Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
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Complete Nucleotide Sequence and Organization of the Mitogenome of the Red-Spotted Apollo Butterfly, Parnassius bremeri (Lepidoptera: Papilionidae) and Comparison with Other Lepidopteran Insects

  • Kim, Man Il (College of Agriculture and Life Sciences, Chonnam National University) ;
  • Baek, Jee Yeon (College of Agriculture and Life Sciences, Chonnam National University) ;
  • Kim, Min Jee (College of Agriculture and Life Sciences, Chonnam National University) ;
  • Jeong, Heon Cheon (Insect Research Institute of Hampyeong) ;
  • Kim, Ki-Gyoung (Biological Resources Research Department, National Institute of Biological Resources) ;
  • Bae, Chang Hwan (Biological Resources Research Department, National Institute of Biological Resources) ;
  • Han, Yeon Soo (College of Agriculture and Life Sciences, Chonnam National University) ;
  • Jin, Byung Rae (College of Natural Resources and Life Science, Dong-A University) ;
  • Kim, Iksoo (College of Agriculture and Life Sciences, Chonnam National University)
  • Received : 2009.05.06
  • Accepted : 2009.08.04
  • Published : 2009.10.31
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Abstract

The 15,389-bp long complete mitogenome of the endangered red-spotted apollo butterfly, Parnassius bremeri (Lepidoptera: Papilionidae) was determined in this study. The start codon for the COI gene in insects has been extensively discussed, and has long remained a matter of some controversy. Herein, we propose that the CGA (arginine) sequence functions as the start codon for the COI gene in lepidopteran insects, on the basis of complete mitogenome sequences of lepidopteran insects, including P. bremeri, as well as additional sequences of the COI start region from a diverse taxonomic range of lepidopteran species (a total of 53 species from 15 families). In our extensive search for a tRNA-like structure in the A+T-rich region, one $tRNA^{Trp}$-like sequence and one $tRNA^{Leu}(UUR)$-like sequence were detected in the P. bremeri A+T-rich region, and one or more tRNA-like structures were detected in the A+T-rich region of the majority of other sequenced lepidopteran insects, thereby indicating that such features occur frequently in the lepidopteran mitogenomes. Phylogenetic analysis using the concatenated 13 amino acid sequences and nucleotide sequences of PCGs of the four macrolepidopteran superfamilies together with the Tortricoidea and Pyraloidea resulted in the successful recovery of a monophyly of Papilionoidea and a monophyly of Bombycoidea. However, the Geometroidea were unexpectedly identified as a sister group of the Bombycoidea, rather than the Papilionoidea.

Keywords

Acknowledgement

Grant : The Genetic Evaluation of Important Biological Resources, Origin of Biological Diversity of Korea: Molecular Phylogenetic Analyses of Major Korean Taxa

Supported by : National Institute of Biological Resources

References

  1. Abascal, F., Zardoya, R., and Posada, D. (2005). ProTest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104-2105 https://doi.org/10.1093/bioinformatics/bti263
  2. Abascal, F., Posada, D., and Zardoya, R. (2007). MtArt: a new model of amino acid replacement for arthropoda. Mol. Biol. Evol. 24, 1-5
  3. Adachi, J., and Hasegawa, M. (1996). Model of amino acid substitution in proteins encoded by mitochondrial DNA. J. Mol. Evol. 42, 459-468 https://doi.org/10.1007/BF02498640
  4. Akaike, H. (1974). A new look at the statistical model identification. IEEE Trans. Autom. Contr. 19, 716-723
  5. Anderson, S., Bankier, A.T., Barrell, B.G., de Bruijin, M.H.L., Droujn, A.R.J., Eperon, I.C., Nierlich, D.P., Roe, B.A., Sanger, F., Schreier, P.H., et al. (1981). Sequence and organization of the human mitochondrial genome. Nature 290, 457-465 https://doi.org/10.1038/290457a0
  6. Beard, C.B., Mills, D., and Collins, F.H. (1993). The mitochondrial genome of the mosquito Anopheles gambiae: DNA sequence, genome organization, and comparisons with mitochondrial sequences of other insects. Insect Mol. Biol. 2, 103-124 https://doi.org/10.1111/j.1365-2583.1993.tb00131.x
  7. Boore, J.L., lavrov, D., and Brown,W.M. (1998). Gene translocation links insects and crustaceans. Nature 393, 667-668
  8. Brehm, A., Harris, D.J., Hernández, M., Cabrera, V.M., Larruga, J.M., Pinto, F.M., and González, A.M. (2001). Structure and evolution of the mitochondrial DNA complete control region in the Drosophila subobscura subgroup. Insect Mol. Biol. 10, 573-578 https://doi.org/10.1046/j.0962-1075.2001.00295.x
  9. Brown, G.G. (1986). Structural conservation and variation in the Dloop- containing region of vertebrate mitochondrial DNA. J. Mol. Biol. 192, 503-511 https://doi.org/10.1016/0022-2836(86)90272-X
  10. Cameron, S.L., and Whiting, M.F. (2008). The complete mitochondrial genome of the tobacco hornworm, Manduca sexta, (Insecta: Lepidoptera: Sphingidae), and an examination of mitochondrial gene variability within butterflies and moths. Gene 408, 112-123 https://doi.org/10.1016/j.gene.2007.10.023
  11. Cantatore, P., Gadaleta, M.N., Roberti, M., Saccone, C., and Wilson, A.C. (1987). Duplication and remodeling of tRNA genes during the evolutionary rearrangement of mitochondrial genomes. Nature 329, 853-855 https://doi.org/10.1038/329853a0
  12. Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic tool. Curr. Opin. Genet. Dev. 8, 668-674
  13. Cha, S.Y., Yoon, H.J., Lee, E.M., Yoon, M.H., Hwang, J.S., Jin, B.R., Han, Y.S., and Kim, I. (2007). The complete nucleotide sequence and gene organization of the mitochondrial genome of the bumblebee, Bombus ignitus (Hymenoptera: Apidae). Gene 392, 206-220 https://doi.org/10.1016/j.gene.2006.12.031
  14. Clary, D.O., and Wolstenholme, D.R. (1985). The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J. Mol. Evol. 22, 252-271 https://doi.org/10.1007/BF02099755
  15. Clary, D.O., and Wolstenholme, D.R. (1987). 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. 25, 116-125 https://doi.org/10.1007/BF02101753
  16. Coates, B.S., Sumerford, D.V., Hellmich, R.L., and Lewis, L.C. (2005). Partial mitochondrial genome sequences of Ostrinia nubilalis and Ostrinia furnicalis. Int. J. Biol. Sci. 1, 13-18
  17. Crozier, R.H., and Crozier, Y.C. (1993). The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization. Genetics 133, 97-117
  18. Fauron, C.M.R., and Wolstenholmn, D.R. (1980). Extensive diver-sity among Drosophila species with respect to nucleotide sequences within the adenine+thymine-rich region of mitochondrial DNA molecules. Nucleic Acids Res. 8, 2439-2452 https://doi.org/10.1093/nar/8.11.2439
  19. Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3, 294-299
  20. Grimaldi, D., and Engel, M.S. (2005). Evolution of the insects. (New York: Cambridge University Press, Cambridge, U.K.)
  21. Guindon, S., Lethiec, F., Duroux, P., and Gascuel, O. (2005). PHYML Online - a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res. 33, W557-W559 https://doi.org/10.1093/nar/gki352
  22. Hall, T.A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 41, 95-98
  23. Hong, M.Y., Lee, E.M., Jo, Y.H., Park, H.C., Kim, S.R., Hwang, J.S., Jin, B.R., Kang, P.D., Kim, K.-G., Han, Y.S., et al. (2008). Complete nucleotide sequence and organization of the mito-genome of the silk moth Caligula boisduvalii (Lepidoptera: Saturniidae) and comparison with other lepidopteran insects. Gene 413, 49-57
  24. Hong, G., Jiang, S., Yu, M., Yang Y., Li, F., Xue, F., and Wei, Z. (2009a). The complete nucleotide sequence of the mitochondrial genome of the cabbage butterfly, Artogeia melete (Lepidoptera: Pieridae). Acta. Biochim. Biophys. Sin. 41, 446-455 https://doi.org/10.1093/abbs/gmp030
  25. Hong, M.Y., Jeong, H.C., Kim, M.J., Jeong, H.U., Lee, S.H., and Kim, I. (2009b). Complete mitogenome sequence of the jewel beetle, Chrysochroa fulgidissima (Coleoptera: Buprestidae). Mitochondrial DNA. 20, 46-60 https://doi.org/10.1080/19401730802644978
  26. Huelsenbeck, J.P., and Ronquist, F. (2001). MrBayes: Bayesian inference of phylogeny. Bioinformatics 17, 754-755 https://doi.org/10.1093/bioinformatics/17.8.754
  27. Kim, Y.S. (2005). Illustrated book of Korean butterflies in color (Seoul, Korea: Kyo-Hak Pub. Co.)
  28. Kim, I., Lee, E.M., Seol, K.Y., Yun, E.Y., Lee, Y.B., Hwang, J.S., and Jin, B.R. (2006). The mitochondrial genome of the Korean hairstreak, Coreana raphaelis (Lepidoptera: Lycaenidae). Insect Mol. Biol. 15, 217-225 https://doi.org/10.1111/j.1365-2583.2006.00630.x
  29. Kim, S.R., Kim, M.I., Hong, M.Y., Kim, K.Y., Kang, P.D., Hwang, J.S., Han, Y.S., Jin, B.R., and Kim, I. (2009). The complete mitogenome sequence of the Japanese oak silkmoth, Antheraea yamamai (Lepidoptera: Saturniidae). Mol. Biol. Rep. 36, 1871-1880 https://doi.org/10.1007/s11033-008-9393-2
  30. Ko, M.S., Lee, J.S., Kim, C.H., Kim, S.S., and Park, K.T. (2004). Distributional data and ecological characteristics of Parnassius bremeri Bremer in Korea. Kor. J. App. Entomol. 43, 7-14
  31. Kristensen, N.P., Scoble, M.J., and Karsholt, O. (2007). Lepidoptera phylogeny and systematic: the state of inventorying moth and butterfly diversity. Zootaxa 1668, 699-747
  32. Lanave, C., Preparata, G., Saccone, C., and Serio, G. (1984). A new method for calculating evolutionary substitution rates. J. Mol. Evol. 20, 86-93 https://doi.org/10.1007/BF02101990
  33. Lee, E.S., Shin, K.S., Kim, M.S., Park, H., Cho, S., and Kim, C.B. (2006). The mitochondrial genome of the smaller tea tortrix Adoxophyes honmai (Lepidoptera: Tortricidae). Gene 373, 52-57 https://doi.org/10.1016/j.gene.2006.01.003
  34. Liu, Y., Li, Y., Pan, M., Dai, F., Zhu, X., Lu, C., and Xiang, Z. (2008). The complete mitochondrial genome of the Chinese oak silkmoth, Antheraea pernyi (Lepidoptera: Saturniidae). Acta. Biochim. Biophys. Sin. 40, 693-703 https://doi.org/10.1093/abbs/40.8.693
  35. Lowe, T.M., and Eddy, S.R. (1997). tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25, 955-964 https://doi.org/10.1093/nar/25.5.955
  36. Minet, J. (1991). Tentative reconstruction of the ditrysian phylogeny (Lepidoptera: Glossata). Entomol. Scand. 22, 69-95 https://doi.org/10.1163/187631291X00327
  37. Minet, J. (1994). The Bombycoidea: phylogeny and higher classification (Lepidoptera: Glossata). Entomol. Scand. 25, 63-88 https://doi.org/10.1163/187631294X00045
  38. Nardi, F., Caeapelli, A., Dallai, R., and Frati, F. (2003). The mitochondrial genome of the olive fly Bactrocera oleae: two haplotypes from distant geographic locations. Insect Mol. Biol. 12, 605-611 https://doi.org/10.1046/j.1365-2583.2003.00445.x
  39. Nielsen, E.S. (1989). Phylogeny of major lepidopteran groups. In the Hierarchy of Life, B. Fernholm, K. Bremer, and H. Jornvall, eds., (Amsterdam: Elsevier), pp. 281-294
  40. Ohtsuki, T., Kawai, G.., and Watanabe, K. (2002). The minimal tRNA: unique structure of Ascaris suum mitochondrial tRNASer-UCU having a short T arm and lacking the entire D arm. FEBS Lett. 514, 37-43 https://doi.org/10.1016/S0014-5793(02)02328-1
  41. Ojala, D., Montoya, J., and Attardi, G. (1981). tRNA punctuation model of RNA processing in human mitochondria. Nature 290, 470-474 https://doi.org/10.1038/290470a0
  42. Posada, D., and Crandal, K.A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817-818 https://doi.org/10.1093/bioinformatics/14.9.817
  43. Saito, S., Tamuea, K., and Aotsuka, T. (2005). Replicatiion origin of mitochondrial DNA in insects. Genetics 171, 433-448
  44. Salvato, P., Simonato, M., Battisti, A., and Negrisolo, E. (2008). The complete mitochondrial genome of the bag-shelter moth Ochrogaster lunifer (Lepidoptera, Notodontidae). BMC Genomics 9, 331 https://doi.org/10.1186/1471-2164-9-331
  45. Schmidt, H.A., Strimmer, K., and von Haeseler, A. (2002). TREEPUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18, 502-504 https://doi.org/10.1093/bioinformatics/18.3.502
  46. Scott, J. (1986). On the monophyly of the Macrolepidoptera, including a reassessment of their relationship to Cossoidea and Castnioidea, and a reaasignment of Mimallonidae to Pyraloidea. J. Res. Lepid. 25, 30-38
  47. Sheffield, N.C., Song, H., Cameron, S.L., and Whiting, M.F. (2008). A comparative analysis of mitochondrial genomes in Coleoptera (Arthropoda: Insecta) and genome descriptions of six new beetles. Mol. Biol. Evol. 25, 2499-2509 https://doi.org/10.1093/molbev/msn198
  48. Taanman, J.W. (1999). The mitochondrial genome: structure, transcription, translation and replication. Biochim. Biophys. Acta 1410, 103-123 https://doi.org/10.1016/S0005-2728(98)00161-3
  49. Tapper, D.A., and Clayton, D.A. (1981). Mechanism of replication of human mitochondrial DNA: localization of the 5′ ends of nacent daughter strands. J. Biol. Chem. 256, 5109-5115
  50. Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994). Clustal-W - improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680 https://doi.org/10.1093/nar/22.22.4673
  51. Thompson, J.D., Gibson, T.J, Plewniak, F., Jeanmougin, F., and Higgins, D.G. (1997) The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24, 173-216
  52. Weller, S.J., and Pashely, D.P. (1995). In search of butterfly origins. Mol. Phylogenet. Evol. 4, 235-246 https://doi.org/10.1006/mpev.1995.1022
  53. Wernersson, R., and Pedersen, A.G. (2003). Multiple alignment of coding DNA from aligned amino acid sequences. Nucleic Acids Res. 31, 3537-3539 https://doi.org/10.1093/nar/gkg609
  54. Wettstein, W., and Schmid, B. (1999). Conservation of arthropod diversity in montane wetlands: effect of altitude, habitat quality and habitat fragmentation on butterflies and grasshoppers. J. Appl. Ecol. 36, 363-373 https://doi.org/10.1046/j.1365-2664.1999.00404.x
  55. Wilson, K., Cahill, V., Ballment, E., and Benzie, J. (2000). The complete sequence of the mitochondrial genome of the crustacean Penaeus mondon: are malacostracan crustaceans more closely related to insects than to branchiopods? Mol. Biol. Evol. 17, 863-874 https://doi.org/10.1093/oxfordjournals.molbev.a026366
  56. Wolstenholme, D.R. (1992). Animal mitochondrial DNA: structure and evolution. Int. Rev. Cytol. 141, 173-216 https://doi.org/10.1016/S0074-7696(08)62066-5
  57. Woo, H.J., Lee, Y.S., Park, S.J., Lim, J.T., Jang, K.H., Choi, E.H., Choi, Y.G., and Hwang, U.W. (2007). Complete mitochondrial genome of a troglobite millipede Antrokoreana gracilipes (Diplopoda, Juliformia, Julida), and juliformian phylogeny. Mol. Cells, 23, 182-191
  58. Yang, L., Wei, Z.J., Hong, G.Y., Jiang, S.T., and Wen, L.P. (2009). The complete nucleotide sequence of the mitochondrial genome of Phthonandria atrilineata (Lepidoptera: Geometridae). Mol. Biol. Rep. 36, 1441-1449 https://doi.org/10.1007/s11033-008-9334-0
  59. Yukuhiro, K., Sezutsu, H., Itoh, M., Shimizu, K., and Banno, Y. (2002). Significant levels of sequence divergence and gene rearrangements have occurred between the mitochondrial genomes of the wild mulberry silk moth, Bombyx mandarina, and its close relative, the domesticated silk moth, Bombyx mori. Mol. Biol. Evol. 19, 1385-1389 https://doi.org/10.1093/oxfordjournals.molbev.a004200

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