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Genetics. Jan 1993; 133(1): 97–117.
PMCID: PMC1205303

The Mitochondrial Genome of the Honeybee Apis Mellifera: Complete Sequence and Genome Organization

Abstract

The complete sequence of honeybee (Apis mellifera) mitochondrial DNA is reported being 16,343 bp long in the strain sequenced. Relative to their positions in the Drosophila map, 11 of the tRNA genes are in altered positions, but the other genes and regions are in the same relative positions. Comparisons of the predicted protein sequences indicate that the honeybee mitochondrial genetic code is the same as that for Drosophila; but the anticodons of two tRNAs differ between these two insects. The base composition shows extreme bias, being 84.9% AT (cf. 78.6% in Drosophila yakuba). In protein-encoding genes, the AT bias is strongest at the third codon positions (which in some cases lack guanines altogether), and least in second codon positions. Multiple stepwise regression analysis of the predicted products of the protein-encoding genes shows a significant association between the numbers of occurrences of amino acids and %T in codon family, but not with the number of codons per codon family or other parameters associated with codon family base composition. Differences in amino acid abundances are apparent between the predicted Apis and Drosophila proteins, with a relative abundance in the Apis proteins of lysine and a relative deficiency of alanine. Drosophila alanine residues are as often replaced by serine as conserved in Apis. The differences in abundances between Drosophila and Apis are associated with %AT in the codon families, and the degree of divergence in amino acid composition between proteins correlates with the divergence in %AT at the second codon positions. Overall, transversions are about twice as abundant as transitions when comparing Drosophila and Apis protein-encoding genes, but this ratio varies between codon positions. Marked excesses of transitions over chance expectation are seen for the third positions of protein-coding genes and for the gene for the small subunit of ribosomal RNA. For the third codon positions the excess of transitions is adequately explained as due to the restriction of observable substitutions to transitions for conserved amino acids with two-codon families; the excess of transitions over expectation for the small ribosomal subunit suggests that the conservation of nucleotide size is favored by selection.

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Selected References

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  • Almagor H. A Markov analysis of DNA sequences. J Theor Biol. 1983 Oct 21;104(4):633–645. [PubMed]
  • Bernardi G. The isochore organization of the human genome. Annu Rev Genet. 1989;23:637–661. [PubMed]
  • Clary DO, Goddard JM, Martin SC, Fauron CM, Wolstenholme DR. Drosophila mitochondrial DNA: a novel gene order. Nucleic Acids Res. 1982 Nov 11;10(21):6619–6637. [PMC free article] [PubMed]
  • Clary DO, Wahleithner JA, Wolstenholme DR. 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. [PMC free article] [PubMed]
  • Clary DO, Wolstenholme DR. Genes for cytochrome c oxidase subunit I, URF2, and three tRNAs in Drosophila mitochondrial DNA. Nucleic Acids Res. 1983 Oct 11;11(19):6859–6872. [PMC free article] [PubMed]
  • Clary DO, Wolstenholme DR. 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. [PMC free article] [PubMed]
  • Clary DO, Wolstenholme DR. The mitochondrial DNA molecular of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol. 1985;22(3):252–271. [PubMed]
  • Clary DO, Wolstenholme DR. Drosophila mitochondrial DNA: conserved sequences in the A + T-rich region and supporting evidence for a secondary structure model of the small ribosomal RNA. J Mol Evol. 1987;25(2):116–125. [PubMed]
  • Cornuet JM, Garnery L, Solignac M. Putative origin and function of the intergenic region between COI and COII of Apis mellifera L. mitochondrial DNA. Genetics. 1991 Jun;128(2):393–403. [PMC free article] [PubMed]
  • Crozier RH, Crozier YC, Mackinlay AG. The CO-I and CO-II region of honeybee mitochondrial DNA: evidence for variation in insect mitochondrial evolutionary rates. Mol Biol Evol. 1989 Jul;6(4):399–411. [PubMed]
  • de Bruijn MH. Drosophila melanogaster mitochondrial DNA, a novel organization and genetic code. Nature. 1983 Jul 21;304(5923):234–241. [PubMed]
  • DeSalle R, Freedman T, Prager EM, Wilson AC. Tempo and mode of sequence evolution in mitochondrial DNA of Hawaiian Drosophila. J Mol Evol. 1987;26(1-2):157–164. [PubMed]
  • Desjardins P, Morais R. Sequence and gene organization of the chicken mitochondrial genome. A novel gene order in higher vertebrates. J Mol Biol. 1990 Apr 20;212(4):599–634. [PubMed]
  • Goddard JM, Wolstenholme DR. 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. [PMC free article] [PubMed]
  • Goddard JM, Wolstenholme DR. 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]
  • HsuChen CC, Dubin DT. A cluster of four transfer RNA genes in mosquito mitochondrial DNA. Biochem Int. 1984 Mar;8(3):385–391. [PubMed]
  • HsuChen CC, Kotin RM, Dubin DT. Sequences of the coding and flanking regions of the large ribosomal subunit RNA gene of mosquito mitochondria. Nucleic Acids Res. 1984 Oct 25;12(20):7771–7785. [PMC free article] [PubMed]
  • Ojala D, Montoya J, Attardi G. tRNA punctuation model of RNA processing in human mitochondria. Nature. 1981 Apr 9;290(5806):470–474. [PubMed]
  • Osawa S, Jukes TH, Watanabe K, Muto A. Recent evidence for evolution of the genetic code. Microbiol Rev. 1992 Mar;56(1):229–264. [PMC free article] [PubMed]
  • Päbo S, Thomas WK, Whitfield KM, Kumazawa Y, Wilson AC. Rearrangements of mitochondrial transfer RNA genes in marsupials. J Mol Evol. 1991 Nov;33(5):426–430. [PubMed]
  • Rebeck GW, Samson L. Increased spontaneous mutation and alkylation sensitivity of Escherichia coli strains lacking the ogt O6-methylguanine DNA repair methyltransferase. J Bacteriol. 1991 Mar;173(6):2068–2076. [PMC free article] [PubMed]
  • Roe BA, Ma DP, Wilson RK, Wong JF. The complete nucleotide sequence of the Xenopus laevis mitochondrial genome. J Biol Chem. 1985 Aug 15;260(17):9759–9774. [PubMed]
  • Saccone C, Pesole G, Sbisá E. The main regulatory region of mammalian mitochondrial DNA: structure-function model and evolutionary pattern. J Mol Evol. 1991 Jul;33(1):83–91. [PubMed]
  • Sanger F, Coulson AR, Barrell BG, Smith AJ, Roe BA. Cloning in single-stranded bacteriophage as an aid to rapid DNA sequencing. J Mol Biol. 1980 Oct 25;143(2):161–178. [PubMed]
  • Satta Y, Ishiwa H, Chigusa SI. Analysis of nucleotide substitutions of mitochondrial DNAs in Drosophila melanogaster and its sibling species. Mol Biol Evol. 1987 Nov;4(6):638–650. [PubMed]
  • Smith DR, Brown WM. Polymorphisms in mitochondrial DNA of European and Africanized honeybees (Apis mellifera). Experientia. 1988 Mar 15;44(3):257–260. [PubMed]
  • Vlasak I, Burgschwaiger S, Kreil G. Nucleotide sequence of the large ribosomal RNA of honeybee mitochondria. Nucleic Acids Res. 1987 Mar 11;15(5):2388–2388. [PMC free article] [PubMed]
  • Wolstenholme DR, Clary DO. Sequence evolution of Drosophila mitochondrial DNA. Genetics. 1985 Apr;109(4):725–744. [PMC free article] [PubMed]
  • Wolstenholme DR, Macfarlane JL, Okimoto R, Clary DO, Wahleithner JA. Bizarre tRNAs inferred from DNA sequences of mitochondrial genomes of nematode worms. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1324–1328. [PMC free article] [PubMed]

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