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. 1986 Jun 11;14(11):4519–4533. doi: 10.1093/nar/14.11.4519

RNA mapping on Drosophila mitochondrial DNA: precursors and template strands.

F Berthier, M Renaud, S Alziari, R Durand
PMCID: PMC311462  PMID: 3086843

Abstract

Drosophila melanogaster mitochondrial DNA (mtDNA) is closely related to the mammalian and amphibian mtDNA except for gene organization. In Drosophila, genes are distributed in clusters alternatively coded on each strand. Besides the eleven major foreseeable transcripts previously described (MERTEN and PARDUE, 1981, J. Mol. Biol., 153, 1-21), we have characterized two poly A+ transcripts, one major and one minor which could correspond respectively to the ND3 and ND6 reading frames, and 27 poly A+ minor transcripts (0.2 to greater than 3.2 kb) which are distributed along the mtDNA except in the rRNAs, ND 1 and A+ T rich regions. The mapping and length of 25 of these transcripts strongly suggest a precursor role. They would be processed at the level of tRNA or tRNA-like sequences. Most of them are transcribed from the template strand of each gene cluster and their distribution is in agreement with the hypothesis of several transcription origins and terminations located near the extremities of each gene cluster. Quantitatively our results show a large variation in each presumptive mature transcript compared to the other, even in a given gene cluster, suggesting a specific degradation of some of the mature transcripts.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alziari S., Berthier F., Touraille S., Stepien G., Durand R. Mitochondrial DNA expression in Drosophila melanogaster: neosynthesized polypeptides in isolated mitochondria. Biochimie. 1985 Sep;67(9):1023–1034. doi: 10.1016/s0300-9084(85)80297-2. [DOI] [PubMed] [Google Scholar]
  2. Anderson S., Bankier A. T., Barrell B. G., de Bruijn M. H., Coulson A. R., Drouin J., Eperon I. C., Nierlich D. P., Roe B. A., Sanger F. Sequence and organization of the human mitochondrial genome. Nature. 1981 Apr 9;290(5806):457–465. doi: 10.1038/290457a0. [DOI] [PubMed] [Google Scholar]
  3. Anderson S., de Bruijn M. H., Coulson A. R., Eperon I. C., Sanger F., Young I. G. Complete sequence of bovine mitochondrial DNA. Conserved features of the mammalian mitochondrial genome. J Mol Biol. 1982 Apr 25;156(4):683–717. doi: 10.1016/0022-2836(82)90137-1. [DOI] [PubMed] [Google Scholar]
  4. Bhat K. S., Bhat N. K., Kulkarni G. R., Iyengar A., Avadhani N. G. Expression of the cytochrome b-URF6-URF5 region of the mouse mitochondrial genome. Biochemistry. 1985 Oct 8;24(21):5818–5825. doi: 10.1021/bi00342a020. [DOI] [PubMed] [Google Scholar]
  5. Bhat K. S., Kantharaj G. R., Avadhani N. G. Nature of steady-state and newly synthesized mitochondrial messenger ribonucleic acids in mouse liver and Ehrlich ascites tumor cells. Biochemistry. 1984 Apr 10;23(8):1695–1701. doi: 10.1021/bi00303a018. [DOI] [PubMed] [Google Scholar]
  6. Bibb M. J., Van Etten R. A., Wright C. T., Walberg M. W., Clayton D. A. Sequence and gene organization of mouse mitochondrial DNA. Cell. 1981 Oct;26(2 Pt 2):167–180. doi: 10.1016/0092-8674(81)90300-7. [DOI] [PubMed] [Google Scholar]
  7. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Breitenberger C. A., Browning K. S., Alzner-DeWeerd B., RajBhandary U. L. RNA processing in Neurospora crassa mitochondria: use of transfer RNA sequences as signals. EMBO J. 1985 Jan;4(1):185–195. doi: 10.1002/j.1460-2075.1985.tb02335.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bultmann H., Laird C. D. Mitochondrial DNA from Drosophila melanogaster. Biochim Biophys Acta. 1973 Mar 19;299(2):196–209. doi: 10.1016/0005-2787(73)90342-0. [DOI] [PubMed] [Google Scholar]
  10. Burger G., Helmer Citterich M., Nelson M. A., Werner S., Macino G. RNA processing in Neurospora crassa mitochondria: transfer RNAs punctuate a large precursor transcript. EMBO J. 1985 Jan;4(1):197–204. doi: 10.1002/j.1460-2075.1985.tb02336.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chang D. D., Clayton D. A. Precise identification of individual promoters for transcription of each strand of human mitochondrial DNA. Cell. 1984 Mar;36(3):635–643. doi: 10.1016/0092-8674(84)90343-x. [DOI] [PubMed] [Google Scholar]
  12. Chomyn A., Mariottini P., Cleeter M. W., Ragan C. I., Matsuno-Yagi A., Hatefi Y., Doolittle R. F., Attardi G. Six unidentified reading frames of human mitochondrial DNA encode components of the respiratory-chain NADH dehydrogenase. Nature. 1985 Apr 18;314(6012):592–597. doi: 10.1038/314592a0. [DOI] [PubMed] [Google Scholar]
  13. Clary D. O., Goddard J. M., Martin S. C., Fauron C. M., Wolstenholme D. R. Drosophila mitochondrial DNA: a novel gene order. Nucleic Acids Res. 1982 Nov 11;10(21):6619–6637. doi: 10.1093/nar/10.21.6619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Clary D. O., Wahleithner J. A., Wolstenholme D. R. Sequence and arrangement of the genes for cytochrome b, URF1, URF4L, URF4, URF5, URF6 and five tRNAs in Drosophila mitochondrial DNA. Nucleic Acids Res. 1984 May 11;12(9):3747–3762. doi: 10.1093/nar/12.9.3747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Clary D. O., Wahleithner J. A., Wolstenholme D. R. Transfer RNA genes in Drosophila mitochondrial DNA: related 5' flanking sequences and comparisons to mammalian mitochondrial tRNA genes. Nucleic Acids Res. 1983 Apr 25;11(8):2411–2425. doi: 10.1093/nar/11.8.2411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Clary D. O., Wolstenholme D. R. A cluster of six tRNA genes in Drosophila mitochondrial DNA that includes a gene for an unusual tRNAserAGY. Nucleic Acids Res. 1984 Mar 12;12(5):2367–2379. doi: 10.1093/nar/12.5.2367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Clary D. O., Wolstenholme D. R. The mitochondrial DNA molecular of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol. 1985;22(3):252–271. doi: 10.1007/BF02099755. [DOI] [PubMed] [Google Scholar]
  18. Clary D. O., Wolstenholme D. R. The ribosomal RNA genes of Drosophila mitochondrial DNA. Nucleic Acids Res. 1985 Jun 11;13(11):4029–4045. doi: 10.1093/nar/13.11.4029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Echalier G., Ohanessian A. Isolement, en cultures in vitro, de lignées cellulaires diploïdes de Drosophila melanogaster. C R Acad Sci Hebd Seances Acad Sci D. 1969 Mar 31;268(13):1771–1773. [PubMed] [Google Scholar]
  20. Feagin J. E., Jasmer D. P., Stuart K. Apocytochrome b and other mitochondrial DNA sequences are differentially expressed during the life cycle of Trypanosoma brucei. Nucleic Acids Res. 1985 Jun 25;13(12):4577–4596. doi: 10.1093/nar/13.12.4577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Feagin J. E., Stuart K. Differential expression of mitochondrial genes between life cycle stages of Trypanosoma brucei. Proc Natl Acad Sci U S A. 1985 May;82(10):3380–3384. doi: 10.1073/pnas.82.10.3380. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Gaines G., Attardi G. Intercalating drugs and low temperatures inhibit synthesis and processing of ribosomal RNA in isolated human mitochondria. J Mol Biol. 1984 Feb 5;172(4):451–466. doi: 10.1016/s0022-2836(84)80017-0. [DOI] [PubMed] [Google Scholar]
  23. Goddard J. M., Wolstenholme D. R. Origin and direction of replication in mitochondrial DNA molecules from Drosophila melanogaster. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3886–3890. doi: 10.1073/pnas.75.8.3886. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Greenawalt J. W. The isolation of outer and inner mitochondrial membranes. Methods Enzymol. 1974;31:310–323. doi: 10.1016/0076-6879(74)31033-6. [DOI] [PubMed] [Google Scholar]
  25. Ise W., Haiker H., Weiss H. Mitochondrial translation of subunits of the rotenone-sensitive NADH:ubiquinone reductase in Neurospora crassa. EMBO J. 1985 Aug;4(8):2075–2080. doi: 10.1002/j.1460-2075.1985.tb03894.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kellems R. E., Allison V. F., Butow R. A. Cytoplasmic type 80 S ribosomes associated with yeast mitochondria. II. Evidence for the association of cytoplasmic ribosomes with the outer mitochondrial membrane in situ. J Biol Chem. 1974 May 25;249(10):3297–3303. [PubMed] [Google Scholar]
  27. Kidd S. J., Glover D. M. A DNA segment from D. melanogaster which contains five tandemly repeating units homologous to the major rDNA insertion. Cell. 1980 Jan;19(1):103–119. doi: 10.1016/0092-8674(80)90392-x. [DOI] [PubMed] [Google Scholar]
  28. Lehrach H., Diamond D., Wozney J. M., Boedtker H. RNA molecular weight determinations by gel electrophoresis under denaturing conditions, a critical reexamination. Biochemistry. 1977 Oct 18;16(21):4743–4751. doi: 10.1021/bi00640a033. [DOI] [PubMed] [Google Scholar]
  29. Merten S. H., Pardue M. L. Mitochondrial DNA in Drosophila. An analysis of genome organization and transcription in Drosophila melanogaster and Drosophila virilis. J Mol Biol. 1981 Nov 25;153(1):1–21. doi: 10.1016/0022-2836(81)90523-4. [DOI] [PubMed] [Google Scholar]
  30. Messing J. New M13 vectors for cloning. Methods Enzymol. 1983;101:20–78. doi: 10.1016/0076-6879(83)01005-8. [DOI] [PubMed] [Google Scholar]
  31. Micard D., Sobrier M. L., Couderc J. L., Dastugue B. Purification of RNA-free plasmid DNA using alkaline extraction followed by Ultrogel A2 column chromatography. Anal Biochem. 1985 Jul;148(1):121–126. doi: 10.1016/0003-2697(85)90636-0. [DOI] [PubMed] [Google Scholar]
  32. Montoya J., Christianson T., Levens D., Rabinowitz M., Attardi G. Identification of initiation sites for heavy-strand and light-strand transcription in human mitochondrial DNA. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7195–7199. doi: 10.1073/pnas.79.23.7195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Ojala D., Merkel C., Gelfand R., Attardi G. The tRNA genes punctuate the reading of genetic information in human mitochondrial DNA. Cell. 1980 Nov;22(2 Pt 2):393–403. doi: 10.1016/0092-8674(80)90350-5. [DOI] [PubMed] [Google Scholar]
  34. Ojala D., Montoya J., Attardi G. tRNA punctuation model of RNA processing in human mitochondria. Nature. 1981 Apr 9;290(5806):470–474. doi: 10.1038/290470a0. [DOI] [PubMed] [Google Scholar]
  35. Oliver N. A., Greenberg B. D., Wallace D. C. Assignment of a polymorphic polypeptide to the human mitochondrial DNA unidentified reading frame 3 gene by a new peptide mapping strategy. J Biol Chem. 1983 May 10;258(9):5834–5839. [PubMed] [Google Scholar]
  36. Peacock W. J., Brutlag D., Goldring E., Appels R., Hinton C. W., Lindsley D. L. The organization of highly repeated DNA sequences in Drosophila melanogaster chromosomes. Cold Spring Harb Symp Quant Biol. 1974;38:405–416. doi: 10.1101/sqb.1974.038.01.043. [DOI] [PubMed] [Google Scholar]
  37. Polan M. L., Friedman S., Gall J. G., Gehring W. Isolation and characterization of mitochondrial DNA from Drosophila melanogaster. J Cell Biol. 1973 Feb;56(2):580–589. doi: 10.1083/jcb.56.2.580. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Pusyriov A. T., Mazo A. M., Minchenko A. G., Avdonina T. A. Transcriptional mapping of the rat liver mitochondrial genome. Gene. 1983 Sep;24(1):115–124. doi: 10.1016/0378-1119(83)90136-1. [DOI] [PubMed] [Google Scholar]
  39. Rastl E., Dawid I. B. Expression of the mitochondrial genome in Xenopus laevis: a map of transcripts. Cell. 1979 Oct;18(2):501–510. doi: 10.1016/0092-8674(79)90067-9. [DOI] [PubMed] [Google Scholar]
  40. Roe B. A., Ma D. P., Wilson R. K., Wong J. F. The complete nucleotide sequence of the Xenopus laevis mitochondrial genome. J Biol Chem. 1985 Aug 15;260(17):9759–9774. [PubMed] [Google Scholar]
  41. Suissa M., Schatz G. Import of proteins into mitochondria. Translatable mRNAs for imported mitochondrial proteins are present in free as well as mitochondria-bound cytoplasmic polysomes. J Biol Chem. 1982 Nov 10;257(21):13048–13055. [PubMed] [Google Scholar]
  42. Tzagoloff A., Macino G., Sebald W. Mitochondrial genes and translation products. Annu Rev Biochem. 1979;48:419–441. doi: 10.1146/annurev.bi.48.070179.002223. [DOI] [PubMed] [Google Scholar]
  43. Wolstenholme D. R., Fauron C. M. A partial map of the circular mitochondrial genome of Drosophila melanogaster. Location of EcoRI-sensitive sites and the adenine-thymine-rich region. J Cell Biol. 1976 Nov;71(2):434–448. doi: 10.1083/jcb.71.2.434. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. de Bruijn M. H. Drosophila melanogaster mitochondrial DNA, a novel organization and genetic code. Nature. 1983 Jul 21;304(5923):234–241. doi: 10.1038/304234a0. [DOI] [PubMed] [Google Scholar]

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