Molecules and Cells

, Volume 28, Issue 3, pp 155–165 | Cite as

Complete mitochondrial genome of brown marmorated stink bug Halyomorpha halys (Hemiptera: Pentatomidae), and phylogenetic relationships of hemipteran suborders

  • Wonhoon Lee
  • Joongnam Kang
  • Chansik Jung
  • Kim Hoelmer
  • Si Hyeock Lee
  • Seunghwan Lee


The newly sequenced complete mitochondrial genome of the brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), is a circular molecule of 16,518 bp with a total A+T content of 76.4% and two extensive repeat regions in A+T rich region. Nucleotide composition and codon usage of H. halys are about average when compared with values observed in 19 other published hemipteran mitochondrial genomes. Phylogenetic analyses using these 20 hemipteran mitochondrial genomes support the currently accepted hypothesis that suborders Heteroptera and Auchenorrhyncha form a monophyletic group. The mitochondrial gene arrangements of the 20 genomes are also consistent with our results.


gene rearrangement Halyomorpha halys Hemiptera mitochondrial genome phylogeny 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Benson, G. (1999). Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27, 573–580.PubMedCrossRefGoogle Scholar
  2. Boore, J.L. (1999) Animal mitochondrial genomes. Nucleic Acids Res. 27, 1767–1780.PubMedCrossRefGoogle Scholar
  3. Boore, J.L., and Brown, W.M. (1998). Big trees from little genomes: mitochondrial gene order as a phylogenetic tool. Curr. Opin. Genet. Dev. 8, 668–674.PubMedCrossRefGoogle Scholar
  4. Boore, J.L., Collins, T.M., Stanton, D., Daehler, L.L., and Brown, W.M. (1995). Deducing the pattern of arthropod phylogeny from mitochondrial DNA rearrangements. Nature 376, 163–165.PubMedCrossRefGoogle Scholar
  5. Boore, J.L., Macey, J.R., and Medina, M. (2005). Sequencing and comparing whole mitochondrial genomes of animals. Meth. Enzymol. 395, 311–348.PubMedCrossRefGoogle Scholar
  6. Carver, M., Gross, G., and Woodward, T. (1991). Hemiptera (bugs, leafhoppers, cicadas, aphids, scale insects etc.). In: CSIRO (ed) The insects of Australia. A textbook for students and research workers, Vol. I, 2nd ed. (Carlton: Melbourne University Press), p. 429.Google Scholar
  7. Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540–552.PubMedGoogle Scholar
  8. Cobben, R.H. (1978). Evolutionary trends in Heteroptera. Part II. Mouthpart-structures and feeding strategies (The Netherlands, Wageningen: Mededelingen Landbouwhogeschool).Google Scholar
  9. Dotson, E.M., and Beard, C.B. (2001). Sequence and organization of the mitochondrial genome of the Chagas disease vector, Triatoma dimidiata. Insect Mol. Biol. 11, 205–215.CrossRefGoogle Scholar
  10. Dowton, M. (1999). Relationships among the cyclostome braconid (Hymenoptera: Braconidae) subfamilies inferred from a mitochondrial tRNA gene rearrangement. Mol. Phylogenet. Evol. 11, 283–287.PubMedCrossRefGoogle Scholar
  11. Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791CrossRefGoogle Scholar
  12. Folmer, O., Black, M., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxydase subunit I from diverse metazoan invertebrates. Mol. Marine Biol. Biotechnol. 3, 294–299.PubMedGoogle Scholar
  13. Goodchild, A. (1966). Evolution of the alimentary canal in the Hemiptera. Biol. Rev. 41, 97–140.CrossRefGoogle Scholar
  14. Hamilton, K. (1981). Morphology and evolution of the rhynchotan head (Insecta: Hemiptera, Homoptera). Can. Entomol. 113, 953–974.CrossRefGoogle Scholar
  15. Hennig, W. (1981). Insect phylogeny (New York: J Wiley and Sons)Google Scholar
  16. Hoebeke, E.R., and Carter, M.E. (2003). Halyomorpha halys (Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. Proc. Entomol. Soc. Wash. 105, 225–237.Google Scholar
  17. Hua, J., Li, M., Dong, P., Cui, Y., Xie, Q., and Bu, W. (2008). Comparative and phylogenomic studies on the mitochondrial genomes of Pentatomomorpha (Insecta: Hemiptera: Heteroptera). BMC Genomics 9, 610.PubMedCrossRefGoogle Scholar
  18. Huelsenbeck, J.P., and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.PubMedCrossRefGoogle Scholar
  19. Jermiin, L.S., and Crozier, R.H. (1994). The cytochrome b region in the mitochondrial DNA of the ant Tetraponera rufoniger: sequence divergence in Hymenoptera may be associated with nucleotide content. J. Mol. Evol. 38, 282–294.PubMedCrossRefGoogle Scholar
  20. Kambhampati, S., and Smith, P.T. (1995). PCR primers for the amplification of four insect mitochondrial gene fragments. Insect Mol. Biol. 4, 233–236.PubMedCrossRefGoogle Scholar
  21. Kim, K.-G., Hong, M.Y., Kim, M.J., Im, H.H., Kim, M.I., Bae, C.H., Seo, S.J., Lee, S.H., and Kim, I. (2009). Complete mitochondrial genome sequence of the yellow-spotted long-horned beetle Psacothea hilaris (Coleoptera: Cerambycidae) and phylogenetic analysis among coleopteran insects. Mol. Cells 27, 429–441.PubMedCrossRefGoogle Scholar
  22. Kristensen, N. (1973). The phylogeny of hexapod “orders.” A critical review of recent accounts. J. Zool. Syst. Evol. Res. 26, 1–44.Google Scholar
  23. Kristensen, N. (1981). Phylogeny of insect orders. Annu. Rev. Entomol. 26, 135–157.CrossRefGoogle Scholar
  24. Kristensen, N.P. (1991). Phylogeny of extant hexapods, In: CSIRO (ed) The insects of Australia. A textbook for students and research workers, Vol. I, 2nd ed. (Carlton: Melbourne University Press), p. 125.Google Scholar
  25. Kukalová-Peck, J. (1991). Fossil history and the evolution of hexapod structures. In: CSIRO (ed) The insects of Australia. A textbook for students and research workers, Vol. I, 2nd ed. (Carlton: Melbourne University Press), p. 141.Google Scholar
  26. Lee, W., Park, J., Choi, J., Jung, K., Park, B., Kim, D., Lee, J., Ahn, K., Song, W., Kang, S., et al. (2009). IMGD: an integrated platform supporting comparative genomics and phylogenetics of insect mitochondrial genomes. BMC Genomics 10, 148.PubMedCrossRefGoogle Scholar
  27. Lessinger, A.C., Martins Junqueira, A.C., Lemos, T.A., Kemper, E.L., da Silva, F.R., Vettore, A.L., Arruda, P., and Azeredo-Espin, A.M. (2000). The mitochondrial genome of the primary screwworm fly Cochliomyia hominivorax (Diptera: Calliphoridae). Insect Mol. Biol. 9, 521–529.PubMedCrossRefGoogle Scholar
  28. 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.PubMedCrossRefGoogle Scholar
  29. Muraji, M., and Tachikawa, S. (2000). Phylogenetic analysis of water striders (Hemiptera:Gerroidea) based on partial sequences of mitochondrial and nuclear ribosomal RNA genes. Entomol. Sci. 3, 615–626.Google Scholar
  30. Muraji, M., Kawasaki, K., and Shimizu, T. (2000). Phylogenetic utility of nucleotide sequences of mitochondrial 16S ribosomal RNA and cytochrome b genes in anthocorid bugs (Heteroptera: Anthocoridae). Appl. Entomol. Zool. (Jpn.) 35, 293–300.CrossRefGoogle Scholar
  31. Nylander, J.A., Ronquist, F., Huelsenbeck, J.P., and Nieves-Aldrey, J.L. (2004). Bayesian phylogenetic analysis of combined data. Syst. Biol. 53, 47–67.PubMedCrossRefGoogle Scholar
  32. Poisson, R., and Pesson, P. (1951). Super-ordre des Hémiptéroïdes (Hemiptera Linné, 1758, Rhynchota Burrueister, 1835), In: Grassé P-P (ed) Traité de Zoologic: Anatomic, Systématique, Biologic. Tome X. Insectes superieurs, et Hémiptéroïdes.2 vols (Masson, Paris), pp. 1–975, 976–1948Google Scholar
  33. Posada, D., and Crandall, K.A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818.PubMedCrossRefGoogle Scholar
  34. Rawlings, T.A., Collins, T.M., and Bieler, R. (2001). A major mitochondrial gene rearrangement among closely related species. Mol. Biol. Evol. 18, 1604–1609.PubMedGoogle Scholar
  35. Rokas, A., and Holland, P.W. (2000). Rare genomic changes as a tool for phylogenetics. Trends Ecol. Evol. 18, 454–459.CrossRefGoogle Scholar
  36. Ross, H. (1965). A textbook of entomology, 3rd ed. (New York: Wiley).Google Scholar
  37. Schuh, R.T., and Slater, J.A. (1995). True bugs of the world (Hemiptera, Heteroptera): Classification and Natural History. (New York: Cornell University Press).Google Scholar
  38. Scudder, G. (1973). Recent advances in the higher systematics and phylogenetic concepts in entomology. Can. Entomol. 105, 1251–1263.Google Scholar
  39. Shao, R., and Barker, S.C. (2003). The highly rearranged mitochondrial genome of the plague thrips, Thrips imaginis (Insecta: Thysanoptera): convergence of two novel gene boundaries and an extraordinary arrangement of rRNA genes. Mol. Biol. Evol. 20, 362–370.PubMedCrossRefGoogle Scholar
  40. Stewart, J.B., and Beckenbach, A.T. (2005). Insect mitochondrial genomics: the complete mitochondrial genome sequence of the meadow spittlebug Philaenus spumarius (Hemiptera: Auchenorrhyncha: Cercopoidae). Genome 48, 46–54.PubMedCrossRefGoogle Scholar
  41. Swofford, D.L. (2002). PAUP*: Phylogenetic analysis using parsimony (*and other methods) Sunderland: Sinauer Associates.Google Scholar
  42. Szelegiewicz, H. (1971). Autapomorphous wing characters in the recent subgroups of Sternorrhyncha (Hemiptera) and their significance in the interpretation of the Paleozoic members of the group. Ann. Zool. Fenn. 29, 1–67.Google Scholar
  43. Thao, M.L., Baumann, L., and Baumann, P. (2004). Organization of the mitochondrial genomes of whiteflies, aphids, and psyllids (Hemiptera, Sternorrhyncha). BMC Evol. Biol. 4, 25.PubMedCrossRefGoogle Scholar
  44. 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. 25, 4876–4882.PubMedCrossRefGoogle Scholar
  45. von Dohlen, C.D., and Moran, N.A. (1995). Molecular phylogeny of the Homoptera: a paraphyletic taxon. J. Mol. Evol. 41, 211–223.CrossRefGoogle Scholar
  46. Wootton, R.J., and Betts, C.R. (1986). Homology and function in the wings of Heteroptera. Syst. Entomol. 11, 389–400.CrossRefGoogle Scholar

Copyright information

© The Korean Society for Molecular and Cellular Biology and Springer Netherlands 2009

Authors and Affiliations

  • Wonhoon Lee
    • 1
  • Joongnam Kang
    • 2
  • Chansik Jung
    • 2
  • Kim Hoelmer
    • 3
  • Si Hyeock Lee
    • 4
  • Seunghwan Lee
    • 1
  1. 1.Insect Biosystematics Laboratory, Research Institute for Agricultural and Life Sciences, Department of Agricultural BiotechnologySeoul National UniversitySeoulKorea
  2. 2.Department of Forest Insect Pests and DiseasesKorea Forest Research InstituteSeoulKorea
  3. 3.Beneficial Insect Introduction Research LaboratoryUSDA Agricultural Research ServiceNewarkUSA
  4. 4.Insect Molecular Biology and Toxicology Laboratory, Research Institute for Agricultural and Life Sciences, Department of Agricultural BiotechnologySeoul National UniversitySeoulKorea

Personalised recommendations