Skip to main content
SpringerLink
Log in

Copia Retrotransposon in the Zaprionus Genus: Another Case of Transposable Element Sharing with the Drosophila melanogaster Subgroup

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

Abstract

Copia is a retrotransposon that appears to be distributed widely among the Drosophilidae subfamily. Evolutionary analyses of regulatory regions have indicated that the Copia retrotransposon evolved through both positive and purifying selection, and that horizontal transfer (HT) could also explain its patchy distribution of the among the subfamilies of the melanogaster subgroup. Additionally, Copia elements could also have transferred between melanogaster subgroup and other species of Drosophilidae—D. willistoni and Z. tuberculatus. In this study, we surveyed seven species of the Zaprionus genus by sequencing the LTR–ULR and reverse transcriptase regions, and by using RT–PCR in order to understand the distribution and evolutionary history of Copia in the Zaprionus genus. The Copia element was detected, and was transcriptionally active, in all species investigated. Structural and selection analysis revealed Zaprionus elements to be closely related to the most ancient subfamily of the melanogaster subgroup, and they seem to be evolving mainly under relaxed purifying selection. Taken together, these results allowed us to classify the Zaprionus sequences as a new subfamily—ZapCopia, a member of the Copia retrotransposon family of the melanogaster subgroup. These findings indicate that the Copia retrotransposon is an ancient component of the genomes of the Zaprionus species and broaden our understanding of the diversity of retrotransposons in the Zaprionus genus.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Almeida LM, Carareto CM (2006) Sequence heterogeneity and phylogenetic relationships between the copia retrotransposon in Drosophila species of the repleta and melanogaster groups. Genet Sel Evol 38(5):535–550

    Article  PubMed  Google Scholar 

  • Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27(2):573–580

    Article  PubMed  CAS  Google Scholar 

  • Bergsten J (2005) A review of long-branch attraction. Cladistics 21(2):163–193

    Article  Google Scholar 

  • Biémont C, Cizeron G (1999) Distribution of transposable elements in Drosophila species. Genetica 105(1):43–62

    Article  PubMed  Google Scholar 

  • Bowen NJ, McDonald JF (2001) Drosophila euchromatic LTR retrotransposons are much younger than the host species in which they reside. Genome Res 11(9):1527–1540

    Article  PubMed  CAS  Google Scholar 

  • Brunet F, Godin F, Bazin C, Capy P (1999) Phylogenetic analysis of Mos1-like transposable elements in the Drosophilidae. J Mol Evol 49(6):760–768

    Article  PubMed  CAS  Google Scholar 

  • Cavarec L, Heidmann T (1993) The Drosophila copia retrotransposon contains binding sites for transcriptional regulation by homeoproteins. Nucleic Acids Res 21(22):5041–5049

    Article  PubMed  CAS  Google Scholar 

  • Chassagnard M-T, Kraaijeveld AR (1991) The occurrence of Zaprionus sensu stricto in the Palearctic region (Diptera: Drosophilidae). Ann Soc Entomol Fr 27(4):495–496

    Google Scholar 

  • Cizeron G, Lemeunier F, Loevenbruck C, Brehm A, Biémont C (1998) Distribution of the retrotransposable element 412 in Drosophila species. Mol Biol Evol 15(12):1589–1599

    PubMed  CAS  Google Scholar 

  • Costa AP, Scortecci KC, Hashimoto RY, Araujo PG, Grandbastien MA, Van Sluys MA (1999) Retrolycl-1, a member of the Tntl retrotransposon super-family in the Lycopersicon peruvianum genome. Genetica 107(1–3):65–72

    Article  CAS  Google Scholar 

  • Da Lage JL, Kergoat GJ, Maczkowiak F, Silvain JF, Cariou ML, Lachaise D (2007) A phylogeny of Drosophilidae using the amyrel gene: questioning the Drosophila melanogaster species group boundaries. J Zoolog Syst Evol Res 45(1):47–63

    Article  Google Scholar 

  • De Salle R (1992) The origin and possible time of divergence of the Hawaiian Drosophilidae: evidence from DNA sequences. Mol Biol Evol 9(5):905–916

    Google Scholar 

  • De Setta N, Carareto CMA (2007) Screening for transposable elements in South America invasive species Zaprionus indianus and Drosophila malerkotliana. Drosoph Inf Serv 90(1):96–99

    Google Scholar 

  • De Setta N, Van Sluys MA, Capy P, Carareto CM (2009) Multiple invasions of Gypsy and Micropia retroelements in genus Zaprionus and melanogaster subgroup of the genus Drosophila. BMC Evol Biol 9:279

    Article  PubMed  Google Scholar 

  • Deprá M, Panzera Y, Ludwig A, Valente VL, Loreto EL (2010) Hosimary: a new hAT transposon group involved in horizontal transfer. Mol Genet Genomics 283(5):451–459

    Article  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39(4):783–791

    Article  Google Scholar 

  • Grabe N (2002) AliBaba2: context specific identification of transcription factor binding sites. In Silico Biol 2(1):S1–S15

    PubMed  Google Scholar 

  • Gradstein F, Ogg J, Smith A (2006) A geological time scale 2004. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Graur D, Li W-H (2000) Fundamentals of molecular evolution. Sinauer Associates, Sunderland

    Google Scholar 

  • Grimaldi DA (1990) A phylogenetic, revised classification of genera in the Drosophilidae (Diptera). Bull Am Mus Nat Hist 197:123–128

    Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52(5):696–704

    Article  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by molecular clock of mitochondrial DNA. J Mol Evol 22(2):160–174

    Article  PubMed  CAS  Google Scholar 

  • Heredia F, Loreto ELS, Valente VL (2004) Complex evolution of gypsy in drosophilid species. Mol Biol Evol 21(10):1831–1842

    Article  PubMed  CAS  Google Scholar 

  • Jordan IK, McDonald JF (1998a) Evolution of the copia retrotransposon in the Drosophila melanogaster species subgroup. Mol Biol Evol 15(9):1160–1171

    PubMed  CAS  Google Scholar 

  • Jordan IK, McDonald JF (1998b) Interelement selection in the regulatory region of the copia retrotransposon. J Mol Evol 47(6):670–676

    Article  PubMed  CAS  Google Scholar 

  • Jordan IK, Matyunina LV, McDonald JF (1999) Evidence for the recent horizontal transfer of long terminal repeat retrotransposon. Proc Natl Acad Sci USA 96(22):12621–12625

    Article  PubMed  CAS  Google Scholar 

  • Jowett T (1986) Preparation of nucleic acids. In: Roberts DB (ed) Drosophila: a practical approach. IRL Press, Oxford, pp 275–277

    Google Scholar 

  • Klimczak LJ, Schindler U, Cashmore AR (1992) DNA binding activity of the Arabidopsis G-box binding factor GBF1 is stimulated by phosphorylation by casein kinase II from broccoli. Plant Cell 4(1):87–98

    Article  PubMed  CAS  Google Scholar 

  • Kwiatowski J, Ayala FJ (1999) Phylogeny of Drosophila and related genera: conflict between molecular and anatomical analyses. Mol Phylogenet Evol 13(2):319–328

    Article  PubMed  CAS  Google Scholar 

  • Kwiatowski J, Skarecky D, Bailey K, Ayala FJ (1994) Phylogeny of Drosophila and related genera inferred from the nucleotide sequence of the Cu, Zn Sod gene. J Mol Evol 38(5):443–454

    Article  PubMed  CAS  Google Scholar 

  • Lachaise D, Silvain JF (2004) How two Afrotropical endemics made two cosmopolitan human commensals: the Drosophila melanogaster-D. simulans palaeogeographic riddle. Genetica 120(1–3):17–39

    Article  PubMed  Google Scholar 

  • Ludwig A, Valente VL, Loreto EL (2008) Multiple invasions of Errantivirus in the genus Drosophila. Insect Mol Biol 17(2):112–113

    Article  Google Scholar 

  • Maruyama K, Hartl DL (1991) Evidence for interspecific transfer of the transposable element mariner between Drosophila and Zaprionus. J Mol Evol 33(6):514–524

    Article  PubMed  CAS  Google Scholar 

  • Matyunina LV, Jordan IK, McDonald JF (1996) Naturally occurring variation in copia expression is due to both element (cis) and host (trans) regulatory variation. Proc Natl Acad Sci USA 93(14):7097–7102

    Article  PubMed  CAS  Google Scholar 

  • McDonald JF, Matyunina LV, Wilson S, Jordan IK, Bowen NJ, Miller WJ (1997) LTR retrotransposons and the evolution of eukaryotic enhancers. Genetica 100(1–3):3–13

    Article  PubMed  CAS  Google Scholar 

  • Montchamp-Moreau C, Ronsseray M, Jacques M, Lehmann M, Anxolabéhère D (1993) Distribution and conservation of sequences homologous to the 1731 retrotransposon in Drosophila. Mol Biol Evol 10(4):791–803

    PubMed  CAS  Google Scholar 

  • Mota NR, Ludwig A, da Silva Valente VL, Loreto EL (2009) Harrow: new Drosophila hAT transposons involved in horizontal transfer. Insect Mol Biol 19(2):217–228

    Article  PubMed  Google Scholar 

  • Mount SM, Rubin GM (1985) Complete nucleotide sequence of the Drosophila transposable element copia: homology between copia and retroviral proteins. Mol Cell Biol 5(7):1630–1638

    PubMed  CAS  Google Scholar 

  • Okada T, Carson HL (1983) The genera Phorticella DUDA and Zaprionus COQUILLETT (Diptera, Drosophilidae) of the Oriental region and New Guinea. Jpn J Entomol 51(4):539–553

    Google Scholar 

  • Pélandakis M, Solignac M (1993) Molecular phylogeny of Drosophila based on ribosomal RNA sequences. J Mol Evol 37(5):525–543

    Article  PubMed  Google Scholar 

  • Remsen J, DeSalle R (1998) Character congruence of multiple data partitions and the origin of the Hawaiian Drosophilidae. Mol Phylogenet Evol 9(2):225–235

    Article  PubMed  CAS  Google Scholar 

  • Robe LJ, Valente VL, Budnik M, Loreto EL (2005) Molecular phylogeny of the subgenus Drosophila (Diptera, Drosophilidae) with an emphasis on neotropical species and groups: a nuclear versus mitochondrial gene approach. Mol Phylogenet Evol 36(3):623–640

    Article  PubMed  CAS  Google Scholar 

  • Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19(18):2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Russo CA, Takezaki N, Nei M (1995) Molecular phylogeny and divergence times of drosophilid species. Mol Biol Evol 12(3):391–404

    PubMed  CAS  Google Scholar 

  • Sánchez-Gracia A, Maside X, Charlesworth B (2005) High rate of horizontal transfer of transposable elements in Drosophila. Trends Genet 21(4):200–203

    Article  PubMed  Google Scholar 

  • Swofford D (1997) PAUP: phylogenetic analysis using parsimony, Version 4.0b10. Smithsonian Institution, Washington DC

    Google Scholar 

  • Tabata T, Nakayama T, Mikami K, Iwabuchi M (1991) HBP-1a and HBP-1b: leucine zipper-type transcription factors of wheat. EMBO J 10(6):1459–1467

    PubMed  CAS  Google Scholar 

  • Tamura K, Nei M, Kumar S (2004a) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA 101(30):11030–11035

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Subramanian S, Kumar S (2004b) Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Mol Biol Evol 21(1):36–44

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24(8):1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Tatarenkov A, Kwiatowski J, Skarecky D, Barrio E, Ayala FJ (1999) On the evolution of Dopa decarboxylase (Ddc) and Drosophila systematics. J Mol Evol 48(4):445–462

    Article  PubMed  CAS  Google Scholar 

  • Thomas RH, Hunt JA (1993) Phylogenetic relationships in Drosophila: a conflict between molecular and morphological data. Mol Biol Evol 10(2):362–374

    PubMed  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Throckmorton LH (1975) The phylogeny, ecology and geography of Drosophila. In: King RC (ed) Handbook of genetics. Plenum, New York, pp 421–469

    Google Scholar 

  • Vidal NM, Ludwig A, Loreto EL (2009) Evolution of Tom, 297, 17.6 and rover retrotransposons in Drosophilidae species. Mol Genet Genomics 282(4):351–362

    Article  PubMed  CAS  Google Scholar 

  • Vilela CR (1999) Is Zaprionus indianus Gupta 1970 (Diptera, Drosophilidae) currently colonizing the Neotropical region? Drosoph Inf Serv 82(1):37–39

    Google Scholar 

  • Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O, Paux E, SanMiguel P, Schulman AH (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8(12):973–982

    Article  PubMed  CAS  Google Scholar 

  • Wilson S, Matyunina LV, McDonald JF (1998) An enhancer region within the copia untranslated leader contains binding sites for Drosophila regulatory proteins. Gene 209(1–2):239–246

    Article  PubMed  CAS  Google Scholar 

  • Xiang C, Miao Z, Lam E (1997) DNA-binding properties, genomic organization and expression pattern of TGA6, a new member of the TGA family of bZIP transcription factors in Arabidopsis thaliana. Plant Mol Biol 34(3):403–415

    Article  PubMed  CAS  Google Scholar 

  • Yang Z (2007) PAML 4: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol 24(8):1586–1591

    Article  PubMed  CAS  Google Scholar 

  • Yassin AE, Abou-Youssef (2004) A new front for a global invasive drosophilid: the colonization of the Northern-Western desert of Egypt by Zaprionus indianus Gupta, 1970. Drosoph Inf Serv 87(1):67–68

    Google Scholar 

  • Yassin A, Araripe LO, Capy P, Da Lage JL, Klaczko LB, Maisonhaute C, Ogereau D, David JR (2008a) Grafting the molecular phylogenetic tree with morphological branches to reconstruct the evolutionary history of the genus Zaprionus (Diptera: Drosophilidae). Mol Phylogenet Evol 47(3):903–915

    Article  PubMed  CAS  Google Scholar 

  • Yassin A, Capy P, Madi-Ravazzi L, Ogereau D, David JR (2008b) DNA barcode discovers two cryptic species and two geographical radiations in the invasive drosophilid Zaprionus indianus. Mol Ecol Notes 8(3):491–501

    CAS  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge funding from the CAPES-COFECUB International Cooperation Program (to NS, CMAC, and PC), FAPESP (MAVS-04/02851-9), CNPq (CMAC and MAVS). NS was the recipient of a CNPq fellowship. We thank J. David and A. Yassin for providing the Zaprionus strains, F. Lemeunier for technical help, and C Metcalfe for correcting the English text.

Author information

Authors and Affiliations

  1. Laboratory of Molecular Evolution, Department of Biology, UNESP, São Paulo State University, 15054-000, São José do Rio Preto, SP, Brazil

    Nathalia de Setta & Claudia Marcia Aparecida Carareto

  2. Genomics and Transposable Elements Lab, Department of Botany, São Paulo University (USP), 05508-090, São Paulo, SP, Brazil

    Nathalia de Setta & Marie-Anne Van Sluys

  3. Laboratoire Evolution, Génomes et Spéciation, UPR9034, CNRS, Gif-sur-Yvette, 91198, Paris, France

    Pierre Capy

  4. Université Paris-Sud 11, 91405, Orsay, France

    Pierre Capy

Authors
  1. Nathalia de Setta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marie-Anne Van Sluys
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pierre Capy
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Claudia Marcia Aparecida Carareto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Claudia Marcia Aparecida Carareto.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 887 kb)

239_2011_9435_MOESM2_ESM.tif

Supplementary Figure 1 Multiple alignment between Copia 5’ LTR–ULR sequences illustrating the regulatory signal conservation between the Zaprionus Copia sequences and the melanogaster variants (Full-length and Double-gap). a: heat shock element; b: TATA box; c: imperfect repeat; d: transcription start; e: downstream element; f: poly-A signal; g: PBS; h: engrailed binding site; i: DmC/EBP biding site; j-i: dyad symmetric (core SV40 enhancer); k: G-box binding factor-1 (GBF-1); l: B-box binding factor-2 (BBF-2). (TIFF 28891 kb)

239_2011_9435_MOESM3_ESM.tif

Supplementary Figure 2 Phylogenetic relationships of the Copia RT region using the first and second codon position (ML method, HKY85 distance). The elimination of the third codon positions minimizes the long-branch attraction effect in the Group D. Bootstrap analysis was computed with 1,000 replications and sequences of repleta species group were used as outgroup. (TIFF 5172 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

de Setta, N., Van Sluys, MA., Capy, P. et al. Copia Retrotransposon in the Zaprionus Genus: Another Case of Transposable Element Sharing with the Drosophila melanogaster Subgroup. J Mol Evol 72, 326–338 (2011). https://doi.org/10.1007/s00239-011-9435-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-011-9435-6

Keywords

Search

Navigation