Skip to main content
SpringerLink
Log in

High transposition rates of Osvaldo, a new Drosophila buzzatii retrotransposon

  • Original Paper
  • Published:
Molecular and General Genetics MGG Aims and scope Submit manuscript

Abstract

Transposition of a new Drosophila retrotransposon was investigated. Total genomic Southern analysis and polytene in situ hybridizations in D. buzzatii strains and other related species using a 6 kb D. buzzatii clone (cDb314) showed a dispersed, repetitive DNA pattern, suggesting that this clone contains a transposable element (TE). We have sequenced the cDb314 clone and demonstrated that it contains all the conserved protein sequences and motifs typical of retrovirus-related sequences. Although cDb314 does not include the complete TE, the protein sequence alignment demonstrates that it includes a defective copy of a new long terminal repeat (LTR) retrotransposon, related to the gypsy family, which we have named Osvaldo. Using a D. buzzatii inbred line in which all insertion sites are known, we have measured Osvaldo transposition rates in hybrids between this D. buzzatii line and its sibling species D. koepferae. The results show that Osvaldo transposes in bursts at high rate, both in the D. buzzatii inbred line and in species hybrids.

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

  • Adams SE, Mellor J, Gull K, Sim RB, Tutte MF, Kingsman SM, Kingsman AJ (1987) The functions and relationships of TyVLP proteins in yeast reflect those of mammalian retroviral proteins. Cell 49:111–119

    Google Scholar 

  • Arkhipova IR, Ilyin YV (1991) Properties of promoter regions of mdg1 Drosophila retrotransposon indicate that it belongs to a specific class of promoters. EMBO J 10:1169–1177

    Google Scholar 

  • Arkhipova IR, Ilyin YV (1992) Control of transcription of Drosophila retrotransposons. BioEssays 14:161–168

    Google Scholar 

  • Biémont CA, Aouar A, Arnault C (1987) Genome reshuffling of the copia element in an inbred line of Drosophila melanogaster. Nature 329:742–744

    Google Scholar 

  • Blackman RK, Gelbart WM (1989) The transposable element hobo of Drosophila melanogaster. In: Berg DE, Howe MM (eds) Mobile DNA. American Society for Microbiology, Washington DC, pp 523–529

    Google Scholar 

  • Brookfield JFY, Montgomery E, Langley CH (1984) Apparent absence of transposable elements related to the P elements of Drosophila melanogaster in other species of Drosophila. Nature 310:330–332

    Google Scholar 

  • Charlesworth B, Langley CH (1989) The population genetics of Drosophila transposable elements. Annu Rev Genet 23:251–287

    Google Scholar 

  • Clare J, Farabaugh P (1985) Nucleotide sequence of a yeast Ty element: evidence for an unusual mechanism of gene expression. Proc Natl Acad Sci USA 82:2829–2833

    Google Scholar 

  • Covey SN (1986) Amino acid sequence homology in gag region of reverse transcribing elements and the coat protein gene of cauliflower mosaic virus. Nucleic Acids Res 14:623–633

    Google Scholar 

  • Coyne JA (1989) Mutation rates in hybrids between sibling species of Drosophila. Heredity 63:155–162

    Google Scholar 

  • Di Franco C, Pisano C, Dimitri P, Gigliotti S, Junakovic N (1989) Genomic distribution of copia like transposable elements in somatic tissues and during development of Drosophila melanogaster. Chromosoma 98:402–410

    Google Scholar 

  • Doolittle RF, Feng DF, Johnson MS, McClure MA (1989) Origin and evolutionary relationships of retroviruses Q Rev Biol 64:1–30

    Google Scholar 

  • Dowsett AP, Young MW (1982) Different levels of dispersed middle repetitive DNA along closely related species of Drosophila. Proc Natl Acad Sci USA 79:4570–4574

    Google Scholar 

  • Eggleston WB, Johnson-Schlitz DM, Engels WR (1988) P-M hybrid dysgenesis does not mobilize other transposable element families in Drosophila melanogaster. Nature 331:368–70

    Google Scholar 

  • Engels WR (1989) P elements in Drosophila melanogaster. In: Berg DE, Howe MM (eds) Mobile DNA. American Society for Microbiology, Washington DC, pp 437–484

    Google Scholar 

  • Engels WR, Preston CR, Thompson P, Eggleston WB (1986) In situ hybridization of Drosophila salivary chromosomes with biotinylated DNA probes and alkaline phosphatase Focus 8:6–8

    Google Scholar 

  • Evgen'ev NB, Yenikolopov GN, Peunova NJ, Ilyin YV (1982) Transposition of mobile genetic elements in interspecific hybrids of Drosophila. Chromosoma 85:375–386

    Google Scholar 

  • Finnegan DJ (1989) The I factor and I-R hybrid dysgenesis in Drosophila melanogaster. In: Berg DE, Howe MM (eds) Mobile DNA. American Society for Microbiology, Washington DC, pp 503–518

    Google Scholar 

  • Fontdevila A (1987) The unstable genome: an evolutionary approach. Genet Iber 39:315–349

    Google Scholar 

  • Fontdevila A (1988) The evolutionary potential of the unstable genome. In: de Jong G (ed) Population genetics and evolution. Springer, Berlin, Heidelberg, pp 251–263

    Google Scholar 

  • Fontdevila A, Pla C, Hasson E, Wasserman M, Sanchez A, Naveira H, Ruiz A (1988) Drosophila koepferae: a new member of the Drosophila serido (Diptera: Drosophilidae) superspecies taxon. Ann Entomol Soc Am 81:380–385

    Google Scholar 

  • Friesen PD, Nissen MS (1990) Gene organization and transcription of TED, a lepidopteran retrotransposon integrated within the baculovirus genome. Mol Cell Biol 10:3067–3077

    Google Scholar 

  • de Frutos R, Kimura K, Peterson KR (1989) In situ hybridization of Drosophila polytene chromosomes with digoxigenin-dUTP labeled probes. Trends Genet 5:366

    Google Scholar 

  • Georgiev PG, Tchurikov NA, Ilyin YV, Georgieva SG, Mizrokhi LJ, Priimaagi AE, Gerasimova TI, Georgiev PG, Simonova OB, Kiselev SL, Kochieva EZ (1989) Mobile genetic elements in Drosophila melanogaster (recent experiments) Genome 31:920–928

    Google Scholar 

  • Georgiev PG, Kiselev SL, Simonova OB, Gerasimova TI (1990) A novel transposition system in Drosophila melanogaster depending on the Stalker mobile genetic element. EMBO J 9:2037–2044

    Google Scholar 

  • Gerasimova TI, Mizrokhi LJ, Georgiev GP (1984) Transposition bursts in genetically unstable Drosophila melanogaster. Nature 309:714–716

    Google Scholar 

  • Gerasimova TI, Matjunina LV, Mizrokhi LJ, Georgiev GP (1985) Successive transposition explosions in Drosophila melanogaster and reverse transpositions of mobile dispersed genetic elements. EMBO J 4:3773–3779

    Google Scholar 

  • Gerstel DU, Burns JA (1967) Phenotypic and chromosomal abnormalities asociated with the introduction of heterochromatin from Nicotiana otophora into N. tabacum. Genetics 56:483–502

    Google Scholar 

  • Hagele K (1984) Different hybrid effects in reciprocal crosses between Chironomus thummi thummi and Ch. th. piger including spontaneous chromosome aberrations and sterility. Genetica 63:105–111

    Google Scholar 

  • Harada K, Yukuhiro K, Mukai T (1990) Transposition rates of movable genetic elements in Drosophila melanogaster. Proc Natl Acad Sci USA 87:3248–3252

    Google Scholar 

  • Haymer DS, Marsh JL (1986) Germ line and somatic instability of a white mutation in Drosophila mauritiana due to a transposable genetic element. Dev Genet 6:281–291

    Google Scholar 

  • Hey J (1989) Speciation via hybrid dysgenesis: negative evidence from the Drosophila affinis subgroup. Genetica 78:97–104

    Google Scholar 

  • Higgins DG, Bleasby AJ, Fuchs R (1992) CLUSTAL V: improved software for multiple sequence alignment Cabios 8:189–191

    Google Scholar 

  • Hirsh VM, Olmsted RA, Murphey-Corb M, Purcell RH, Johnson PR (1989) An African primate lentivirus (SIVsm) closely related to HIV-2. Nature 339:389–392

    Google Scholar 

  • Khan E, Mack JPG, Katz RA, Kulkosky J, Skalka AM (1990) Retroviral integrase domains: DNA binding and the recognition of LTR sequences. Nucleic Acids Res 19:851–860

    Google Scholar 

  • Kim AI, Belyaeva ES, Aslaniam MM (1990) Autonomous transposition of gypsy mobile elements and genetic instability in Drosophila melanogaster. Mol Gen Genet 224:303–308

    Google Scholar 

  • Labrador M, Naveira H, Fontdevila A (1990) Genetic mapping of the Adh locus in the repleta group of Drosophila by in situ hybridization. J Hered 81:83–86

    Google Scholar 

  • Lankenau D-H, Huijser P, Jansen E, Miedema K, Hennig W (1988) Micropia: a retrotransposon of Drosophila combining structural features of DNA viruses, retroviruses and non-viral transposable elements. J Mol Biol 204:233–246

    Google Scholar 

  • Leigh-Brown AJ, Ross SJ, Alphey LS, Flavell AJ, Gerasimova TI (1989) Instability in the ct MRZ strain of Drosophila melanogaster: role of P element functions and structure of revertants. Mol Gen Genet 218:208–213

    Google Scholar 

  • Lozovskaya ER, Scheinker VSH, Evgen'ev MB (1990) A hybrid dysgenesis syndrome in Drosophila virilis. Genetics 126:619–623

    Google Scholar 

  • Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York

    Google Scholar 

  • Martin G, Wiernasz D, Schedl P (1983) Evolution of Drosophila repetitive-dispersed DNA. J Mol Evol 19:203–213

    Google Scholar 

  • McClintock B (1951) Chromosome organization and genic expression. Cold Spring Harbor Symp Quant Biol 16:13–47

    Google Scholar 

  • McClure MA (1991) Evolution of retroposons by acquisition or deletion of retrovirus-like genes. Mol Biol Evol 8:835–856

    Google Scholar 

  • McClure MA (1992) Sequence analysis of eukaryotic retroid proteins. Math computer modeling 16:121–136

    Google Scholar 

  • Michaille J-J, Mathavan S, Gaillard J, Garel A (1990) The complete sequence of mag a new retrotransposon in Bombyx mori. Nucleic Acids Res 18:674

    Google Scholar 

  • Miller DD (1950) Observations on two cases of interspecific hybridization with Drosophila athabasca. Am Nat 84:81–93

    Google Scholar 

  • Naveira H, Fontdevila A (1985) The evolutionary history of Drosophila buzzatii. IX. High frequencies of new chromosome rearrangements induced by introgressive hybridization. Chromosoma 91:87–94

    Google Scholar 

  • Naveira H, Fontdevila A (1986) The evolutionary history of Drosophila buzzatii. XII. The genetic basis of sterility in hybrids between D buzzatii and its sibling D serido from Argentina. Genetics 114:841–857

    Google Scholar 

  • Naveira H, Fontdevila A (1991a) The evolutionary history of Drosophila buzzatii. XXII. Chromosomal and genic sterility in male hybrids of Drosophila buzzatii and Drosophila koepferae. Heredity 66:233–239

    Google Scholar 

  • Naveira H, Fontdevila A (1991b) The evolutionary history of Drosophila buzzatii. XXI. Cumulative action of multiple sterility factors on spermatogenesis in hybrids of D buzzatii and D koepferae. Heredity 67:57–72

    Google Scholar 

  • Naveira H, Pla C, Fontdevila A (1986) The evolutionary history of Drosophila buzzatii. XI. A new method for cytogenetic localization based on asynapsis of polytene chromosomes in interspecific hybrids of Drosophila. Genetica 71:199–212

    Google Scholar 

  • Nével-Ninio M, Mariol M-C, Gans M (1989) Mobilization of the gypsy and copia retrotransposons in Drosophila melanogaster induces reversion of the OVOD dominant female-sterile mutations: molecular analysis of revertant alleles. EMBO J 8:1549–1558

    Google Scholar 

  • Parkhurst SM, Corces VG (1987) Developmental expression of Drosophila melanogaster retrovirus like transposable elements. EMBO J 6:419–424

    Google Scholar 

  • Pasyukova EG, Nuzhdin SV (1993) Doe and copia instability in an isogenic Drosophila melanogaster stock. Mol Gen Genet 240:302–306

    Google Scholar 

  • Pasyukova EG, Belyaeva ES, Kogan GL, Kaidanov LZ, Gvozdev VA (1986) Concerted transpositions of mobile genetic elements coupled with fitness changes in Drosophila melanogaster. Mol Biol Evol 3:299–312

    Google Scholar 

  • Piñol J, Francino O, Fontdevila A, Cabre O (1988) Rapid isolation of Drosophila high molecular weight DNA to obtain genomic libraries. Nucleic Acids Res 16:2736–2737

    Google Scholar 

  • Rose MR, Doolittle WF (1983) Molecular biological mechanisms of speciation. Science 220:157–162

    Google Scholar 

  • Sambrook J, Maniatis T, Fritsch EF (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York

    Google Scholar 

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

    Google Scholar 

  • Scheinker VSH, Lozovskaya ER, Bishop JG, Corces VG, Evgen'ev MB (1990) A long terminal repeat-containing retrotransposon is mobilized during hybrid dysgenesis in Drosophila virilis. Proc Natl Acad Sci USA 87:9615–9619

    Google Scholar 

  • Schmidt ER (1984) Clustered and interspersed repetitive DNA sequence family of Chironomus. J Mol Biol 178:1–15

    Google Scholar 

  • Shaw DD, Wilkinson P, Coates DJ (1983) Increased chromosomal mutation rates after hybridization between two subspecies of grasshoppers. Science 220:1165–1167

    Google Scholar 

  • Shevelyov YY, Balakireva MD, Gvozdev VA (1989) Heterochromatic regions in different Drosophila melanogaster stocks contain similar arrangements of moderate repeats with inserted copia-like elements (MDG1). Chromosoma 98:117–122

    Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn. WH Freeman, San Francisco

    Google Scholar 

  • Stacey SN, Lansman RA, Brock H, Grigliatti TA (1986) Distribution and conservation of mobile elements in the genus Drosophila. Mol Biol Evol 3:522–534

    Google Scholar 

  • Sturtevant A H (1939) High mutation frequency induced by hybridization. Proc Natl Acad Sci USA 25:308–310

    Google Scholar 

  • Thompson JN Jr, Woodruff RC (1978) Mutator genes-pacemakers of evolution. Nature 274:317–321

    Google Scholar 

  • Vaury C, Bucheton A, Pelisson A (1989) The heterochromatic sequences flanking the I elements are themselves defective transposable elements. Chromosoma 98:215–224

    Google Scholar 

  • Wasserman M (1982) Evolution of the repleta group. In: Ashburner M, Carson HL, Thompson JN (eds) The genetics and biology of Drosophila, vol 3b. Academic Press, London, pp 62–139

    Google Scholar 

  • Wharton LT (1942) Analysis of the repleta group of Drosophila. Univ Texas Publ 4228:23–53

    Google Scholar 

  • Wilke CM, Maimer E, Adams J (1992) The population biology and evolutionary significance of the Ty elements in Saccaromyces cerevisiae. Genetica 86:155–173

    Google Scholar 

  • Xiong Y, Eickbush TH (1990) Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J 9:3353–3362

    Google Scholar 

  • Youngren SD, Boeke JD, Sanders NJ, Garfinkel DJ (1988) Functional organization of the retrotransposon Ty from Saccharomyces cerevisiae: Ty protease is required for transposition. Mol Cell Biol 8:1421–1431

    Google Scholar 

  • Yuki S, Inouye S, Ishimaru S, Kulkosky J, Skalka M (1986a) Nucleotide sequence characterization of a Drosophila retrotransposon, 412. Eur J Biochem 158:403–410

    Google Scholar 

  • Yuki S, Ishimaru S, Inouye S, Saigo K (1986b) Identification of genes for reverse transcriptase-like enzymes in two Drosophila retrotransposons, 412 and gypsy; a rapid detection method of reverse transcriptase genes using YXDD box probes. Nucleic Acids Res 14:3017–3030

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departament de Genètica i de Microbiologia, Universitat Autònoma de Barcelona, 08193, Bellaterra, Spain

    Mariano Labrador & Antonio Fontdevila

Authors
  1. Mariano Labrador
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Antonio Fontdevila
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

This paper is dedicated posthumously to Osvaldo A. Reig in recognition of his contributions to evolutionary biology and his early appreciation of the role of transposable elements in evolution

Rights and permissions

Reprints and permissions

About this article

Cite this article

Labrador, M., Fontdevila, A. High transposition rates of Osvaldo, a new Drosophila buzzatii retrotransposon. Molec. Gen. Genet. 245, 661–674 (1994). https://doi.org/10.1007/BF00297273

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00297273

Key words

Search

Navigation