Skip to main content
SpringerLink
Log in

The sequence, organization, and evolution of the Locusta migratoria mitochondrial genome

  • Articles
  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

The sequencing of the cloned Locusta migratoria mitochondrial genome has been completed. The sequence is 15,722 by in length and contains 75.3% A+T, the lowest value in any of the five insect mitochondrial sequences so far determined. The protein coding genes have a similar A+T content (74.1%) but are distinguished by a high cytosine content at the third codon position. The gene content and organization are the same as in Drosophila yakuba except for a rearrangement of the two tRNA genes tRNAlys and tRNAasp. The A+T-rich region has a lower A+T nucleotide content than in other insects, and this is largely due to the presence of two G+C-rich 155-bp repetitive sequences at the 5′ end of this section and the beginning of the adjacent small rRNA gene. The sizes of the large and small rRNA genes are 1,314 and 827 bp, respectively, and both sequences can be folded to form secondary structures similar to those previously predicted for Drosophila. The tRNA genes have also been modeled and these show a strong resemblance to the dipteran tRNAs, all anticodons apparently being conserved between the two species. A comparison of the protein coding nucleotide sequences of the locust DNA with the homologous sequences of five other arthropods (Drosophila yakuba, Anopheles quadrimaculatus, Anopheles gambiae, Apis mellifera, and Artemia franciscana) was performed. The amino acid composition of the encoded proteins in Locusta is similar to that of Drosophila, with a Dayhoff distance twice that of the distance between the fruit fly and the mosquitoes. A phylogenetic analysis revealed the locust genes to be more similar to those of the Dipterans than to those of the honeybee at both the nucleotide and amino acid levels. A comparative analysis of tRNA orders, using crustacean mtDNAs as outgroups, supported this. This high level of divergence in the Apis genome has been noted elsewhere and is possibly an effect of directional mutation pressure having resulted in an accelerated pattern of sequence evolution. If the general assumption that the Holometabola are monophyletic holds, then these results emphasize the difficulties of reconstructing phylogenies that include lineages with variable substitution rates and base composition biases. The need to exercise caution in using information about tRNA gene orders in phylogenetic analysis is also illustrated. However, if the honeybee sequence is excluded, the correspondence between the other five arthropod sequences supports the findings of previous studies which have endorsed the use of mtDNA sequences for studies of phylogeny at deep levels of taxonomy when mutation rates are equivalent.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

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

    CAS  PubMed  Google Scholar 

  • Anderson S, de Bruijn MHL, Coulson AR, Eperon IC, Sanger F, Young IG (1982) The complete sequence of the bovine mitochondrial DNA: conserved features of the mammalian mitochondrial genome. J Mol Biol 156:683–717

    Google Scholar 

  • Aquadro CF, Kaplan N, Risko KJ (1984) An analysis of the dynamics of mammalian mitochondrial DNA sequence evolution. Mol Biol Evol 1:423–434

    Google Scholar 

  • Asakawa S, Kumazawa Y, Araki T, Himeno H, Miura K, Watanabe K (1991) Strand-specific nucleotide composition bias in Echinoderm and vertebrate mitochondrial genomes. J Mol Evol 32:511–520

    Google Scholar 

  • Avise JC (1994) Molecular markers, natural history and evolution. Chapman and Hall, New York

    Google Scholar 

  • Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18:489–522

    Google Scholar 

  • Baker CS, Perry A, Bannister J, Weinrich M, Abernethy R, Calambolcidis J, Lien J, Lambertsen R, Urbàn Ramirez J, Vasquez O, Clapham P, Alling A, O'Brien S, Palumbi SR (1993) Abundant mitochondrial DNA variation and world-wide population structure in humpback whales. Proc Natl Acad Sci USA 90:8239–8243

    Google Scholar 

  • Ballard JWO, Olsen GJ, Faith DP, Odgers WA, Rowell DM, Atkinson PW (1992) Evidence from 12s ribosomal RNA sequences that onychophorans are modified arthropods. Science 258:1345–1348

    CAS  PubMed  Google Scholar 

  • Beard CB, Mills Hamm D, Collins FH (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

    Google Scholar 

  • Beckenbach AT, Wei YW, Liu H (1993) Relationships in the Drosophila obscura species group, inferred from mitochondrial cytochrome oxidase II sequences. Mol Biol Evol 10:619–634

    Google Scholar 

  • Bibb MJ, van Etten RA, Wright CT, Walberg MW, Clayton DA (1981) Sequence and gene organisation of mouse mitochondrial genome. Cell 26:167–180

    Google Scholar 

  • Birley AJ, Croft JH (1992) Mitochondrial DNAs and phylogenetic relationships. In: Dutta SK (ed) DNA systematics. CRC Press, Boca Raton, pp 107–137

    Google Scholar 

  • Boyce TM, Zwick ME, Aquadro CF (1994) Mitochondrial DNA in the bark weevils: phylogeny and evolution in the Pissodes strobi species group (Coleoptera: Curculionidae). Mol Biol Evol 11:183–194

    Google Scholar 

  • Carpenter FM, Burnham L (1985) The geological record of insects. Annu Rev Earth Planet Sci 13:297–314

    Google Scholar 

  • Clary DO, Wahleithner JA, Wolstenholme DR (1983) Transfer RNA genes in Drosophila mitochondrial DNA: related 5′ flanking sequences and comparisons to mammalian mitochondrial tRNA genes. Nucleic Acids Res 11:2411–2425

    Google Scholar 

  • Clary DO, Wolstenholme DR (1985a) The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization and genetic code. J Mol Evol 22:252–271

    Google Scholar 

  • Clary DO, Wolstenholme DR (1985b) The ribosomal genes of Drosophila mitochondrial DNA. Nucleic Acids Res 13:4029–4045

    Google Scholar 

  • Clayton DA (1992) Transcription and replication of animal mitochondrila DNAs. Int Rev Cytol 141:217–323

    CAS  PubMed  Google Scholar 

  • Coria R, Zalce ME, Mendoza V, Alvarez G, de Cobos AT, Brunner A (1990) Restriction site variation, length polymorphism and changes in gene order in the mitochondrial DNA of the yeast Kluyveromyces lactis. Ant Van Leeuwen 58:227–234

    Google Scholar 

  • Cornuet J-M, Garnery L, Solignac M (1991) Putative origin and function of the intergenic region between COI and COII of Apis mellifera L. mitochondrial DNA. Generics 128:393–403

    Google Scholar 

  • Crozier RH, Crozier YC (1992) The cytochrome band ATPase genes of honeybee mitochondrial DNA. Mol Biol Evol 9:474–482

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Crozier RH, Crozier YC, Mackinlay AG (1989) The CO-I and CO-II region of honeybee mitochondrial DNA: evidence for variation in insect mitochondrial DNA evolutionary rates. Mol Biol Evol 6: 399–411

    Google Scholar 

  • Dayhoff MO (1979) Atlas of protein structure and function, vol 5, supplement 3, 1978. National Biomedical Research Foundation, Washington, DC

    Google Scholar 

  • DeBruijn MHL (1983) Drosophila melanogaster mitochondrial DNA, a novel organization and genetic code. Nature 304:234–241

    Google Scholar 

  • DeSalle R, Freedman T, Prager EM, Wilson AC (1987) Tempo and mode of sequence evolution in mitochondrial DNA of Hawaiian Drosophila. J Mol Evol 26:157–164

    Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Google Scholar 

  • Felsenstein J (1993) PHYLIP manual, version 3.5. University of Washington, Seattle

    Google Scholar 

  • Fitch WM (1986) The estimate of total nucleotide substitutions from pairwise differences is biased. Philos Trans Roy Soc Lond Biol 312:317–324

    Google Scholar 

  • Gadelata G, Pepe G, Decanadia G, Quagliariello C, Sbisa E, Saccone C (1989) The complete nucleotide sequence of the Rattus norvegicus mitochondrial genome: cryptic signals revealed by comparative analysis between vertebrates. J Mol Evol 28:497–516

    Google Scholar 

  • Gellissen G, Bradfield JFY, White BN, Wyatt OR (1983) Mitochondrial DNA sequences in the nuclear genome of a locust. Nature 301:631–634

    Google Scholar 

  • Gellissen G, Michaelis G (1987) Gene transfer: mitochondria to nucleus. Ann NY Acad Sci 503:391–401

    Google Scholar 

  • Haucke H-R, Gellissen G (1988) Different mitochondrial gene orders among insects: exchanged tRNA gene positions in the COII/COIII region between an orthopteran and a dipteran species. Curr Genet 14:471–476

    Google Scholar 

  • Hedges SB (1992) The number of replications needed for accurate estimation of the bootstrap P value in phylogenetic studies. Mol Biol Evol 9:366–369

    Google Scholar 

  • Henikoff S (1984) Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene 28:351–359

    Google Scholar 

  • Hennig W (1981) Insect phylogeny. Wiley, New York.

    Google Scholar 

  • Higgins DG, Bleasby AJ, Fuchs R (1991) CLUSTAL V: improved software for multiple sequence alignment. CABIOS 8:189–191

    Google Scholar 

  • Higgins DG, Sharp PM (1989) Fast and sensitive multiple sequence alignments on a microcomputer. CABIOS 5:151–153

    Google Scholar 

  • Hinton HE (1958) The phylogeny of panorpoid orders. Annu Rev Entomol 3:181–206

    Google Scholar 

  • Hoeben P, Weiller G, Clark-Walker GD (1993) Larger rearranged mitochondrial genomes in Dekkera/Brettanomyces yeasts are more closely related than similar genomes with a conserved gene order. J Mol Evol 36:263–269

    Google Scholar 

  • Jermiin LS, Crozier RH (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

    Google Scholar 

  • Jermiin LS, Grant D, Lowe RM, Crozier RH (1994) Analysis of directional mutation pressure and nucleotide content in mitochondrial cytochrome B genes. J Mol Evol (in press)

  • Jin L, Nei M (1990) Limitations of the evolutionary parsimony method of phylogenetic analysis. Mol Biol Evol 7:82–102

    Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    CAS  PubMed  Google Scholar 

  • Kocher TD, Thomas WK, Mexer A, Edwards SV, Pääbo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci USA 86:6196–6200

    CAS  PubMed  Google Scholar 

  • Kristensen NP (1991) Phylogeny of extant hexapods. In: Naumann ID, CSIRO (eds) Insects of Australia. Cornell Univ Press, Ithaca, NY, pp 125–140

    Google Scholar 

  • Kumar S, Tamura K, Nei M (1993) MEGA: molecular evolutionary genetics analysis, version 1.01. The Pennsylvania State University, University Park, PA

    Google Scholar 

  • Liu H, Beckenbach AT (1992) Evolution of the mitochondrial cytochrome oxidase II gene among ten orders of insects. Mol Phyl Evol 1:41–52

    CAS  PubMed  Google Scholar 

  • Loomis WE, Smith DW (1990) Molecular phylogeny of Dictyostelium discoideum by protein sequence comparison. Proc Natl Acad Sci USA 87:9093–9097

    Google Scholar 

  • Lynch M, Jarrell PE (1993) A method for calibrating molecular clocks and its application to animal mitochondrial DNA. Genetics 135: 1197–1208

    Google Scholar 

  • Maddison WP, Maddison DR (1992) MacClade: analysis of phylogeny and character evolution, version 3.0. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Martin AP, Naylor GJP, Palumbi SR (1992) Rates of mitochondrial DNA evolution in sharks are slow compared with mammals. Nature 357:153–155

    Google Scholar 

  • McCracken A, Uhlenbusch I, Gellissen G (1987) Structure of the cloned Locusta migratoria mitochondrial genome: restriction mapping and sequence of its ND-1 gene. Curr Genet 11:625–630

    Google Scholar 

  • Mitchell SE, Cockburn AF, Seawright JA (1993) The mitochondrial genome of Anopheles quadrimaculatus species A: complete nucleotide sequence and gene organization. Genome 36:1058–1073

    CAS  PubMed  Google Scholar 

  • Miyata T, Hayashida H, Kikuno R, Hasegawa M, Kobayashi M, Koike K (1982) Molecular clock of silent substitutions: At least six fold preponderance of silent substitutions in mitochondrial genes over those in nuclear genes. J Mot Evol 19:28–35

    Google Scholar 

  • Miyamoto MM, Kraus F, Ryder OA (1990) Phylogeny and evolution of antlered deer determined from mitochondrial DNA sequences. Proc Natl Acad Sci USA 87:6127–6131

    Google Scholar 

  • Moritz C (1991) The origin and evolution of parthenogenesis in Heteronotia binoei (Gekkonidae): evidence for recent and localized origin of widespread clones. Genetics 129:221–230

    Google Scholar 

  • Moritz C, Brown WM (1986) Tandem duplications of D-loop and ribosomal RNA sequences in lizard mitochondrial DNA. Science 233:1425–1527

    CAS  PubMed  Google Scholar 

  • Moritz C, Brown WM (1987) Tandem duplications in animal mitochondrial DNAs: variation in incidence and gene content among lizards. Proc Natl Acad Sci USA 84:7183–7187

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Okimoto R, Chamberlin HM, MacFarlane JL, Wolstenholme DR (1991) Repeated sequence sets in mitochondrial DNA molecules of root knot nematodes (Meloidogyne): nucleotide sequences, genome location and potential for host-race identification. Nucleic Acids Res 19:1619–1626

    CAS  PubMed  Google Scholar 

  • Okimoto R, MacFarlane JL, Clary DO, Wolstenholme DR (1992) The mitochondrial genomes of two nematodes, Caenorhabditis elegans and Ascaris suum. Genetics 130:471–498

    CAS  PubMed  Google Scholar 

  • Parker SP (1982) Synopsis and classification of living organisms. McGraw-Hill, New York

    Google Scholar 

  • Pashley DP, McPheron BA, Zimmer EA (1993) Systematics of holometabolous insect orders based on 18S ribosomal RNA. Mol Phyl Evol 2:132–142

    PubMed  Google Scholar 

  • Pelandakis M, Solignac M (1993) Molecular phylogeny of Drosophila based on ribosomal RNA sequences. J Mol Evol 37:525–543

    Google Scholar 

  • Perez ML, Valverde JR, Batuecas B, Amat F, Marco R, Garesse R (1994) Speciation of the Artemia genus: mitochondrial DNA analysis of bisexual and parthenogenetic brine shrimps. J Mol Evol 38:156–168

    CAS  PubMed  Google Scholar 

  • Pustell J, Kafatos FC (1982) A high speed, high capacity homology matrix: zooming through SV40 and polyoma. Nucleic Acids Res 10:4765–4782

    Google Scholar 

  • Rand DM (1993) Endotherms, ectotherms, and mitochondrial genome size variation. J Mol Evol 37:281–295

    Google Scholar 

  • Rand DM (1994) Thermal habit, metabolic rate and the evolution of mitochondrial DNA. TREE 9:125–131

    Google Scholar 

  • Rand DM, Harrison RG (1989) Molecular population genetics of mtDNA size variation in crickets. Genetics 121:551–569

    Google Scholar 

  • Reiche L, Fairmaire L (1849) Orthoptera. In: Ferret A, Gallinier D (eds) Voyage en Abyssinie. Charpentier, Paris, vol 3, p 430

    Google Scholar 

  • Rippe RM, Gellissen G (1994) The genes for cytochrome b, ND 4L, ND6 and two tRNAs from the mitochondrial genome of the locust, Locusta migratoria. Curr Genet 25:135–141

    Google Scholar 

  • Ruvolo M, Zehr S, von Dornum M, Pan D, Chang B, Lin J (1993) Mitochondrial DNA sequences and modern human origins. Mol Biol Evol 10:1115–1135

    Google Scholar 

  • Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mot Biol Evol 4:406–425

    Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467

    CAS  PubMed  Google Scholar 

  • Sankoff D, Leduc G, Antoine N, Paquin B, Lang BF, Cedegren R (1992) Gene order comparisons for phylogenetic inference: Evolution of the mitochondrial genome. Proc Natl Acad Sci USA 89: 6575–6579

    Google Scholar 

  • Seutin G, Lang BF, Mindell DP, Morais R (1994) Evolution of the WANCY region in amniote mitochondrial DNA. Mol Biol Evol 11:329–340

    Google Scholar 

  • Sharp PM, Tuohy TMF, Mosurski KR (1986) Codon usage in yeast: cluster analysis differentiates highly and lowly expressed genes. Nucleic Acids Res 14:5125–5143

    Google Scholar 

  • Simon C (1991) Molecular systematics at the species boundary: Exploiting conserved and variable regions of the mitochondrial genome of animals via direct sequencing from amplified DNA. In: Hewitt GM, Johnston AWB, Young JPW (eds) Molecular techniques in taxonomy. NATO ASI series, Springer-Verlag, Berlin, pp 33–71

    Google Scholar 

  • Skelly PJ, Hardy CM, Clark-Walker GD (1991) A mobile group II intron of a naturally occurring rearranged mitochondrial genome in Kluyveromyces lactis. Curr Genet 20:115–120

    Google Scholar 

  • Smith MJ, Arndt A, Gorski S, Fajber E (1993) The phylogeny of Echinoderm classes based on mitochondrial gene arrangements. J Mol Evol 36:545–554

    CAS  PubMed  Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry, 2nd ed. WH Freeman, New York

    Google Scholar 

  • Steel MA, Lockhart PJ, Penny D (1993) Confidence in evolutionary trees from biological sequence data. Nature 364:440–442

    Google Scholar 

  • Swofford DL (1993) PAUP: phylogenetic analysis using parsimony, version 3.1.1. Illinois Natural History Survey, Champaign, IL

    Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of the mitochondrial DNA of chimps and humans. Mol Biol Evol 10:512–526

    CAS  PubMed  Google Scholar 

  • Taylor MFJ, McKechnie SW, Pierce N, Kreitman M (1993) The Lepidopteran mitochondrial control region: structure and evolution. Mol Biol Evol 10:1259–1272

    Google Scholar 

  • Uhlenbusch I, McCracken A, Gellissen G (1987) The gene for the large (16S) ribosomal RNA from the Locusta migratoria mitochondrial genome. Curr Genet 11:631–638

    Google Scholar 

  • Van Raay TJ, Crease TJ (1994) Partial mitochondrial DNA sequences of the crustacean Daphnia pulex. Curr Genet 25:66–72

    Google Scholar 

  • Vawter L, Brown WM (1986) Nuclear and mitochondrial comparisons reveal extreme rate variation in the molecular clock. Science 234: 194–196

    Google Scholar 

  • Willis LG, Winston ML, Honda BM (1992) Phylogenetic relationships in the honeybee (genus Apis) as determined by the sequence of the cytochrome oxidase II region of mitochondrial DNA. Mol Phyl Evol 1:169–178

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Wolstenholme DR, Macfarlane JL, Okimoto R, Clary DO, Wahleithner JA (1987) Bizarre tRNAs inferred from DNA sequences of mitochondrial genomes of nematode worms. Proc Natl Acad Sci USA 84:1324–1328

    Google Scholar 

  • Wooton (1981) Palaeozoic insects. Annu Rev Entomol 26:319–344

    Google Scholar 

Download references

Author information

Author notes

  1. G. Gellissen

    Present address: Rhein Biotech GmbH, Eichsfelderstrasse 11, 40595, Düsseldorf, Germany

Authors and Affiliations

  1. Zoologisches Institut, Universität Basel, Rheinsprung 9, 4051, Basel CH, Switzerland

    P. K. Flook & C. H. F. Rowell

  2. Institut für Zoologie III, Universität Düsseldorf, 40225, Düsseldorf, Germany

    G. Gellissen

Authors
  1. P. K. Flook
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. H. F. Rowell
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. G. Gellissen
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Correspondence to: P.K. Flook

Rights and permissions

Reprints and permissions

About this article

Cite this article

Flook, P.K., Rowell, C.H.F. & Gellissen, G. The sequence, organization, and evolution of the Locusta migratoria mitochondrial genome. J Mol Evol 41, 928–941 (1995). https://doi.org/10.1007/BF00173173

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00173173

Key words

Search

Navigation