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Polymorphism of canonical and noncanonical gypsy sequences in different species of Drosophila melanogaster subgroup: possible evolutionary relations

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Abstract

Mobile genetic elements constitute a substantial part of eukaryotic genome and play an important role in its organization and functioning. Co-evolution of retrotransposons and their hosts resulted in the establishment of control systems employing mechanisms of RNA interference that seem to be impossible to evade. However, “active” copies of endogenous retrovirus gypsy escape cellular control in some cases, while its evolutionary elder “inactive” variants do not. To clarify the evolutionary relationship between “active” and “inactive” gypsy we combined two approaches: the analysis of gypsy sequences, isolated from G32 Drosophila melanogaster strain and from different Drosophila species of the melanogaster subgroup, as well as the study of databases, available on the Internet. No signs of “intermediate” (between “active” and “inactive”) gypsy form were found in GenBank, and four full-size G32 gypsy copies demonstrated a convergence that presumably involves gene conversion. No “active” gypsy were revealed among PCR generated gypsy ORF3 sequences from the various Drosophila species indicating that “active” gypsy appeared in some population of D. melanogaster and then started to spread out. Analysis of sequences flanking gypsy variants in G32 revealed their predominantly heterochromatic location. Discrepancy between the structure of actual gypsy sites in G32 and corresponding sequences in database might indicate significant inter-strain heterochromatin diversity.

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References

  • Alberola TM, de Frutos R (1996) Molecular structure of a Gypsy element of Drosophila subobscura (GypsyDs) constituting a degenerate form of insect retroviruses. Nucleic Acids Res 24:914–923

    Article  PubMed  CAS  Google Scholar 

  • Bergman CM, Quesneville H, Anxolabehere D, Ashburner M (2006) Recurrent insertion and duplication generate networks of transposable element sequences in the Drosophila melanogaster genome. Genome Biol 7:R112

    Article  PubMed  Google Scholar 

  • Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, Hannon GJ (2007) Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128:1089–1103

    Article  PubMed  CAS  Google Scholar 

  • Dorsett D, Viglianti GA, Rutledge BJ, Meselson M (1989) Alteration of hsp82 gene expression by the gypsy transposon and suppressor genes in Drosophila melanogaster. Genes Dev 3:454–468

    Article  PubMed  CAS  Google Scholar 

  • Flavell AJ, Alphey LS, Ross SJ, Leigh-Brown AJ (1990) Complete reversions of a gypsy retrotransposon-induced cut locus mutation in Drosophila melanogaster involving jockey transposon insertions and flanking gypsy sequence deletions. Mol Gen Genet 220:181–185

    Article  PubMed  CAS  Google Scholar 

  • Freund R, Meselson M (1984) Long terminal repeat nucleotide sequence and specific insertion of the gypsy transposon. Proc Natl Acad Sci USA 81:4462–4464

    Article  PubMed  CAS  Google Scholar 

  • Hoover KK, Chien AJ, Corces VG (1993) Effects of transposable elements on the expression of the forked gene of Drosophila melanogaster. Genetics 135:507–526

    PubMed  CAS  Google Scholar 

  • Jensen S, Gassama MP, Heidmann T (1999) Taming of transposable elements by homology-dependent gene silencing. Nat Genet 21:209–212

    Article  PubMed  CAS  Google Scholar 

  • Kim AI, Terzian C, Santamaria P, Pelisson A, Prud’homme N, Bucheton A (1994) Retroviruses in invertebrates: the gypsy retrotransposon is apparently an infectious retrovirus of Drosophila melanogaster. Proc Natl Acad Sci USA 91:1285–1289

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kotnova AP, Karpova NN, Feoktistova MA, Lyubomirskaia NV, Kim AI, Ilyin YV (2005) Retrotransposon gtwin: structural analysis and distribution in Drosophila melanogaster strains. Genetika 41:23–29 (Russian)

    PubMed  CAS  Google Scholar 

  • Kotnova AP, Glukhov IA, Karpova NN, Salenko VB, Lyubomirskaya NV, Ilyin YV (2007) Evidence for recent horizontal transfer of gypsy-homologous LTR-retrotransposon gtwin into Drosophila erecta followed by its amplification with multiple aberrations. Gene 396:39–45

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Lachaise DL, Cariou M-L, David JR, Lemeunier F, Ashburner M (1988) Historical biogeography of the D. melanogaster species subgroup. Evol Biol 22:159–226

    Google Scholar 

  • Lyubomirskaya NV, Arkhipova IR, Ilyin YV, Kim AI (1990) Molecular analysis of retrotransposon gypsy from two strains of Drosophila melanogaster differing in genetic instability. Mol Gen Genet 223:305–309

    Article  PubMed  CAS  Google Scholar 

  • Lyubomirskaya NV, Avedisov SN, Surkov SA, Ilyin YV (1993) Two Drosophila retrotransposon gypsy subfamilies differ in ability to produce new DNA copies via reverse transcription in Drosophila cultured cells. Nucleic Acids Res 21:3265–3268

    Article  PubMed  CAS  Google Scholar 

  • Lyubomirskaya NV, Smirnova JB, Razorenova OV, Karpova NN, Surkov SA, Avedisov SN, Kim AI, Ilyin YV (2001) Two variants of the Drosophila melanogaster retrotransposon gypsy (mdg4): structural and functional differences, and distribution in fly stocks. Mol Genet Genomics 265:367–374

    Article  PubMed  CAS  Google Scholar 

  • Marlor RL, Parkhurst SM, Corces VG (1986) The Drosophila melanogaster gypsy transposable element encodes putative gene products homologous to retroviral proteins. Mol Cell Biol 6:1129–1134

    PubMed  CAS  Google Scholar 

  • Mejlumian L, Pelisson A, Bucheton A, Terzian C (2002) Comparative and functional studies of Drosophila species invasion by the gypsy endogenous retrovirus. Genetics 160:201–209

    PubMed  CAS  Google Scholar 

  • Mizrokhi LJ, Mazo AM (1991) Cloning and analysis of the mobile element Gypsy from D. virilis. Nucleic Acids Res 19:913–916

    Article  PubMed  CAS  Google Scholar 

  • Pelisson A, Payen-Groschene G, Terzian C, Bucheton A (2007) Restrictive flamenco alleles are maintained in Drosophila melanogaster population cages, despite the absence of their endogenous gypsy retroviral targets. Mol Biol Evol 24:498–504

    Article  PubMed  CAS  Google Scholar 

  • Pimpinelli S, Berloco M, Fanti L, Dimitri P, Bonaccorsi S, Marchetti E, Caizzi R, Caggese C, Gatti M (1995) Transposable elements are stable structural components of Drosophila melanogaster heterochromatin. Proc Natl Acad Sci USA 92:3804–3808

    Article  PubMed  CAS  Google Scholar 

  • Prud’homme N, Gans M, Terzian C, Bucheton A (1995) Flamenco, a gene controlling the gypsy retrovirus of Drosophila melanogaster. Genetics 139:697–711

    PubMed  CAS  Google Scholar 

  • Ramos E, Ghosh D, Baxter E, Corces VG (2006) Genomic organization of gypsy chromatin insulators in Drosophila melanogaster. Genetics 172:2337–2349

    Article  PubMed  CAS  Google Scholar 

  • Razorenova OV, Karpova NN, Smirnova JB, Kusulidu LK, Reneva NK, Subocheva EA, Kim AI, Lyubomirskaia NV, Ilyin YV (2001) Interlineage distribution and characteristics of the structure of two subfamilies of Drosophila melanogaster MDG4 (gypsy) retrotransposon. Genetika 37:175–182 (Russian)

    PubMed  CAS  Google Scholar 

  • Robert V, Prud’homme N, Kim A, Bucheton A, Pelisson A (2001) Characterization of the flamenco region of the Drosophila melanogaster genome. Genetics 158:701–713

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Smith PA, Corces VG (1992) The suppressor of Hairy-wing binding region is required for gypsy mutagenesis. Mol Gen Genet 233:65–70

    Article  PubMed  CAS  Google Scholar 

  • Stefanov YE, Kotnova AP, Pasyukova EG, Lyubomirskaya NV, Kim AI, Il’in YV (2007) Retrotransposon gtwin in the Drosophila melanogaster laboratory strain G-32: an increased number of copies of this element in the genome caused chromosomal aberration. Dokl Biochem Biophys 413:76–78

    Article  PubMed  CAS  Google Scholar 

  • Terrinoni A, Franco CD, Dimitri P, Junakovic N (1997) Intragenomic distribution and stability of transposable elements in euchromatin and heterochromatin of Drosophila melanogaster: non-LTR retrotransposon. J Mol Evol 45:145–153

    Article  PubMed  CAS  Google Scholar 

  • Terzian C, Ferraz C, Demaille J, Bucheton A (2000) Evolution of the gypsy endogenous retrovirus in the Drosophila melanogaster subgroup. Mol Biol Evol 17:908–914

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Russian Foundation for Basic Research (05-04-49554, 08-04-00227), and “Leading Scientific Schools” (NSh-4216.2006.4) from the Ministry of Education and Science, Russian Federation. We thank A. Kim for his useful opinions and suggestions with this manuscript.

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Authors and Affiliations

  1. V.A. Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, 32 Vavilov street, 119991, Moscow, Russian Federation

    Veniamin B. Salenko, Alina P. Kotnova, Natalia V. Lyubomirskaya & Yuriy V. Ilyin

  2. Neuroscience Center, University of Helsinki, P.O.Box 56 (Viikinkaari 4), 00014, Helsinki, Finland

    Nina N. Karpova

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  1. Veniamin B. Salenko
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  2. Alina P. Kotnova
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  3. Nina N. Karpova
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  4. Natalia V. Lyubomirskaya
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  5. Yuriy V. Ilyin
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Correspondence to Veniamin B. Salenko.

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Communicated by G. Reuter.

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Salenko, V.B., Kotnova, A.P., Karpova, N.N. et al. Polymorphism of canonical and noncanonical gypsy sequences in different species of Drosophila melanogaster subgroup: possible evolutionary relations. Mol Genet Genomics 279, 463–472 (2008). https://doi.org/10.1007/s00438-008-0325-6

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  • DOI: https://doi.org/10.1007/s00438-008-0325-6

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