The complete mitochondrial genomes sequences of Asio flammeus and Asio otus and comparative analysis

  • Yi Sun
  • Fei Ma
  • Bing Xiao
  • Junjie Zheng
  • Xiaodong Yuan
  • Minqian Tang
  • Li Wang
  • Yefei Yu
  • Qingwei Li
Article
  • 41 Downloads

Abstract

The complete mitochondrial genomes of Asio flammeus and Asio otus were sequenced and found to span 18858 bp and 18493 bp, respectively. It is surprising to find the former to be the largest among all avian mitochondrial genomes sequenced so far. The two genomes have very similar gene order with that of Gallus gallus, neither contains the pseudo control region, but both have a single extra base, namely Cytidine, at position 174 in ND3 gene. The control regions of Asio flammeus and Asio otus’ mitochondrial genomes span 3288 bp and 2926 bp respectively, which are the longest among vertebrates except for Myxine glutinosa and contribute to the large size of two genomes. The 3′ end of the control region of Asio flammeus and Asio otus contains many tandemly repeated sequences, which are highly similar to a putative control element, i.e. Mt5, and may form stable stem-loop secondary structures. Such repeated sequences probably play an important role in regulating transcription and replication of mitochondrial genome. Our results may provide important clues for uncovering the origin and evolution mechanisms of mitochondrion genome.

Keywords

Asio flammeus Asio otus mitochondrial genome control region repeated sequence 

References

  1. 1.
    Stoneking, M., Soodyall, H., Human evolution and the mitochondrial genome, Curr. Opin. Genet. Dev., 1996, 6(6): 731–736.PubMedCrossRefGoogle Scholar
  2. 2.
    Zardoya, R., Meyer, A., The complete nucleotide sequence of the mitochondrial genome of the lungfish (Protopterus dolloi) supports its phylogenetic position as a close relative of land vertebrates, Genetics, 1996, 142: 1249–1263.PubMedGoogle Scholar
  3. 3.
    Naylor, G. J., Brown, W. M., Amphioxus mitochondrial DNA, chordate phylogeny, and the limits of inference based on comparisons of sequences, Syst. Biol., 1998, 47: 61–76.PubMedCrossRefGoogle Scholar
  4. 4.
    Rasmussen, A. S., Arnason, U., Phylogenetic studies of complete mitochondrial DNA molecules place cartilaginous fishes within the tree ofbony fishes, J. Mol. Evol., 1999, 48: 118–123.PubMedCrossRefGoogle Scholar
  5. 5.
    Anderson, S., Bankier, A. T., Barrell, B. G. et al., Sequence and organization of the human mitochondrial genome, Nature, 1981, 290: 457–465.PubMedCrossRefGoogle Scholar
  6. 6.
    Li, Q. W., Chen, Y. F., Enlarge the mitochondrial genome in bird, Zoological Research (in Chinese), 1996, 17(4): 376, 384,392.Google Scholar
  7. 7.
    Haring, E., Kruckenhauser, L., Gamauf, A. et al., The complete sequence of the mitochondrial genome of Buteo buteo (Aves, Accipitridae) indicates an early split in the phylogeny of raptors, Mol. Biol. Evol., 2001, 18(10): 1892–1904.PubMedGoogle Scholar
  8. 8.
    Mindell, D. P., Sorenson, M. D., Dimcheff, D. E. et al., Interordinal relationships of birds and other reptiles based on whole mitochondrial genomes, Syst. Biol., 1999, 48 (1): 138–152.PubMedCrossRefGoogle Scholar
  9. 9.
    Harrison, G. L., Mclenachan, P. A., Phillips, M. J. et al., Four new avian mitochondrial genomes help get to basic evolutionary questions in the Late Cretaceous, Mol. Biol. Evol., 2004, 21(6): 974–983.PubMedCrossRefGoogle Scholar
  10. 10.
    Arnason, U., Gullberg, A., Widegren, B., The complete nucleotide sequence of the mitochondrial DNA of the fin whale, Balaenopteraphysalus, J. Mol. Evol., 1991, 33: 556–568.PubMedCrossRefGoogle Scholar
  11. 11.
    Sorenson, M. D., Ast, J. C., Dimcheff, D. E. et al., Primers for a PCR-based approach to mitochondrial genome sequencing in birds and other vertebrates, Mol. Phylogenet. Evol., 1999, 12(2): 105–114.PubMedCrossRefGoogle Scholar
  12. 12.
    Thompson, J. D., Gibson, T. J., Plewniak, F. et al., The ClustalX windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools, Nucleic Acids Res., 1997, 24:4876–4882.CrossRefGoogle Scholar
  13. 13.
    Desjardins, P., Morais, R., Sequence and gene organization of the chicken mitochondrial genome, J. Mol. Biol., 1990, 212: 599–634.PubMedCrossRefGoogle Scholar
  14. 14.
    Mindell, D. P., Sorenson, M. D., Dimcheff, D. E., Multiple independent origins of mitochondrial gene order in birds, Proc. Natl. Acad. Sci. USA, 1998, 95: 10693–10697.PubMedCrossRefGoogle Scholar
  15. 15.
    Slack, K. E., Janke, A., Penny, D. et al., Two new avian mitochondrial genomes (penguin and goose) and a summary of birds and reptile mitogenomic features, Gene, 2003, 302: 43–52.PubMedCrossRefGoogle Scholar
  16. 16.
    Mindell, D. P., Sorenson, M. D., Dimcheff, D. E., An extra nucleotide is not translated in mitochondrial ND3 of some birds and turtles, Mol. Biol. Evol., 1998, 15(11): 1568–1571.PubMedGoogle Scholar
  17. 17.
    Brown, G. G., Gadaleta, G., Pepe, G. et al., Structural conservation and variation in the D-loop containing region of vertebrate mitochondrial DNA, J. Mol. Biol., 1986, 192: 503–511.PubMedCrossRefGoogle Scholar
  18. 18.
    Saccone, C., Pesole, G., Sbisa, E., The main regulatory region of mammalian mitochondrial DNA: Structure-function model and evolutionary pattern, J. Mol. Evol., 1991, 33: 83–91.PubMedCrossRefGoogle Scholar
  19. 19.
    Ruokonen, M., Kvist, L., Structure and evolution of the avian mitochondrial control region, Mol. Phylogenet. Evol., 2002, 23: 422–432.PubMedCrossRefGoogle Scholar
  20. 20.
    Delarbre, C., Rasmussen, A. S., Arnason, U. et al., The complete mitochondrial genome of the hagfish Myxine glutinosa: Unique features of the control region, J. Mol. Evol., 2001, 53: 634–641.PubMedCrossRefGoogle Scholar
  21. 21.
    Bensch, S., Harlid, A., Mitochondrial genomic rearrangements in songbirds, Mol. Biol. Evol., 2000, 17(1): 107–113.PubMedGoogle Scholar
  22. 22.
    Haddrath, O., Baker, A. J., Complete mitochondrial DNA genome sequences of extinct birds: Ratite phylogenetics and the vicariance biogeography hypothesis, Proc. R. Soc. Lond. B., 2001, 268: 939–945.CrossRefGoogle Scholar
  23. 23.
    Nishibori, M., Hayashi, T., Tsudzuki, M. et al., Complete sequence of the Japanese quail (Coturnix japonica) mitochondrial genome and its genetic relationship with related species, Anim. Genet., 2001, 32(6): 380–385.PubMedCrossRefGoogle Scholar
  24. 24.
    Ojala, D., Montoya, J., Attardi, G., tRNA punctuation model of RNA processing in human mitochondria, Nature, 1981, 290: 470–474.PubMedCrossRefGoogle Scholar
  25. 25.
    Crick, F. H., Codon-anticodon pairing: The Wobble Hypothesis, J. Mol. Biol., 1966, 19: 548–555.PubMedCrossRefGoogle Scholar
  26. 26.
    Chen, W. C., Chen, Z. H., Wang, Z. Q. et al., Symmetrial analysis of the motochondrial and genomic codes, Acta Biophysica Sinica (in Chinese), 2002, 18: 87–94.Google Scholar
  27. 27.
    Moritz, C., Dowling, T. E., Brown, W. M., Evolution of animal mitochondrial DNA: Relevance for population biology and systematics, Ann. Rev. Ecol. Syst., 1987, 18: 269–292.CrossRefGoogle Scholar
  28. 28.
    Buroker, N. E., Brown, J. R., Gilbert, T. A. et al., Length heteroplasmy of sturgeon mitochondrial DNA: An illegitimate elongation model, Genetics, 1990, 124: 157–163.PubMedGoogle Scholar
  29. 29.
    Faber, J. E., Stepien, C. A., Tandemly repeated sequences in the mitochondrial DNA control region and phylogeography of the pike-perches Stizostedion, Mol. Phylogenet. Evol., 1998, 10: 310–322.PubMedCrossRefGoogle Scholar
  30. 30.
    Ohno, K., Tanaka, M., Suzuki, H. et al., Identification of a possible control element, Mt5, in the major noncoding region of mitochondrial DNA by intraspecific nucleotide conservation, Biochem. Int., 1991, 24(2): 263–271.PubMedGoogle Scholar
  31. 31.
    Kumar, S., Suzuki, H., Onoue, S. et al., Rat mitochondrial mtDNA binding proteins to inter-specifically conserved sequences in the displacement loop region of vertebrate mtDNA, Biochem. Mol. Biol. Int., 1995, 36(5): 973–981.PubMedGoogle Scholar
  32. 32.
    Nesbo, C. L., Arab, M. O., Jakobsen, K. S., Heteroplasmy, length and sequence variation in the mtDNA control region of three percid fish species (Perca fluviatilis, Acerina cernua, Stizostedion lucioperca), Genetics, 1998, 148: 1907–1919.PubMedGoogle Scholar
  33. 33.
    Delport, W., Ferguson, J. W., Bloomer, P., Characterization and evolution of the mitochondrial DNA control region in Hornbills (Bucerotifoormes), J. Mol. Evol., 2002, 54: 794–806.PubMedCrossRefGoogle Scholar
  34. 34.
    Randi, E., Lucchini, V., Organization and evolution of the mitochondrial DNA control region in the Avian Genus Alectoris, J. Mol. Evol., 1998, 47:449–462.PubMedCrossRefGoogle Scholar
  35. 35.
    Fumagalli, L., Taberlet, P., Favre, L. et al., Origin and evolution of homologous repeated sequences in the mitochondrial DNA control region of shrews, Mol. Biol. Evol., 1996, 13(1): 31–46.PubMedGoogle Scholar
  36. 36.
    Crochet, P. A., Desmarais, E., Slow rate of evolution in the mitochondrial control region of gulls (Aves: Laridae), Mol. Biol. Evol., 2000, 17(12): 1797–1806.PubMedGoogle Scholar
  37. 37.
    Sbisa, E., Tanzariello, F., Reyes, A. et al., Mammalian mitochondrial D-loop region structural analysis: Identification of new conserved sequences and their functional and evolutionary implications, Gene, 1997, 205: 125–140.PubMedCrossRefGoogle Scholar
  38. 38.
    Casane, D., Dennebouy, N., Rochambeau, H. et al., Nonneutral evolution of tandem repeats in the mitochondrial DNA control region of Lagomorphs, Mol. Biol. Evol., 1997, 14(8): 779–789.PubMedGoogle Scholar
  39. 39.
    Ravago, R. G., Monje, V. D., Juinio-Menez, M. A., Length and sequence variability in mitochondrial control region of the Milkfish, Chanos chanos, Mar. Biotechnol., 2002, 4: 40–50.PubMedCrossRefGoogle Scholar
  40. 40.
    Douzery, E., Randi, E., The mitochondrial control region of Cervidae: Evolutionary patterns and phylogenetic content, Mol. Biol. Evol., 1997, 14(11): 1154–1166.PubMedGoogle Scholar
  41. 41.
    Margulis, L., Origin of Eukaryotic Cells, New Haven: Yale University Press, 1970.Google Scholar
  42. 42.
    Andersson, S. G., Zomorodipour, A., Andersson, J. O. et al., The genome sequence of Rickettsia prowazekii and the origin of mitochondria, Nature, 1998, 396(6707): 133–140.PubMedCrossRefGoogle Scholar
  43. 43.
    Cavalier-Smith, T., The simultaneous symbiotic origin of mitochondria, chloroplasts, and microbodies, Ann. N. Y. Acad. Sci., 1987, 503:55–71.PubMedCrossRefGoogle Scholar

Copyright information

© Science in China Press 2004

Authors and Affiliations

  • Yi Sun
    • 1
  • Fei Ma
    • 1
  • Bing Xiao
    • 1
  • Junjie Zheng
    • 2
  • Xiaodong Yuan
    • 2
  • Minqian Tang
    • 2
  • Li Wang
    • 3
  • Yefei Yu
    • 3
  • Qingwei Li
    • 1
  1. 1.College of Life SciencesLiaoning Normal UniversityDalianChina
  2. 2.TaKaRa Biotechnology (Dalian) Co., Ltd.DalianChina
  3. 3.The Administrative Office of the Natural Protective Zone of Snake Island-Lao Tie HillDalianChina

Personalised recommendations