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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

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Molecules and Cells

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 tRNATrp-like sequence and one tRNALeu (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.

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References

  • Abascal, F., Zardoya, R., and Posada, D. (2005). ProTest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104–2105.

    Article  CAS  PubMed  Google Scholar 

  • Abascal, F., Posada, D., and Zardoya, R. (2007). MtArt: a new model of amino acid replacement for arthropoda. Mol. Biol. Evol. 24, 1–5.

    Article  CAS  PubMed  Google Scholar 

  • Adachi, J., and Hasegawa, M. (1996). Model of amino acid substitution in proteins encoded by mitochondrial DNA. J. Mol. Evol. 42, 459–468.

    Article  CAS  PubMed  Google Scholar 

  • Akaike, H. (1974). A new look at the statistical model identification. IEEE Trans. Autom. Contr. 19, 716–723.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Boore, J.L., Iavrov, D., and Brown, W.M. (1998). Gene translocation links insects and crustaceans. Nature 393, 667–668.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Brown, G.G. (1986). Structural conservation and variation in the D-loop-containing region of vertebrate mitochondrial DNA. J. Mol. Biol. 192, 503–511.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic tool. Curr. Opin. Genet. Dev. 8, 668–674.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Grimaldi, D., and Engel, M.S. (2005). Evolution of the insects. (New York: Cambridge University Press, Cambridge, U.K.).

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Huelsenbeck, J.P., and Ronquist, F. (2001). MrBayes: Bayesian inference of phylogeny. Bioinformatics 17, 754–755.

    Article  CAS  PubMed  Google Scholar 

  • Kim, Y.S. (2005). Illustrated book of Korean butterflies in color (Seoul, Korea: Kyo-Hak Pub. Co.).

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Lanave, C., Preparata, G., Saccone, C., and Serio, G. (1984). A new method for calculating evolutionary substitution rates. J. Mol. Evol. 20, 86–93.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Minet, J. (1991). Tentative reconstruction of the ditrysian phylogeny (Lepidoptera: Glossata). Entomol. Scand. 22, 69–95.

    Google Scholar 

  • Minet, J. (1994). The Bombycoidea: phylogeny and higher classification (Lepidoptera: Glossata). Entomol. Scand. 25, 63–88.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Nielsen, E.S. (1989). Phylogeny of major lepidopteran groups. In the Hierarchy of Life, B. Fernholm, K. Bremer, and H. Jörnvall, eds., (Amsterdam: Elsevier), pp. 281–294.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Ojala, D., Montoya, J., and Attardi, G. (1981). tRNA punctuation model of RNA processing in human mitochondria. Nature 290, 470–474.

    Article  CAS  PubMed  Google Scholar 

  • Posada, D., and Crandal, K.A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.

    Article  CAS  PubMed  Google Scholar 

  • Saito, S., Tamuea, K., and Aotsuka, T. (2005). Replicatiion origin of mitochondrial DNA in insects. Genetics 171, 433–448.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Schmidt, H.A., Strimmer, K., and von Haeseler, A. (2002). TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18, 502–504.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Taanman, J.W. (1999). The mitochondrial genome: structure, transcription, translation and replication. Biochim. Biophys. Acta 1410, 103–123.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • Weller, S.J., and Pashely, D.P. (1995). In search of butterfly origins. Mol. Phylogenet. Evol. 4, 235–246.

    Article  CAS  PubMed  Google Scholar 

  • Wernersson, R., and Pedersen, A.G. (2003). Multiple alignment of coding DNA from aligned amino acid sequences. Nucleic Acids Res. 31, 3537–3539.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Wolstenholme, D.R. (1992). Animal mitochondrial DNA: structure and evolution. Int. Rev. Cytol. 141, 173–216.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

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Correspondence to Iksoo Kim.

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Kim, M.I., Baek, J.Y., Kim, M.J. et al. Complete nucleotide sequence and organization of the mitogenome of the red-spotted apollo butterfly, Parnassius bremeri (Lepidoptera: Papilionidae) and comparison with other lepidopteran insects. Mol Cells 28, 347–363 (2009). https://doi.org/10.1007/s10059-009-0129-5

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