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hosimary: a new hAT transposon group involved in horizontal transfer

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Abstract

A PCR screening approach was used to search for sequences homologous to a previously described hAT transposon found in Drosophila simulans and Drosophila sechellia, named here as hosimary. In this study, 52 Drosophilidae species were analyzed and these sequences seem to be restricted to some species of the melanogaster group and Zaprionus indianus. These species present variable number of copies and most of those appear to be putatively encoding. The high hosimary sequences similarity among different species and the patchy distribution presented by this transposon strongly support the hypothesis that hosimary was horizontally transferred between the melanogaster group species and Z. indianus.

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References

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

    Article  PubMed  Google Scholar 

  • Arensburger P, Kim YJ, Orsetti J, Aluvihare C, O’Brochta DA, Atkinson PW (2005) An active transposable element, Herves, from the African malaria mosquito Anopheles gambiae. Genetics 169:697–708

    Article  CAS  PubMed  Google Scholar 

  • Bartolomé C, Bello X, Maside X (2009) Widespread evidence for horizontal transfer of transposable elements across Drosophila genomes. Genome Biol. doi:10.1186/gb-2009-10-2-r22

  • Biémont C, Vieira C (2006) Junk DNA as an evolutionary force. Nature 443:521–524

    Article  PubMed  Google Scholar 

  • Boer JG, Yazawa R, Davidson WS, Koop BF (2007) Bursts and horizontal evolution of DNA transposons in the speciation of pseudotetraploid salmonids. BMC Genomics. doi:10.1186/1471-2164-8-422 8:422

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

    Article  CAS  PubMed  Google Scholar 

  • Calvi BR, Hong TJ, Findley SD, Gelbart WM (1991) Evidence for a common evolutionary origin of inverted repeat transposons in Drosophila and plants: hobo, Activator, and Tam3. Cell 66:465–471

    Article  CAS  PubMed  Google Scholar 

  • Capy P, Bazin C, Higuet D, Langin T (1998) Dynamics and evolution of transposable elements. Landes Bioscience, Austin, Texas

    Google Scholar 

  • Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, Markow TA et al (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450:203–218

    Article  PubMed  Google Scholar 

  • Coates CJ, Jonhson KM, Perkins HD, Howells AJ, O’Brochta DA, Atkinson PW (1996) The hermit transposable element of the Australian sheep blowfly, Lucilia cuprina, belongs to the hAT family of transposable elements. Genetica 97:23–31

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • David J, Lemeunier F, Tsacas L, Yassin A (2007) The historical discovery of the nine species in the Drosophila melanogaster species subgroup. Genetics 177:1969–1973

    Article  PubMed  Google Scholar 

  • Diao X, Freeling M, Lisch D (2006) Horizontal transfer of a plant transposon. PLoS Biology 4:119–128

    Article  CAS  Google Scholar 

  • Finnegan DJ (1989) Eukaryotic transposable elements and genome evolution. Trends Genet 5:103–107

    Article  CAS  PubMed  Google Scholar 

  • Grumbling G, Strelets V (2006) FlyBase: anatomical data, images and queries. Nucleic Acids Res 34:484–488

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hehl R, Nacken WK, Krause A, Saedler H, Sommer H (1991) Structural analysis of Tam3, a transposable element from Antirrhinum majus, reveal homologies to the Ac element from maize. Plant Mol Biol 16:369–371

    Article  CAS  PubMed  Google Scholar 

  • Herédia FO, Loreto ELS, Valente VLS (2004) Complex evolution of gypsy in Drosophilid species. Mol Biol Evol 21:1–12

    Article  Google Scholar 

  • Hickman AB, Perez ZN, Zhou LQ, Musingarimi P, Ghirlando R, Hinshaw JE, Craig NL, Dyda F (2005) Molecular architecture of a eukaryotic DNA transposase. Nat Struct Mol Biol 12:715–721

    Article  CAS  PubMed  Google Scholar 

  • Hotopp JC, Clark ME, Oliveira DC, Foster JM, Fischer P, Torres MC et al (2007) Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317:1753–1756

    Article  CAS  PubMed  Google Scholar 

  • Kapitonov VV, Jurka J (2003) Molecular paleontology of transposable elements in the Drosophila melanogaster genome. Proc Natl Acad Sci USA 100:6569–6574

    Article  CAS  PubMed  Google Scholar 

  • Kempken F, Windhofer F (2001) The hAT family: a versatile transposon group common to plants, fungi, animals, and man. Chromosoma 110:1–9

    Article  CAS  PubMed  Google Scholar 

  • Kidwell MG, Lisch DR (1997) Transposable elements as sources of variation in animals and plants. Proc Natl Acad Sci USA 94:7704–7711

    Article  CAS  PubMed  Google Scholar 

  • Kidwell MG, Lisch DR (2001) Transposable elements, parasitic DNA, and genome evolution. Evolution 55:1–24

    CAS  PubMed  Google Scholar 

  • Klasson L, Kambris Z, Cook PE, Walker T, Sinkins SP (2009) Horizontal gene transfer between Wolbachia and the mosquito Aedes aegypti. BMC Genomics. doi:10.1186/1471-2164-10-33

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

    Article  PubMed  Google Scholar 

  • Lachaise D, David JR, Lemeunier F, Tsacas L, Ashburner M (1986) The reproductive relationships of Drosophila sechellia with D. mauritiana, D. simulans and D. melanogaster from the Afrotropical region. Evolution 40:262–271

    Article  Google Scholar 

  • Le Rouzic A, Boutin TS, Capy P (2007) Long-term evolution of transposable elements. Proc Natl Acad Sci USA 104:19375–19380

    Article  CAS  PubMed  Google Scholar 

  • Lerat E, Rizzon C, Biémont C (2003) Sequence divergence of transposable elements in the D. melanogaster genome. Genome Res 13:1889–1896

    CAS  PubMed  Google Scholar 

  • Loreto EL, Zaha A, Nichols C, Pollock JA, Valente VLS (1998) Characterization of a hypermutable strain of Drosophila simulans. Cell Mol Life Sci 54:1283–1290

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ludwig A, Valente VLS, Loreto ELS (2008) Multiple invasions of Errantivirus in the genus Drosophila. Insect Mol Biol 17:113–124

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Maside X, Assimacopoulos S, Charlesworth B (2005) Fixation of transposable elements in the Drosophila melanogaster genome. Genet Res 85:195–203

    Article  CAS  PubMed  Google Scholar 

  • McClintock B (1947) Cytogenetic studies of maize and Neurospora. Carnegie Inst Washington Year Book 46:146–152

    Google Scholar 

  • Michalak P, Noor MAF (2004) Association of Misexpression with Sterility in Hybrids of Drosophila simulans and D. mauritiana. J Mol Evol 59:277–282

    Article  CAS  PubMed  Google Scholar 

  • Morton BR (1993) Chloroplast DNA codon use: evidence for selection at the psbA locus based on tRNA availability. J Mol Evol 37:273–280

    Article  CAS  PubMed  Google Scholar 

  • Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426

    CAS  PubMed  Google Scholar 

  • Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala

    Google Scholar 

  • Ortiz M, Loreto EL (2009) Characterization of new hAT transposable elements in twelve Drosophila genomes. Genetica 135:67–75

    Article  Google Scholar 

  • Pace JK II, Gilbert C, Clark MS, Feschotte C (2008) Repeated horizontal transfer of a DNA transposon in mammals and other tetrapods. Proc Natl Acad Sci USA 105:17023–17028

    Article  CAS  PubMed  Google Scholar 

  • Remsen J, O’Grady P (2002) Phylogeny of Drosophilinae (Diptera: Drosophilidae), with comments on combined analysis and character support. Mol Phylogenet Evol 24:249–264

    Article  PubMed  Google Scholar 

  • Robe LJ (2008) Relações filogenéticas no gênero Drosophila (Diptera, Drosophilidae): uma abordagem molecular. PhD Thesis. Universidade Federal do Rio Grande do Sul

  • Robe LJ, Valente VLS, Budnik M, Loreto ELS (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 36:623–640

    Article  CAS  PubMed  Google Scholar 

  • Robert CE (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Roulin A, Piegu B, Wing RA, Panaud O (2008) Evidence of multiple horizontal transfers of the long terminal repeat retrotransposon RIRE1 within the genus Oryza. Plant J 53:950–959

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Rubin E, Lithwick G, Levy AA (2001) Structure and evolution of the hAT transposon superfamily. Genetics 158:949–957

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Sassi AK, Herédia FO, Loreto ELS, Valente VLS, Rohde C (2005) Transposable elements P and gypsy in natural populations of Drosophila willistoni. Genet Mol Biol 28:734–739

    Article  CAS  Google Scholar 

  • Sharp PM, Li W-H (1989) On the rate of DNA sequence evolution in Drosophila. J Mol Evol 28:398–402

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Silva JC, Loreto EL, Clark JB (2004) Factors that affect the horizontal transfer of transposable elements. Curr Issues Mol Biol 6:57–72

    CAS  PubMed  Google Scholar 

  • Souames S, Bazin C, Bonnivard E, Higuet D (2003) Behavior of the hobo transposable element with regard to TPE repeats in transgenic lines of Drosophila. Mol Biol Evol 20:2055–2066

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Subramanian RA, Cathcart LA, Krafsur ES, Atkinson PW, O’Brochta DA (2009) Hermes transposon distribution and structure in Musca domestica. J Hered 100:473–480

    Article  CAS  PubMed  Google Scholar 

  • Tamura K (1992) Estimation of the number of nucleotide substitution when there are strong transition-transversion and G + C biases. Mol Biol Evol 9:678–687

    CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Vidal NM, Ludwig A, Loreto ELS (2009) Evolution of Tom, 297, 17.6 and rover retrotransposons in Drosophilidae species. Mol Genet Genomics Doi:10.1007/s00438-009-0468-0

  • Vieira C, Fablet M, Lerat E (2009) Infra- and transspecific Clues to understanding the dynamics of transposable elements. In: Lankenau DH, Volff JN (eds) Transposons and the dynamic genome. Springer, Berlin

    Google Scholar 

  • Warren WD, Atkinson PW, O’Brochta DA (1994) The Hermes transposable element from the house fly, Musca domestica, is a short inverted repeat-type element of the hobo, Ac, and Tam3 (hAT) element family. Genet Res 64:87–97

    Article  CAS  PubMed  Google Scholar 

  • Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B et al (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8:973–982

    Article  CAS  PubMed  Google Scholar 

  • Wright F (1990) The “effective number of codons” used in a gene. Gene 87:23–29

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

To Dra. Claude Bazin for gently providing the Zola strain. To M.Sc. Nina Roth Mota and Dra. Lizandra Robe for the valuable help and critical comments which contributed significantly to the improvement of this manuscript. To M.Sc. Paloma Rubin for sequencing the DNA samples. This work was supported by grants from CNPq.

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Authors and Affiliations

  1. Programa de Pós-Graduação em Genética e Biologia Molecular, Departamento de Genética, Universidade Federal do Rio Grande do Sul (UFRGS), Rio Grande do Sul, Porto Alegre, Brazil

    Maríndia Deprá, Adriana Ludwig, Vera L. S. Valente & Elgion L. S. Loreto

  2. Sección Genética Evolutiva, Facultad de Ciencias, Universidad de la República, Montevideo, Uruguay

    Yanina Panzera

  3. Departamento de Biologia, Universidade Federal de Santa Maria (UFSM), Rio Grande do Sul, Santa Maria, 97105-900, Brazil

    Elgion L. S. Loreto

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  1. Maríndia Deprá
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  2. Yanina Panzera
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Correspondence to Elgion L. S. Loreto.

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Communicated by G. Reuter.

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Deprá, M., Panzera, Y., Ludwig, A. et al. hosimary: a new hAT transposon group involved in horizontal transfer. Mol Genet Genomics 283, 451–459 (2010). https://doi.org/10.1007/s00438-010-0531-x

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