Skip to main content
Log in

Complete mitochondrial genomes of two cockroaches, Blattella germanica and Periplaneta americana, and the phylogenetic position of termites

  • Research Article
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

The mitochondrial genomes are one of the most information-rich markers in phylogenetics. The relationships within superorder Dictyoptera have been debated in the literature. However, the closely related termites (Isoptera) are retained as unranked taxon within the order Blattaria (cockroaches). In this work, we sequenced the complete mitogenomes of two cockroaches, reconstructed the molecular phylogeny and attempted to infer the phylogenetic position of termites in Blattaria more reliably. The complete mtDNA nucleotide sequences of the peridomestic American cockroach (Periplaneta americana L.) and the domestic German cockroach (Blattella germanica L.) are 15,025 and 15,584 bp in size, respectively. The genome shares the gene order and orientation with previously known Blattaria mitogenomes. Most tRNAs could be folded into the typical cloverleaf secondary structure, but the tRNA-Ser (AGN) of P. americana appears to be missing the dihydrouridine arm. Using nucleotide and amino acid sequences as phylogenetic markers, we proposed that termites should be treated as a superfamily (Termitoidea) of cockroaches. We suggested that Polyphagoidea was the sister group of Termitoidea in Blattaria and supported that the suborder Caelifera is more closely related to the Phasmatodea than to the suborder Ensifera of Orthoptera.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Anderson S, Bankier AT, Barrell BG, de Bruijn MH, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJ, Staden R, Young IG (1981) Sequence and organization of the human mitochondrial genome. Nature 290:457–465

    Article  PubMed  CAS  Google Scholar 

  • Boore JL, Lavrov DV, Brown WM (1998) Gene translocation links insects and crustaceans. Nature 392:667–668

    Article  PubMed  CAS  Google Scholar 

  • Caterino MS, Sperling FA (1999) Papilio phylogeny based on mitochondrial cytochrome oxidase I and II genes. Mol Phylogenet Evol 11:122–137

    Article  PubMed  CAS  Google Scholar 

  • Clary DO, Goddard JM, Martin SC, Fauron CM, Wolstenholme DR (1982) Drosophila mitochondrial DNA: a novel gene order. Nucleic Acids Res 10:6619–6637

    Article  PubMed  CAS  Google Scholar 

  • Coucheron D, Nymark M, Breines R, Karlsen B, Andreassen M, Jørgensen T, Moum T, Johansen S (2011) Characterization of mitochondrial mRNAs in codfish reveals unique features compared to mammals. Curr Genet 57:213–222

    Article  PubMed  CAS  Google Scholar 

  • Crease TJ (1999) The complete sequence of the mitochondrial genome of Daphnia pulex (Cladocera: Crustacea). Gene 233:88–99

    Article  Google Scholar 

  • Crozier RH, Crozier YC (1993) The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization. Genetics 133:97–117

    PubMed  CAS  Google Scholar 

  • Curole JP, Kocher TD (1999) Mitogenomics: digging deeper with complete mitochondrial genomes. Trends Ecol Evol 14:394–398

    Article  PubMed  Google Scholar 

  • DeSalle R, Gatesy J, Wheeler W, Grimaldi D (1992) DNA sequences from a fossil termite in Oligo-Miocene amber and their phylogenetic implications. Science 257:1933–1936

    Article  PubMed  CAS  Google Scholar 

  • DjernÆS M, Klass K-D, Picker MD, Damgaard J (2011) Phylogeny of cockroaches (Insecta, Dictyoptera, Blattodea), with placement of aberrant taxa and exploration of out-group sampling. Syst Entomol. doi:10.1111/j.1365-3113.2011.00598.x

  • Dotson EM, Beard CB (2001) Sequence and organization of the mitochondrial genome of the Chagas disease vector, Triatoma dimidiata. Insect Mol Biol 10:205–215

    Article  PubMed  CAS  Google Scholar 

  • Fakoorziba MR, Eghbal F, Hassanzadeh J, Moemenbellah-Fard MD (2010) Cockroaches (Periplaneta americana and Blattella germanica) as potential vectors of the pathogenic bacteria found in nosocomial infections. Ann Trop Med Parasitol 104:521–528

    Article  PubMed  CAS  Google Scholar 

  • Fenn JD, Song H, Cameron SL, Whiting MF (2008) A preliminary mitochondrial genome phylogeny of Orthoptera (Insecta) and approaches to maximizing phylogenetic signal found within mitochondrial genome data. Mol Phylogenet Evol 49:59–68

    Article  PubMed  CAS  Google Scholar 

  • Flegontov P, Gray M, Burger G, Lukeš J (2011) Gene fragmentation: a key to mitochondrial genome evolution in Euglenozoa? Curr Genet 57:225–232

    Article  PubMed  CAS  Google Scholar 

  • Garesse R (1988) Drosophila melanogaster mitochondrial DNA: gene organisation and evolutionary consideration. Genetics 118:649–663

    PubMed  CAS  Google Scholar 

  • Gissi C, Iannelli F, Pesole G (2008) Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species. Heredity 101:301–320

    Article  PubMed  CAS  Google Scholar 

  • Goldman N, Yang Z (1994) A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol 11:725–736

    PubMed  CAS  Google Scholar 

  • Gore JC, Schal C (2005) Expression, production and excretion of Bla g 1, a major human allergen, in relation to food intake in the German cockroach, Blattella germanica. Med Vet Entomol 19:127–134

    Article  PubMed  Google Scholar 

  • Grandcolas P (1996) The phylogeny of cockroach families: a cladistic appraisal of morpho-anatomical data. Can J Zool 74:508–527

    Article  Google Scholar 

  • Hennig W (1981) Insect Phylogeny (translated and edited by Pont, AC; revisionary notes by Schlee D, with 9 collaborators). Wiley, New York

  • Hong MY, Jeong HC, Kim MJ, Jeong HU, Lee SH, Kim I (2009) Complete mitogenome sequence of the jewel beetle, Chrysochroa fulgidissima (Coleoptera: Buprestidae). Mitochondrial DNA 20:46–60

    PubMed  CAS  Google Scholar 

  • Inward D, Beccaloni G, Eggleton P (2007) Death of an order: a comprehensive molecular phylogenetic study confirms that termites are eusocial cockroaches. Biol Lett 3:331–335

    Article  PubMed  CAS  Google Scholar 

  • Irles P, Bellés X, Piulachs MD (2009) Identifying genes related to choriogenesis in insect panoistic ovaries by Suppression Subtractive Hybridization. BMC Genomics 10:206

    Article  PubMed  Google Scholar 

  • Jex A, Hu M, Littlewood DT, Waeschenbach A, Gasser R (2008) Using 454 technology for long-PCR based sequencing of the complete mitochondrial genome from single Haemonchus contortus (Nematoda). BMC Genomics 9:11

    Article  PubMed  Google Scholar 

  • Jung P, Friedrich A, Souciet J-L, Louis V, Potier S, de Montigny J, Schacherer J (2010) Complete mitochondrial genome sequence of the yeast Pichia farinosa and comparative analysis of closely related species. Curr Genet 56:507–515

    Article  PubMed  CAS  Google Scholar 

  • Kim I, Cha SY, Yoon MH, Hwang JS, Lee SM, Sohn HD, Jin BR (2005) The complete nucleotide sequence and gene organization of the mitochondrial genome of the oriental mole cricket, Gryllotalpa orientalis (Orthoptera: Gryllotalpidae). Gene 353:155–168

    Article  PubMed  CAS  Google Scholar 

  • Kim B-C, Kang T-W, Kim M-S, Kim C-B (2006) The complete mitogenome of Rhodeus uyekii (Cypriniformes, Cyprinidae). Mitochondrial DNA 17:181–186

    CAS  Google Scholar 

  • Klass KD, Meier R (2006) A phylogenetic analysis of Dictyoptera (Insecta) based on morphological characters. Entomologische Abhandlungen 63:3–50

    Google Scholar 

  • Lee CY, Hemingway J, Yap HH, Chong NL (2000) Biochemical characterization of insecticide resistance in the German cockroach, Blattella germanica, from Malaysia. Med Vet Entomol 14:11–18

    Article  PubMed  CAS  Google Scholar 

  • Lee DK, Lee WJ, Sim JK (2003) Population densities of cockroaches from human dwellings in urban areas in the Republic of Korea. J Vector Ecol 28:90–96

    PubMed  Google Scholar 

  • Lind R (1994) The evolution and subsequent classification of the Phasmatodea. Phasmid Stud 3:1–5

    Google Scholar 

  • Lo N, Tokuda G, Watanabe H, Rose H, Slaytor M, Maekawa K, Bandi C, Noda H (2000) Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches. Curr Biol 10:801–804

    Article  PubMed  CAS  Google Scholar 

  • Lo N, Bandi C, Watanabe H, Nalepa C, Beninati T (2003) Evidence for cocladogenesis between diverse dictyopteran lineages and their intracellular endosymbionts. Mol Biol Evol 20:907–913

    Article  PubMed  CAS  Google Scholar 

  • Lo N, Beninati T, Stone F, Walker J, Sacchi L (2007) Cockroaches that lack Blattabacterium endosymbionts: the phylogenetically divergent genus Nocticola. Biol Lett 3:327–330

    Article  PubMed  CAS  Google Scholar 

  • Lohse M, Drechsel O, Bock R (2007) OrganellarGenomeDRAW (OGDRAW): a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Curr Genet 52:267–274

    Article  PubMed  CAS  Google Scholar 

  • Maekawa K, Matsumoto T (2000) Molecular phylogeny of cockroaches (Blattaria) based on mitochondrial COII gene sequences. Syst Entomol 25:511–519

    Article  Google Scholar 

  • Minegishi Y, Aoyama J, Inoue JG, Miya M, Nishida M, Tsukamoto K (2005) Molecular phylogeny and evolution of the freshwater eels genus Anguilla based on the whole mitochondrial genome sequences. Mol Phylogenet Evol 34:134–146

    Article  PubMed  CAS  Google Scholar 

  • Mukha DV, Kagramanova AS, Lazebnaya IV, Lazebnyi OE, Vargo EL, Schal C (2007) Intraspecific variation and population structure of the German cockroach, Blattella germanica, revealed with RFLP analysis of the non-transcribed spacer region of ribosomal DNA. Med Vet Entomol 21:132–140

    Article  PubMed  CAS  Google Scholar 

  • Nalepa CA, Lenz M (2000) The ootheca of Mastotermes darwiniensis Froggatt (Isoptera: Mastotermitidae): homology with cockroach oothecae. Proc R Soc B Biol Sci 267:1809–1813

    Article  CAS  Google Scholar 

  • Nardi F, Spinsanti G, Boore JL, Carapelli A, Dallai R, Frati F (2003) Hexapod origins: monophyletic or paraphyletic? Science 299:1887–1889

    Article  PubMed  CAS  Google Scholar 

  • Nylander JAA (2004) MrModeltest: program distributed by the author, v2. Evolutionary Biology Centre, Uppsala University, Sweden

    Google Scholar 

  • Okimoto R, Macfarlane JL, Wolstenholme DR (1990) Evidence for the frequent use of TTG as the translation initiation codon of mitochondrial protein genes in the nematodes, Ascaris suum and Caenorhabditis elegans. Nucleic Acids Res 18:6113–6118

    Article  PubMed  CAS  Google Scholar 

  • Oliveira DCSG, Raychoudhury R, Lavrov DV, Werren JH (2008) Rapidly evolving mitochondrial genome and directional selection in mitochondrial genes in the parasitic wasp Nasonia (Hymenoptera: Pteromalidae). Mol Biol Evol 25:2167–2180

    Article  PubMed  CAS  Google Scholar 

  • Pantou M, Kouvelis V, Typas M (2006) The complete mitochondrial genome of the vascular wilt fungus Verticillium dahliae: a novel gene order for Verticillium and a diagnostic tool for species identification. Curr Genet 50:125–136

    Article  PubMed  CAS  Google Scholar 

  • Piłsyk S, Paszewski A (2009) The Aspergillus nidulans pigP gene encodes a subunit of GPI-N-acetylglucosaminyltransferase which influences filamentation and protein secretion. Curr Genet 55:301–309

    Article  PubMed  Google Scholar 

  • Plazzi F, Ricci A, Passamonti M (2011) The mitochondrial genome of Bacillus stick insects (Phasmatodea) and the phylogeny of orthopteroid insects. Mol Phylogenet Evol 58:304–316

    Article  PubMed  CAS  Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Rambaut A, Drummond AJ (2007) Tracer v1.4: MCMC trace analyses tool. http://beastbioedacuk/Tracer

  • Ravin N, Galachyants Y, Mardanov A, Beletsky A, Petrova D, Sherbakova T, Zakharova Y, Likhoshway Y, Skryabin K, Grachev M (2010) Complete sequence of the mitochondrial genome of a diatom alga Synedra acus and comparative analysis of diatom mitochondrial genomes. Curr Genet 56:215–223

    Article  PubMed  CAS  Google Scholar 

  • Ritchie SA, Rapley LP, Williams C, Johnson PH, Larkman M, Silcock RM, Long SA, Russell RC (2009) A lethal ovitrap-based mass trapping scheme for dengue control in Australia: I. Public acceptability and performance of lethal ovitraps. Med Vet Entomol 23:295–302

    Article  PubMed  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Roth LM (2003) Systematics and phylogeny of cockroaches (Dictyoptera: Blattaria). Orient Insects 37:1–186

    Article  Google Scholar 

  • Roth S, Fromm B, Gäde G, Predel R (2009) A proteomic approach for studying insect phylogeny: CAPA peptides of ancient insect taxa (Dictyoptera, Blattoptera) as a test case. BMC Evol Biol 9:1–12

    Article  Google Scholar 

  • Secq M-P, Goër S, Stam W, Olsen J (2006) Complete mitochondrial genomes of the three brown algae (Heterokonta: Phaeophyceae) Dictyota dichotoma, Fucus vesiculosus and Desmarestia viridis. Curr Genet 49:47–58

    Article  Google Scholar 

  • Shao R, Campbell NJH, Barker SC (2001) Numerous gene rearrangements in the mitochondrial genome of the wallaby louse, Heterodoxus macropus (Phthriptera). Mol Biol Evol 18:858–865

    Article  PubMed  CAS  Google Scholar 

  • Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Rook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87:1–51

    Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed  CAS  Google Scholar 

  • Terry MD, Whiting MF (2005) Mantophasmatodea and phylogeny of the lower neopterous insects. Cladistics 21:240–257

    Article  Google Scholar 

  • Velez A, Wolff M, Gutierrez E (2006) Blattaria of Colombia: list and distribution of genera. Zootaxa 1210:39–52

    Google Scholar 

  • Xu YL, He P, Zhang L, Fang SQ, Dong SL, Zhang YJ, Li F (2009) Large-scale identification of odorant-binding proteins and chemosensory proteins from expressed sequence tags in insects. BMC Genomics 10:632

    Article  PubMed  Google Scholar 

  • Yamauchi MM, Miyaf MU, Nishida M (2004) Use of a PCR-based approach for sequencing whole mitochondrial genomes of insects: two examples (cockroach and dragonfly) based on the method developed for decapod crustaceans. Insect Mol Biol 13:435–442

    Article  PubMed  CAS  Google Scholar 

  • Yoon C, Kang S, Yang J-O, Noh D-J, Indiragandhi P, Kim G-H (2009) Repellent activity of citrus oils against the cockroaches Blattella germanica, Periplaneta americana and P. fuliginosa. J Pestic Sci 34:77–88

    Article  CAS  Google Scholar 

  • Zhang DX, Hewitt GM (1997) Insect mitochondrial control region: a review of its structure, evolution and usefulness in evolutionary studies. Biochem Syst Ecol 25:99–120

    Article  Google Scholar 

  • Zhang Y, Xuan W, Zhao J, Zhu C, Jiang G (2010) The complete mitochondrial genome of the cockroach Eupolyphaga sinensis (Blattaria: Polyphagidae) and the phylogenetic relationships within the Dictyoptera. Mol Biol Rep 37:3509–3516

    Article  PubMed  CAS  Google Scholar 

  • Zhou Z, Huang Y, Shi F (2007) The mitochondrial genome of Ruspolia dubia (Orthoptera: Conocephalidae) contains a short A + T-rich region of 70 bp in length. Genome 50:855–866

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Gang Liu for his assistance in PCR amplification. We also thank four anonymous reviewers for their insightful comments and suggestions. The study is supported by the grants from the Natural Science Foundation of China (Nos. 30670257 and 30770307) and the National Basic Research Program of China (2007CB411604).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Guo-Fang Jiang.

Additional information

Communicated by L. Tomaska.

B. Xiao and A.-H. Chen contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 1070 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Xiao, B., Chen, AH., Zhang, YY. et al. Complete mitochondrial genomes of two cockroaches, Blattella germanica and Periplaneta americana, and the phylogenetic position of termites. Curr Genet 58, 65–77 (2012). https://doi.org/10.1007/s00294-012-0365-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-012-0365-7

Keywords

Navigation