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hobo-brothers elements and their time and place for horizontal transfer

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Abstract

Transposable elements (TEs) are ubiquitous components of nearly all genomes studied. These elements are highly variable in copy number, molecular structure and transposition strategies. They can move within and between genomes, thus increasing their copy numbers and avoiding being eliminated by stochastic and deterministic processes. hobo is a class II element isolated from Drosophila melanogaster. Previous phylogenetic analyses have shown that the canonical hobo element from D. melanogaster has a sister group formed by sequences found in D. willistoni (called howilli2) and D. mojavensis (called homo1). In the present study, we investigated 36 Drosophilidae species for sequences similar to howilli2 and homo1 using degenerate primers. Additionally, in silico searches were performed in 21 available Drosophila genomes. The obtained sequences formed a monophyletic sister group with the canonical hobo element; we termed these sequences ‘hobo-brothers’ elements. These elements showed a patch distribution and incongruities with the TE and host species phylogenies, suggesting possible cases of horizontal transfer (HT). Species that possess hobo-brothers sequences are from the New World, mainly Neotropical areas. In addition, the estimated divergence of the sequences found showed that these elements are or were recently active; the large number of HT events observed suggests that these elements could be experiencing an expansion process in Neotropical genomes. A comparison of these results with the literature is discussed with regard to the importance of the time and location of horizontal transposon transfer events.

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References

  • Andersson JO (2005) Lateral gene transfer in eukaryotes. Cell Mol Life Sci 62:1182–1197

    Article  PubMed  CAS  Google Scholar 

  • Arensburger P, Hice RH, Zhou L, Smith RC, Tom AC, Wright JA, Knapp J, Brochta DAO, Craig NL, Atkinson PW (2011) Phylogenetic and functional characterization of the hAT transposon superfamily. Genetics 111:1–34

    Google Scholar 

  • Bartolomé C, Bello X, Maside X (2009) Widespread evidence for horizontal transfer of transposable elements across Drosophila genomes. Genome Biol 10:R22

    Article  PubMed  Google Scholar 

  • Blackman RK, Gelbart WM (1989) The transposable element hobo of Drosophila melanogaster. In: Mobile DNA, Berg DE, Howe M. Am Soc Microbiol, Washington DC, pp. 523–529

  • Boussy IA, Itoh M (2004) Wanderings of hobo: a transposon in Drosophila melanogaster and its close relatives. Genetica 120:125–136

    Article  PubMed  CAS  Google Scholar 

  • Carareto C (2011) Tropical Africa as a cradle for horizontal transfers of transposable elements between species of the genera Drosophila and Zaprionus. Mob Genet Elem 1:179–186

    Article  Google Scholar 

  • Daniels SB, Chovnick A, Boussy IA (1990a) Distribution of hobo transposable elements in the genus Drosophila. Mol Biol Evol 7:589–606

    PubMed  CAS  Google Scholar 

  • Daniels SB, Petterson KR, Strausbaugh LD, Kidwell MG, Chovnick AC (1990b) Evidence for horizontal transmission of the P transposable elements between Drosophila species. Genetics 124:339–355

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Eickbush TH, Eickbush DG (2007) Finely orchestrated movements: evolution of the ribosomal RNA genes. Genetics 175:477–485

    Article  PubMed  CAS  Google Scholar 

  • Feschotte C, Pritham EJ (2007) DNA transposons and the evolution of eukaryotic genomes. Annu Rev Genet 41:331–368

    Article  PubMed  CAS  Google Scholar 

  • Graur D, LI WH (2000) Fundamentals of molecular evolution, 2nd edn. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Hua-Van A, Le Rouzic A, Boutin TS, File EJ, Capy P (2011) The struggle for life of the genome’s selfish architects. Biol Direct 6:19

    Article  PubMed  Google Scholar 

  • Kidwell MG (1993) Lateral transfer in natural populations of eukaryotes. Annu Rev Genet 27:235–256

    Article  PubMed  CAS  Google Scholar 

  • Ladevèze V, Chaminade N, Lemeunier F, Periquet P, Aulard S (2012) General survey of hAT transposon superfamily with highlight on hobo element in Drosophila. Genetica 140:375–392

    Article  PubMed  Google Scholar 

  • Lohe AR, Moriyama EM, Lidholm DA, Hartl DL (1995) Horizontal transmission, vertical inactivation, and stochastic loss of mariner like transposable elements. Mol Biol Evol 12:62–72

    Article  PubMed  CAS  Google Scholar 

  • Loreto ELS, Carareto C, Capy P (2008) Revisiting horizontal transfer of transposable elements in Drosophila. Heredity 100:545–554

    Article  PubMed  CAS  Google Scholar 

  • McGinnis W, Shermoen AW, Beckendorf SK (1983) A transposable element insert just 5′ to Drosophila glue protein gene alters gene expression and chromatin structure. Cell 34:75–84

    Article  PubMed  CAS  Google Scholar 

  • Mota NR, Robe LJ, Valente VLS, Budnik M, Loreto ELS (2008) Phylogeny of the Drosophila mesophragmatica group (Diptera, Drosophilidae): an example of Andean evolution. Zool Sci 25:526–532

    Article  PubMed  CAS  Google Scholar 

  • Mota NR, Ludwig A, Valente VL, Loreto ELS (2010) Harrow: new Drosophila hAT transposons involved in horizontal transfer. Insect Mol Biol 19:217–228

    Article  PubMed  CAS  Google Scholar 

  • Oliveira LFV, Wallau GL, Loreto ELS (2009) Isolation of high quality DNA: a protocol combining “rennet” and glass milk. Electron J Biotechnol 12:1–6

    Article  Google Scholar 

  • Ortiz MF, Loreto ELS (2008) The hobo-related elements in the melanogaster species group. Genet Res 90:243–252

    CAS  Google Scholar 

  • Ortiz MF, Loreto ELS (2009) Characterization of new hAT transposable elements in 12 Drosophila genomes. Genetica 135:67–75

    Article  Google Scholar 

  • Periquet G, Lemeunier F, Bigot Y, Hamelin MH, Bazin C, Ladevèze V, Eeken J, Galindo MI, Pascual L, Boussy I (1994) The evolutionary genetics of the hobo transposable element in the Drosophila. Genetica 93:79–90

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Robe LJ, Loreto ELS, Valente VLS (2010) Radiation of the Drosophila subgenus (Drosophilidae, Diptera) in the Neotropics. J Zool Syst Evolut Res 4:310–321

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MRBAYES3: bayesian phylogenetic inferenceunder mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Schaack S, Gilbert C, Feschotte C (2010) Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. Trends Ecol Evol 25:537–546

    Article  PubMed  Google Scholar 

  • Silva JC, Kidwell MG (2000) Horizontal transfer and selection in the evolution of P elements. Mol Biol Evol 17:1542–1557

    Article  PubMed  CAS  Google Scholar 

  • Silva JC, Loreto ELS, Clark JB (2004) Factors that affect the horizontal transfer of transposable elements. Curr Issues Mol Biol 6:57–71

    PubMed  CAS  Google Scholar 

  • Simmons G (1992) Horizontal transfer of hobo transposable elements within the Drosophila melanogaster species complex: evidence from DNA sequencing. Mol Biol Evol 9:1050–1060

    PubMed  CAS  Google Scholar 

  • Staden R (1996) The Staden sequence analysis package. Mol Biotechnol 5:233–241

    Article  PubMed  CAS  Google Scholar 

  • Streck RD, MacGaffey JE, Beckendorf SK (1986) The structure of hobo transposable elements and their insertion sites. EMBO 5:3615–3623

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutioary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 4:1–6

    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 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Torti C, Gomulski LM, Bonizzoni M, Murelli V, Moralli D, Guglielmino CR, Raimondi E, Crisafulli D, Capy P, Gasperi G, Malacrida AR (2005) Cchobo, a hobo-related sequence in Ceratitis capitata. Genetica 123:313–325

    Article  PubMed  CAS  Google Scholar 

  • Wallau GL, Ortiz MF, Loreto ELS (2012) Horizontal transposon transfer in eukarya: detection, bias, and perspectives. Genome Biol Evol 4:689–699

    Article  PubMed  Google Scholar 

  • Werren JH (2011) Selfish genetic elements, genetic conflict, and evolutionary innovation. PNAS 108:10863–10870

    Article  PubMed  CAS  Google Scholar 

  • Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavel 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 8:973–982

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Dr. Lizandra Robe and Gabriel Wallau for suggestions. This study was supported by research grants and fellowships from CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superio), CNPq-Conselho Nacional de Desenvolvimento Científico e Tecnológico, PRONEX-FAPERGS (10/0028-7) and Fapergs (11/0938-0).

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Correspondence to Elgion L. S. Loreto.

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Bernardo, L.P., Loreto, E.L.S. hobo-brothers elements and their time and place for horizontal transfer. Genetica 141, 471–478 (2013). https://doi.org/10.1007/s10709-013-9746-1

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  • DOI: https://doi.org/10.1007/s10709-013-9746-1

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