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. 1982 Nov 11;10(21):6619–6637. doi: 10.1093/nar/10.21.6619

Drosophila mitochondrial DNA: a novel gene order.

D O Clary, J M Goddard, S C Martin, C M Fauron, D R Wolstenholme
PMCID: PMC326953  PMID: 6294611

Abstract

Part of the replication origin-containing A+T-rich region of the Drosophila yakuba mtDNA molecule and segments on either side of this region have been sequenced, and the genes within them identified. The data confirm that the small and large rRNA genes lie in tandem adjacent to that side of the A+T-rich region which is replicated first, and establish that a tRNAval gene lies between the two rRNA genes and that URF1 follows the large rRNA gene. The data further establish that the genes for tRNAile, tRNAgln, tRNAf-met and URF2 lie in the order given, on the opposite side of the A+T-rich region to the rRNA genes and, except for tRNAgln, are contained in the opposite strand to the rRNA, tRNAval and URF1 genes. This is in contrast to mammalian mtDNAs where all of these genes are located on the side of the replication origin which is replicated last, within the order tRNAphe, small (12S) rRNA, tRNAval, large (16S) rRNA, tRNAleu, URF1, tRNAile, tRNAgln, tRNAf-met and URF2, and, except tRNAgln, are all contained in the same (H) strand. In D. yakuba URF1 and URF2, the triplet AGA appears to specify an amino acid, which is again different from the situation found in mammalian mtDNAs, where AGA is used only as a rare termination codon.

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Selected References

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

  1. 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]
  2. Anderson S., Gait M. J., Mayol L., Young I. G. A short primer for sequencing DNA cloned in the single-stranded phage vector M13mp2. Nucleic Acids Res. 1980 Apr 25;8(8):1731–1743. doi: 10.1093/nar/8.8.1731. [DOI] [PMC free article] [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. Baer R. J., Dubin D. T. The sequence of a possible 5S RNA-equivalent in hamster mitochondria. Nucleic Acids Res. 1980 Aug 25;8(16):3603–3610. doi: 10.1093/nar/8.16.3603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Barrell B. G., Anderson S., Bankier A. T., de Bruijn M. H., Chen E., Coulson A. R., Drouin J., Eperon I. C., Nierlich D. P., Roe B. A. Different pattern of codon recognition by mammalian mitochondrial tRNAs. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3164–3166. doi: 10.1073/pnas.77.6.3164. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Barrell B. G., Bankier A. T., Drouin J. A different genetic code in human mitochondria. Nature. 1979 Nov 8;282(5735):189–194. doi: 10.1038/282189a0. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Blanc H., Wright C. T., Bibb M. J., Wallace D. C., Clayton D. A. Mitochondrial DNA of chloramphenicol-resistant mouse cells contains a single nucleotide change in the region encoding the 3' end of the large ribosomal RNA. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3789–3793. doi: 10.1073/pnas.78.6.3789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bolivar F. Construction and characterization of new cloning vehicles. III. Derivatives of plasmid pBR322 carrying unique Eco RI sites for selection of Eco RI generated recombinant DNA molecules. Gene. 1978 Oct;4(2):121–136. doi: 10.1016/0378-1119(78)90025-2. [DOI] [PubMed] [Google Scholar]
  10. Bolivar F., Rodriguez R. L., Greene P. J., Betlach M. C., Heyneker H. L., Boyer H. W., Crosa J. H., Falkow S. Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene. 1977;2(2):95–113. [PubMed] [Google Scholar]
  11. Bonitz S. G., Berlani R., Coruzzi G., Li M., Macino G., Nobrega F. G., Nobrega M. P., Thalenfeld B. E., Tzagoloff A. Codon recognition rules in yeast mitochondria. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3167–3170. doi: 10.1073/pnas.77.6.3167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Brosius J., Dull T. J., Noller H. F. Complete nucleotide sequence of a 23S ribosomal RNA gene from Escherichia coli. Proc Natl Acad Sci U S A. 1980 Jan;77(1):201–204. doi: 10.1073/pnas.77.1.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Brosius J., Palmer M. L., Kennedy P. J., Noller H. F. Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli. Proc Natl Acad Sci U S A. 1978 Oct;75(10):4801–4805. doi: 10.1073/pnas.75.10.4801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Brutlag D. L., Clayton J., Friedland P., Kedes L. H. SEQ: a nucleotide sequence analysis and recombination system. Nucleic Acids Res. 1982 Jan 11;10(1):279–294. doi: 10.1093/nar/10.1.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Crews S., Attardi G. The sequences of the small ribosomal RNA gene and the phenylalanine tRNA gene are joined end to end in human mitochondrial DNA. Cell. 1980 Mar;19(3):775–784. doi: 10.1016/s0092-8674(80)80053-5. [DOI] [PubMed] [Google Scholar]
  16. Crews S., Ojala D., Posakony J., Nishiguchi J., Attardi G. Nucleotide sequence of a region of human mitochondrial DNA containing the precisely identified origin of replication. Nature. 1979 Jan 18;277(5693):192–198. doi: 10.1038/277192a0. [DOI] [PubMed] [Google Scholar]
  17. Doolittle R. F. Similar amino acid sequences: chance or common ancestry? Science. 1981 Oct 9;214(4517):149–159. doi: 10.1126/science.7280687. [DOI] [PubMed] [Google Scholar]
  18. Dujon B. Sequence of the intron and flanking exons of the mitochondrial 21S rRNA gene of yeast strains having different alleles at the omega and rib-1 loci. Cell. 1980 May;20(1):185–197. doi: 10.1016/0092-8674(80)90246-9. [DOI] [PubMed] [Google Scholar]
  19. Eperon I. C., Anderson S., Nierlich D. P. Distinctive sequence of human mitochondrial ribosomal RNA genes. Nature. 1980 Jul 31;286(5772):460–467. doi: 10.1038/286460a0. [DOI] [PubMed] [Google Scholar]
  20. Fauron C. M., Wolstenholme D. R. Extensive diversity among Drosophila species with respect to nucleotide sequences within the adenine + thymine-rich region of mitochondrial DNA molecules. Nucleic Acids Res. 1980 Jun 11;8(11):2439–2452. doi: 10.1093/nar/8.11.2439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Fauron C. M., Wolstenholme D. R. Intraspecific diversity of nucleotide sequences within the adenine + thymine-rich region of mitochondrial DNA molecules of Drosophila mauritiana, Drosophila melanogaster and Drosophila simulans. Nucleic Acids Res. 1980 Nov 25;8(22):5391–5410. doi: 10.1093/nar/8.22.5391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Fauron C. M., Wolstenholme D. R. Structural heterogeneity of mitochondrial DNA molecules within the genus Drosophila. Proc Natl Acad Sci U S A. 1976 Oct;73(10):3623–3627. doi: 10.1073/pnas.73.10.3623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ferris S. D., Brown W. M., Davidson W. S., Wilson A. C. Extensive polymorphism in the mitochondrial DNA of apes. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6319–6323. doi: 10.1073/pnas.78.10.6319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Fox T. D., Leaver C. J. The Zea mays mitochondrial gene coding cytochrome oxidase subunit II has an intervening sequence and does not contain TGA codons. Cell. 1981 Nov;26(3 Pt 1):315–323. doi: 10.1016/0092-8674(81)90200-2. [DOI] [PubMed] [Google Scholar]
  25. Goddard J. M., Masters J. N., Jones S. S., Ashworth W. D., Jr, Wolstenholme D. R. Nucleotide sequence variants of Rattus norvegicus mitochondrial DNA. Chromosoma. 1981;82(5):595–609. doi: 10.1007/BF00285770. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Goddard J. M., Wolstenholme D. R. Origin and direction of replication in mitochondrial DNA molecules from the genus Drosophila. Nucleic Acids Res. 1980 Feb 25;8(4):741–757. [PMC free article] [PubMed] [Google Scholar]
  28. Gronenborn B., Messing J. Methylation of single-stranded DNA in vitro introduces new restriction endonuclease cleavage sites. Nature. 1978 Mar 23;272(5651):375–377. doi: 10.1038/272375a0. [DOI] [PubMed] [Google Scholar]
  29. Heckman J. E., Sarnoff J., Alzner-DeWeerd B., Yin S., RajBhandary U. L. Novel features in the genetic code and codon reading patterns in Neurospora crassa mitochondria based on sequences of six mitochondrial tRNAs. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3159–3163. doi: 10.1073/pnas.77.6.3159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Jue R. A., Woodbury N. W., Doolittle R. F. Sequence homologies among E. coli ribosomal proteins: evidence for evolutionarily related groupings and internal duplications. J Mol Evol. 1980 May;15(2):129–148. doi: 10.1007/BF01732666. [DOI] [PubMed] [Google Scholar]
  31. Kim S. H., Suddath F. L., Quigley G. J., McPherson A., Sussman J. L., Wang A. H., Seeman N. C., Rich A. Three-dimensional tertiary structure of yeast phenylalanine transfer RNA. Science. 1974 Aug 2;185(4149):435–440. doi: 10.1126/science.185.4149.435. [DOI] [PubMed] [Google Scholar]
  32. Klukas C. K., Dawid I. B. Characterization and mapping of mitochondrial ribosomal RNA and mitochondrial DNA in Drosophila melanogaster. Cell. 1976 Dec;9(4 Pt 1):615–625. doi: 10.1016/0092-8674(76)90044-1. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. Messing J., Crea R., Seeburg P. H. A system for shotgun DNA sequencing. Nucleic Acids Res. 1981 Jan 24;9(2):309–321. doi: 10.1093/nar/9.2.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Messing J., Gronenborn B., Müller-Hill B., Hans Hopschneider P. Filamentous coliphage M13 as a cloning vehicle: insertion of a HindII fragment of the lac regulatory region in M13 replicative form in vitro. Proc Natl Acad Sci U S A. 1977 Sep;74(9):3642–3646. doi: 10.1073/pnas.74.9.3642. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Montoya J., Ojala D., Attardi G. Distinctive features of the 5'-terminal sequences of the human mitochondrial mRNAs. Nature. 1981 Apr 9;290(5806):465–470. doi: 10.1038/290465a0. [DOI] [PubMed] [Google Scholar]
  37. Ojala D., Crews S., Montoya J., Gelfand R., Attardi G. A small polyadenylated RNA (7 S RNA), containing a putative ribosome attachment site, maps near the origin of human mitochondrial DNA replication. J Mol Biol. 1981 Aug 5;150(2):303–314. doi: 10.1016/0022-2836(81)90454-x. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. 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]
  40. Polisky B., Greene P., Garfin D. E., McCarthy B. J., Goodman H. M., Boyer H. W. Specificity of substrate recognition by the EcoRI restriction endonuclease. Proc Natl Acad Sci U S A. 1975 Sep;72(9):3310–3314. doi: 10.1073/pnas.72.9.3310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Ramirez J. L., Dawid I. B. Mapping of mitochondrial DNA in Xenopus laevis and X. borealis: the positions of ribosomal genes and D-loops. J Mol Biol. 1978 Feb 15;119(1):133–146. doi: 10.1016/0022-2836(78)90273-5. [DOI] [PubMed] [Google Scholar]
  42. 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]
  43. Sanger F., Coulson A. R., Barrell B. G., Smith A. J., Roe B. A. Cloning in single-stranded bacteriophage as an aid to rapid DNA sequencing. J Mol Biol. 1980 Oct 25;143(2):161–178. doi: 10.1016/0022-2836(80)90196-5. [DOI] [PubMed] [Google Scholar]
  44. Sanger F., Coulson A. R. The use of thin acrylamide gels for DNA sequencing. FEBS Lett. 1978 Mar 1;87(1):107–110. doi: 10.1016/0014-5793(78)80145-8. [DOI] [PubMed] [Google Scholar]
  45. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Schnare M. N., Gray M. W. 3'-Terminal sequence of wheat mitochondrial 18S ribosomal RNA: further evidence of a eubacterial evolutionary origin. Nucleic Acids Res. 1982 Jul 10;10(13):3921–3932. doi: 10.1093/nar/10.13.3921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Seilhamer J. J., Cummings D. J. Structure and sequence of the mitochondrial 20S rRNA and tRNA tyr gene of Paramecium primaurelia. Nucleic Acids Res. 1981 Dec 11;9(23):6391–6406. doi: 10.1093/nar/9.23.6391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Sekiya T., Kobayashi M., Seki T., Koike K. Nucleotide sequence of a cloned fragment of rat mitochondrial DNA containing the replication origin. Gene. 1980 Oct;11(1-2):53–62. doi: 10.1016/0378-1119(80)90086-4. [DOI] [PubMed] [Google Scholar]
  49. Upholt W. B., Dawid I. B. Mapping of mitochondrial DNA of individual sheep and goats: rapid evolution in the D loop region. Cell. 1977 Jul;11(3):571–583. doi: 10.1016/0092-8674(77)90075-7. [DOI] [PubMed] [Google Scholar]
  50. Van Etten R. A., Walberg M. W., Clayton D. A. Precise localization and nucleotide sequence of the two mouse mitochondrial rRNA genes and three immediately adjacent novel tRNA genes. Cell. 1980 Nov;22(1 Pt 1):157–170. doi: 10.1016/0092-8674(80)90164-6. [DOI] [PubMed] [Google Scholar]
  51. Walberg M. W., Clayton D. A. Sequence and properties of the human KB cell and mouse L cell D-loop regions of mitochondrial DNA. Nucleic Acids Res. 1981 Oct 24;9(20):5411–5421. doi: 10.1093/nar/9.20.5411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. 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]

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