. andBorsuk, P. 1986. A glycine tRNA gene from lupine mitochondria. Nucl. Acids Res.14: 2407.PubMedGoogle Scholar
  3. Begu, P., Graves, P.-V., Donec, C., Arselin, G., Litvak, S. andAraya, A. 1990. RNA editing of wheat mitochondrial ATP synthase subunit 9: Direct protein and cDNA sequencing. Plant Cell2: 1283–1290.CrossRefPubMedGoogle Scholar
  4. Binder, S., Schuster, W., Grienenberger, J.-M., Weil, J.-H. andBrennicke, A. 1990. Genes for tRNAGly, tRNAHis, tRNAPhe, tRNASer and tRNATyr are encoded inOenothera mitochondrial DNA. Curr. Genet.17: 353–358.CrossRefPubMedGoogle Scholar
  5. Bland, M.M., Levings, C.S., III andMatzinger, D.F. 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.CrossRefPubMedGoogle Scholar
  6. Blum, B., Bakalara N. andSimpson, L. 1990. A model for RNA editing in kinetoplastid mitochondria: “Guide” RNA molecules transcribed from maxicircle DNA provide the edited information. Cell60: 189–198.CrossRefPubMedGoogle Scholar
  7. Braun, C.J. andLevings, C.S., III. 1986. DNA sequence homology between the maize mitochondrial and chloroplast genomes. Maize Genet. Coop. Newsl.60: 111.Google Scholar
  8. Bonen, L. 1987. The mitochondrial S13 ribosomal protein gene is silent in wheat embryos and seedlings. Nucl. Acids Res.15: 10393–10404.PubMedGoogle Scholar
  9. Boutry, M., Briquet, M. andGoggeau, A. 1983. The α subunit of a plant mitochondrial F1-ATPase is translated in mitochondria. J. Biol. Chem.258: 8524–8526.PubMedGoogle Scholar
  10. Chapdelaine, Y. andBonen, L. 1991. The wheat mitochondrial gene for subunit 1 of the NADH dehydrogenase complex: Atrans-splicing model for this gene-in-places. Cell65: 465–472.CrossRefPubMedGoogle Scholar
  11. Choquet, Y., Goldschmidt- Clermont, M., Girard-Bascou, J., Kuck, V., Bennoun, P. andRochaix, J.-D. 1988. Mutant phenotypes support atrans-splicing mechanism for the expression of the tripartilepsaA gene in theC. reinhardti chloroplast. Cell52: 903–913.CrossRefPubMedGoogle Scholar
  12. Covello, P.S. andGray, N.W. 1989. RNA editing in wheat mitochondria. Nature341: 662–666.CrossRefPubMedGoogle Scholar
  13. de Souza, A.P., Jubier, M.-F., Delcher, E., Lancelin, D. andLejeune, B. 1991. Atrans-splicing model for the expression of the tripartitenad5 gene in wheat and maize mitochondria. Plant Cell3: 1363–1378.Google Scholar
  14. Dewey, R.E., Levings, C.S., III andTimothy D.H. 1986. Novel recombinations in the maize mitochondrial genome produce a unique transcriptional unit in the Texas male-sterile cytoplasm. Cell44: 439–449.CrossRefPubMedGoogle Scholar
  15. Dewey, R.E., Timothy, D.H. andLevings, C. S., III 1987. A mitochondrial protein associated with cytoplasmic male sterlity in the T cytoplasm of maize. Proc. Natl. Acad. Sci. USA84: 5374–5378.Google Scholar
  16. Dewey, R.E., Siedow, J.N., Timothy, D.H. andLevings, C.S., III 1988. A 13-kilodalton maize mitochondrial protein inE. coli confers sensitivity toBipolaris maydis toxin. Science239: 293–295.PubMedGoogle Scholar
  17. Feiler, H.S. andNewton, K.J. 1987. Altered mitochondrial gene expression in the nonchromosomal stripe 2 mutant of maize. EMBO J.6: 1535–1539.PubMedGoogle Scholar
  18. Flnnegan, P.M. andBrown, G.G. 1986. Autonomously replicating RNA in mitochondria of maize plants with S-type cytoplasm. Proc. Natl. Acad. Sci. USA83: 5175–5179.Google Scholar
  19. Forde, B.G. andLeaver, C.J. 1980. Nuclear and cytoplasmic genes controlling synthesis of variant mitochondrial polypeptides in male-sterile maize. Proc. Natl. Acad. Sci. USA77: 418–422.Google Scholar
  20. Fox, T.D. andLeaver, C.J. 1981. TheZea mays mitochondrial gene coding cytochrome oxidase subunit II has an intervening sequence and does not contain TGA codons. Cell26: 315–323.CrossRefPubMedGoogle Scholar
  21. Glab, N., Wise, R.P., Pring, D.R., Jacq, C. andSlonimski, P. 1990. Expression inSaccharomyces cerevisiae of a gene associated with cytoplasmic male sterillity from maize: Respiratory dysfunction and uncoupling of yeast mitochondria. Mol. Gen. Genet.223: 24–32.CrossRefPubMedGoogle Scholar
  22. Gray, M.W., Hanic-Joyce, P.J. andCovello, P.S. 1992. Transcription, processing and editing in plant mitochondria. Ann. Rev. Plant Physiol. Plant Mol. Biol.43: 145–175.Google Scholar
  23. Gualberto, J.M., Lamattina, L., Bonnard, G., Weil, J.-H. andGrienenberger, J.-M. 1989. RNA editing in wheat mitochondria results in the conservation of protein sequence. Nature341: 660–662.CrossRefPubMedGoogle Scholar
  24. Gualberto, J.M., Weil J.-H. andGrienenberger, J.-M. 1990. Editing of the wheatcoxIII transcript: evidence for twelve C to U and one U to C conversions and for sequence similarities around editing sites. Nucl. Acids Res.18: 3771–3776.PubMedGoogle Scholar
  25. Gualberto, J.M., Bonnard, G., Lamattina, L. andGrienenberger, J.-M. 1991. Expression of the wheat mitochondrialnad3–rps12 transcription unit: correlation between editing and mRNA maturation. Plant Cell3: 1109–1120.CrossRefPubMedGoogle Scholar
  26. Hack, E. andLeaver, C.J. 1983. The α-subunit of the maize F1-ATPase is synthesized in the mitochondrion. EMBO J.2: 1783–1789.PubMedGoogle Scholar
  27. Hack, E., Yang, L.C. andHorner, H.T. 1991. T-URF13 protein from mitochondria of Texas male-sterile maize (Zea mays L). Plant Physiol.95: 861–870.Google Scholar
  28. Hanson, M.R. 1991. Plant mitochondrial mutations and male sterility. Annu. Rev. Genet.25: 461–486.CrossRefPubMedGoogle Scholar
  29. Hiesel R., Wissinger, B., Schuster, W. andBrennicke, A.. RNA editing in plant mitochondria. Science246: 1632–1634.PubMedGoogle Scholar
  30. Hiesel R., Wissinger, B. andBrennicke, A. 1990. Cyto-chrome oxidase subunit II mRNAs inOenothera mitochondria are edited at 24 sites. Curr. Genet.18: 371–375.CrossRefPubMedGoogle Scholar
  31. Hiratsuka, J., Shimada, H., Whittier, R.F., Ishibashi, T., Sakamoto, M., Mori, M., Kondo, C., Honji, Y., Sun, C.-R., Meng, B.-Y., Li, Y.-Q., Kanno, A., Nishizawa, Y., Hirai, A., Shinozaki, K. andSugiura, M. 1989. The complete sequence of the rice (Oryzasativa) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Mol. Gen. Genet.217: 185–194.PubMedGoogle Scholar
  32. Huang, J., Lee, S.-H., Lin, C., Medici, R., Hack, E. andMyers, A.M. 1990. Expression in yeast of the T-URF13 protein from Texas male-sterile maize mitochondria confers sensitivity to methomyl and to Texas-cytoplasm-specific fungal toxins. EMBO J.9: 339–347.PubMedGoogle Scholar
  33. Hunt, M.D. andNewton, K.J. 1991. The NCS3 mutation: genetic evidence for the expression of ribosomal protein genes inZea mays mitochondria. EMBO J.10: 1045–1052.PubMedGoogle Scholar
  34. Izuchi S., Terachi, T., Sakamoto, M., Mikami, T. andSugita, M. 1990. Structure and expression of tomato mitochondrial genes coding for tRNACys (GCA), tRNAAsn (GUU) and tRNATyr (GUA): a native tRNACys gene is present in dicot plants but absent in monocot plants. Curr. Genet.18: 239–243.CrossRefPubMedGoogle Scholar
  35. Kadowaki, K., Yazaki, K., Osumi, T., Harada, K., Katsuta, M. andNakagahra, M. 1988. Distribution of mitochondrial plasmid-like DNA in cultivated rice (Oryza sativa L.) and its relationship with varietal groups. Theor. Appl. Genet.76: 809–814.CrossRefGoogle Scholar
  36. Kadowaki, K., Suzuki, T. andKazama, S. 1990. A chimeric gene containing the 5' portion ofatp6 is associated with cytoplasmic male-sterility of rice. Mol. Gen. Genet.224: 10–16.CrossRefPubMedGoogle Scholar
  37. Kennell, J.C. andPring, D.R. 1989. Initiation and processing ofatp6, T-urf13 andORF221 transcripts from mitochondria of T cytoplasm maize. Mol. Gen. Genet.216: 16–24.CrossRefGoogle Scholar
  38. Kennell, J.C., Wise, R.P. andPring, D.R. 1987. Influence of nuclear background on transcription of a maize mitochondrial region associated with Texas malesterile cytoplasm. Mol. Gen. Genet.210: 399–406.CrossRefGoogle Scholar
  39. Kemble, R.J. andThompson, R.D. 1982. S1 and S2, the linear mitochondrial DNAs present in a male-sterile line of maize, possess terminally attached proteins. Nucl. Acids Res.10: 8181–8190.PubMedGoogle Scholar
  40. Kempken, F., Mullen, J.A., Pring, D.R. andTang, H.V. 1991. RNA editing of sorghum mitochondrialatp6 transcripts changes 15 amino acids and generates a carboxy-terminus identical to yeast. Curr. Genet.20: 412–422.CrossRefGoogle Scholar
  41. Knoop, V., Schuster, W., Wissinger, B. andBrennicke, A. 1991.Trans splicing integrates an exon of 22 nucleotides into thenad5 mRNA in higher plant mitochondria. EMBO J.10: 3483–3493.PubMedGoogle Scholar
  42. Korth, K.L., Kaspi, C.I., Siedow, J.N. andLevings, C.S., III. 1991. URF13, a maize mitochondrial pore-forming protein is oligomeric and has a mixed orientation inEscherichia coli plasma membranes. Proc. Natl. Acad. Sci. USA88: 10865–10869.PubMedGoogle Scholar
  43. Lamattina, L., Weil, J.-H. andGrienenberger, J.-M. 1989. RNA editing at a splicing site of NADH dehydrogenase subunit IV gene transcript in wheat mitochondria. FEBS Lett.258: 29–38.CrossRefGoogle Scholar
  44. Leaver, C.J. andHarmey, M.A. 1976. Higher plant mitochondrial ribosomes contain a 5S ribosomal ribonucleic acid component. Biochem. J.157: 257–277.Google Scholar
  45. Leon, P., Walbot, V. andBedinger, P. 1989. Molecular analysis of the linear 2.3 kb plasmid of maize mitochondria: apparent capture of tRNA genes. Nucl. Acids Res.17: 4089–4099.PubMedGoogle Scholar
  46. Levings, C.S., III andSederoff, R.R. 1983. Nucleotide sequence of the S-2 mitochondrial DNA from the S cytoplasm of maize. Proc. Natl. Acad. Sci. USA80: 4055–4059.Google Scholar
  47. Levings, C.S., III andBrown, G.G. 1989: Molecular biology of plant mitochondria. Cell56: 171–179.CrossRefPubMedGoogle Scholar
  48. Lonsdale, D.M. 1984. A review of the structure and organization of the mitochondrial genome of higher plants. Plant Mol. Biol.3: 201–206.CrossRefGoogle Scholar
  49. Lonsdale, D.M., Hodge, T.P., Home, C.J. andStern, D.B. 1983. Maize mitochondrial DNA contains a sequence homologous to the ribulose-1, 5,-bisphosphate carboxylase large subunit gene of chloroplast DNA. Cell34: 1007–1014.CrossRefPubMedGoogle Scholar
  50. Lonsdale, D.M., Hodge, T.P. andFauron, C.M.-R. 1984. The physical map and organization of the mitochondrial genome from the fertile cytoplasm of maize. Nucl. Acids Res.12: 9249–9261.PubMedGoogle Scholar
  51. Ludwig, S.R., Pohlman, R.F., Vleira, J., Smith, A.G. andMessing, J. 1985. The nucleotide sequence of a mitochondrial replicon from maize. Gene38: 131–138.CrossRefPubMedGoogle Scholar
  52. Mackenzie, S.A. andChase, C.D. 1990. Fertility restoration is associated with loss of a portion of the mitochondrial genome in cytoplasmic male-sterile common bean. Plant Cell2: 905–912.CrossRefPubMedGoogle Scholar
  53. Makaroff, C.A., Apel, I.J. andPalmer, J.D. 1989. Theatp6 coding region has been disrupted and a novel reading frame generated in the mitochondrial genome of cytoplasmic male-sterile radish. J. Biol. Chem.264: 11706–11713.PubMedGoogle Scholar
  54. Marechal-Drouard, L., Guillemaut, P., Cosset, A., Arbogast, M., Weber, F., Well, J.-H. andDietrich, A. 1990. Transfer RNAs of potato (Solanum tuberosum) mitochondria have different genetic origins. Nucl. Acids Res.18: 3689–3696.PubMedGoogle Scholar
  55. Marechal-Drouard, L., Weil, J.-H. andGuillemant, P. 1988. Import of several tRNAs from the cytoplasm into the mitochondria in beanPhaseolus vulgaris. Nucl. Acids Res.16: 4777–4788.PubMedGoogle Scholar
  56. Michel, F. andDujon, B. 1983. Conservation of RNA secondary structures in two intron families including mitochondrial-, chloroplast-and nuclear-encoded members. EMBO J.2: 33–38.PubMedGoogle Scholar
  57. Mchel, F., Umesono, K. andOzeki, H. 1989. Comparative and functional anatomy of group II catalytic introns-a review. Gene52: 5–30.Google Scholar
  58. Newton, K.J. 1988. Plant mitochondrial genomes: organization, expression and variation. Annu. Rev. Plant Physiol. Plant Mol. Biol.39: 503–532.CrossRefGoogle Scholar
  59. Newton, K.J. andCoe, E.H., Jr. 1986. Mitochondrial DNA changes in abnormal growth (nonchromosomal stripe) mutants of maize. Proc. Natl. Acad. Sci. USA83: 7363–7366.Google Scholar
  60. Newton, K.J., Knudsen, C., Gabay-Laughnan, S. andLaughnan, J.R. 1990. An abnormal growth mutant in maize has a defective mitochondrial cytochrome oxidase gene. Plant Cell2: 107–113.CrossRefPubMedGoogle Scholar
  61. Nugent, J.M. andPalmer, J.D. 1991. RNA-mediated transfer of the genecoxll from the mitochondrion to the nucleus during flowering plant evolution. Cell66: 473–481.CrossRefPubMedGoogle Scholar
  62. Ohyama, K., Fukuzawa, H., Kohchi, T., Shirai, H., Sano, T., Sano, S., Umesono, K., Shiki, Y., Takeuchi, M., Chang, Z., Aota, S.-I., Inokuchi, H. andOzeki, H. 1986. Chloroplast gene organization deduced from complete sequence of liverwortMarchantia polymorpha chloroplast DNA. Nature322: 572–574.CrossRefGoogle Scholar
  63. Paillard, M., Sederoff, R.R. andLevings, C.S., III. 1985. Nucleotide sequence of the S-1 mitochondrial DNA from the S cytoplasm of maize. EMBO J.4: 1125–1128.PubMedGoogle Scholar
  64. Palmer, J.D. andShields, C.R. 1984. Tripartite structure of theBrassica campestris mitochondrial genome. Nature307: 437–440.CrossRefGoogle Scholar
  65. Palmer, J.D. andHerbon, L.A. 1987. Unicircular structure of theBrassica hirta mitochondrial genome. Curr. Genet.11: 565–570.PubMedGoogle Scholar
  66. Pring, D.R. andLonsdale, D.M. 1985. Molecular biology of higher plant mitochondrial DNA. Int. Rev. Cytol.97: 1–46.Google Scholar
  67. Pring, D.R. andLonsdale, D.M. 1989. Cytoplasmic male sterility and maternal inheritance of disease susceptibility in maize. Annu. Rev. Phytopathol.28: 483–502.Google Scholar
  68. Schardl, C.L., Lonsdale, D.M., Pring, D.R. andRose, K.R. 1984. Linearization of maize mitochondrial chromosomes by recombination with linear episomes. Nature310: 292–296.Google Scholar
  69. Schuster, W. andBrennicke, A. 1987a. Plastid, nuclear and reverse transcriptase sequences in the mitochondrial genome ofOenothera: is genetic information transferred between organelles via RNA? EMBO J.6: 2857–2863.PubMedGoogle Scholar
  70. Schuster, W. andBrennicke, A. 1987b. Plastid DNA in the mitochondrial genome ofOenothera: Intra-and interorganellar rearrangements involving part of the ribosomal cistron. Mol. Gen. Genet.210: 44–51.CrossRefGoogle Scholar
  71. Schuster, W., Wissinger, B., Unseld, M. andBrennicke, A. 1990. Transcripts of the NADH-dehydrogenase subunit 3 gene are differentially edited inOenothera mitochondria. EMBO J.9: 263–269.PubMedGoogle Scholar
  72. Schuster, W., Ternes, R., Knoop, V., Hiesel, R., Wissinger, B. andBrennicke, A. 1991a. Distribution of RNA editing sites inOenothera mitochondrial mRNAs. Curr. Genet.20: 397–404.CrossRefPubMedGoogle Scholar
  73. Schuster, W., Wissinger, B., Hiesel, R., Unseld, M., Gerold, E., Knoop, V., Marchfelder, A., Binder, S., Schobel, W., Scheike, R., Gronger, R., Ternes, R. andBrennicke, A. 1991b. Between DNA and protein-RNA editing in plant mitochondria. Physiol. Plant81: 437–445.CrossRefGoogle Scholar
  74. Shih, M.-C., Lazar, G. andGoodman, H.M. 1986. Evidence in favor of the symbiotic origin of chloroplasts: Primary structure and evolution of tobacco glyceraldehyde-3-phosphate dehydrogenase. Cell47: 73–80.CrossRefPubMedGoogle Scholar
  75. Shikanai, T. andYamada, Y. 1988. Properties of the circular plasmid-like DNA, B4 from mitochondria of cytoplasmic male-sterile rice. Curr. Genet.13: 441–443.CrossRefPubMedGoogle Scholar
  76. Shikanai, T., Yang, Z.-Q. andYamada, Y. 1987. Properties of the circular plasmid-like DNA B1 from mitochondria of cytoplasmic male-sterile rice. Plant Cell Physiol.28: 1245–1251.Google Scholar
  77. Shikanai, T., Yang, Z.-Q. andYamada, Y. 1989. Nucleotide sequence and molecular characterization of plasmid-like DNAs from mitochondria of cytoplasmic male-sterile rice. Curr. Genet.15: 349–354.CrossRefPubMedGoogle Scholar
  78. 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, B.Y., Sugita, M., Deno, H., Kamogashira, T., Yamada, K., Kusuda, J., Takaiwa, F., Kato, A., Tohdoh, N., Shimada, H. andSugiura, M. 1986. The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J.5: 2043–2049.PubMedGoogle Scholar
  79. Singh, M. andBrown, G.G. 1991. Suppression of cytoplasmic male sterility by nuclear genes alters expression of a novel mitochondrial gene region. Plant Cell3: 1349–1362.CrossRefPubMedGoogle Scholar
  80. Small, I.D., Isaac, P.G. andLeaver, C.J. 1987. Stoichiometric differences in DNA molecules containing theatpA gene suggest mechanisms for the generation of mitochondrial genome diversity in maize. EMBO J.6: 865–869.PubMedGoogle Scholar
  81. Small, I.D., Suffolk, R. andLeaver, C.J. 1989. Evolution of plant mitochondrial genomes via substoichiometric intermediates. Cell58: 69–76.CrossRefPubMedGoogle Scholar
  82. Smith, A.G. andPring, D.R. 1987. Nucleotide sequence and molecular characterization of maize mitochondrial plasmid-like DNA. Curr. Genet.12: 617–623.CrossRefPubMedGoogle Scholar
  83. Stern, D.B. andLonsdale, D.M. 1982. Mitochondrial and chloroplast genomes of maize have a 12-kilobase DNA sequence in common. Nature229: 698–702.Google Scholar
  84. Stern, D.B. andPalmer, J.D. 1984. Extensive and widespread homologies between mitochondrial DNA and chloroplast DNA in plants. Proc. Natl. Acad. Sci. USA81: 1946–1950.Google Scholar
  85. Suzuki, T., Kazama, S., Hirai, A., Akihama, T. andKadowaki, K. 1991. The rice mitochondrialnad3 gene has an extended reading frame at its 5' end: nucleotide sequence analysis of ricetrnS, nad3, andrps12 genes. Curr. Genet.20: 331–337.CrossRefPubMedGoogle Scholar
  86. Umbeck, P.F. andGengenbach, B.G. 1983. Reversion of male-sterile T-cytoplasm maize to male fertility in tissue culture. Crop Sci.23: 584–588.Google Scholar
  87. von Allmen, J.-M., Tottmann, W.H., Gengenbach, B.G., Harvey, A.J. andLonsdale, D.M. 1991. Transfer of methomyl and Hm-T toxin sensitivity from T-cytoplasm to tobacco. Mol. Gen. Genet.229: 405–412.CrossRefGoogle Scholar
  88. Wahleithner, J.A. andWolstenholme D.R. 1988. Ribosomal protein S14 genes in broad bean mitochondrial DNA. Nucl. Acids Res.16: 6897–6913.PubMedGoogle Scholar
  89. Ward, B.L., Anderson, R.S. andBendich, A.J. 1981. The mitochondrial genome is large and variable in a family of plants (Cucurbitaceae). Cell25: 793–803.CrossRefPubMedGoogle Scholar
  90. Ward, G.C. andLevings, C.S., III. 1991. The protein-encoding gene T-urf13 is not edited in maize mitochondria. Plant Mol. Biol.17: 1083–1088.CrossRefPubMedGoogle Scholar
  91. Weissinger, A.K., Timothy, D.H., Levings, C.S., III, Hu, W.W.L. andGoodman, M.M. 1982. Unique plasmid-like mitochondrial DNAs from indigenous maize races of Latin America. Proc. Natl. Acad. Sci. USA79: 1–5.Google Scholar
  92. Wintz, H. andHanson, M.R., 1991. A temination codon is created by RNA editing in the petunia mitochondrialatp9 gene transcript. Curr. Genet.19: 61–64.CrossRefPubMedGoogle Scholar
  93. Wise, R.P., Pring, D.R. andGengenbach, B.G. 1987. Mutation to fertility and toxin insensitivity in Texas (T) cytoplasm maize is associated with a frameshift in a mitochondrial open-reading frame. Proc. Natl. Acad. Sci. USA84: 2858–2862.Google Scholar
  94. Wissinger, B., Hiesel, R., Schuster, W. andBrennicke, A. 1988. The NADH-dehydrogenase subunit 5 gene inOenothera mitochondria contains two introns and is cotranscribed with the 18S-5S rRNA genes. Mol. Gen. Genet.212: 56–65.CrossRefPubMedGoogle Scholar
  95. Wissinger, B., Schuster, W. andBrennicke, A. 1990. Species-specific RNA editing patterns in the mitochondrialrps13 transcripts ofOenothera andDaucus. Mol. Gen. Genet.224: 389–395.CrossRefPubMedGoogle Scholar
  96. Wissinger, B., Schuster, W. andBrennicke, A. 1991.Trans splicing inOenothera mitochondria:nad1 mRNAs are edited in exon andtrans-splicing group II intron sequences. Cell65: 473–482.CrossRefPubMedGoogle Scholar
  97. Yang, A.J. andMulligan, R.M. 1991. RNA editing intermediates ofcox2 transcripts in maize mitochondria. Mol. Cell. Biol.11: 4278–4281.PubMedGoogle Scholar
  98. Young, E.G. andHanson, M.R. 1987. A fused mitochondrial gene associated with cytoplasmic male sterility is developmentally regulated. Cell50: 41–49.CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan 1993

Authors and Affiliations

  • Koh-ichi Kadowaki
    • 1
  1. 1.Department of Molecular BiologyNational Institute of Agrobiological ResourcesTsukubaJapan

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