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General survey of hAT transposon superfamily with highlight on hobo element in Drosophila

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Abstract

The hAT transposons, very abundant in all kingdoms, have a common evolutionary origin probably predating the plant-fungi-animal divergence. In this paper we present their general characteristics. Members of this superfamily belong to Class II transposable elements. hAT elements share transposase, short terminal inverted repeats and eight base-pairs duplication of genomic target. We focus on hAT elements in Drosophila, especially hobo. Its distribution, dynamics and impact on genome restructuring in laboratory strains as well as in natural populations are reported. Finally, the evolutionary history of hAT elements, their domestication and use as transgenic tools are discussed.

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Abbreviations

EDGP:

European Drosophila Genome Project

GD:

Gonadal dystrophy

HT:

Horizontal transfer

LINE:

Long interspersed element

LTR:

Long terminal repeat

ORF:

Open reading frame

SINE:

Short interspersed element

TE:

Transposable element

TIR:

Terminal inverted repeat

TPase:

Transposase

TPE:

Threonine, proline, glutamic acid

TSD:

Target site duplication

V(D)J:

Variable, diverse, joining

References

  • Agraval A, Eastman QM, Schatz DG (1998) Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system. Nature 394:744–751

    Article  CAS  Google Scholar 

  • Andolfatto P, Wall JD, Kreitman M (1999) Unusual haplotype structure at the proximal breakpoint of In(2L)t in a natural population of Drosophila melanogaster. Genetics 153:1297–1311

    PubMed  CAS  Google Scholar 

  • Arensburger P, Hice H, Zhou L, Smith RC, Tom AC, Wright JA, Knapp J, O’Brochta DA, Craig NL, Atkinson PW (2011) Phylogenetic and functional characterization of the hAT transposon superfamily. Genetics 188:45–57

    Article  PubMed  CAS  Google Scholar 

  • Arkhipova IR, Meselson M (2005) Diverse DNA transposons in rotifers of the class Bdelloidea. Proc Natl Acad Sci USA 102:11781–11786

    Article  PubMed  CAS  Google Scholar 

  • Ashburner M, Lemeunier F (1976) Relationships within the melanogaster species subgroup of the genus Drosophila (Sophophora). I. Inversion polymorphisms in Drosophila melanogaster and Drosophila simulans. Proc R Soc Lond B 193:137–157

    Article  PubMed  CAS  Google Scholar 

  • Atkinson PW, Warren WD, O’Brochta DA (1993) The hobo transposable element of Drosophila can be cross-mobilized in houseflies and excises like the Ac element of maize. Proc Natl Acad Sci USA 90:9693–9697

    Article  PubMed  CAS  Google Scholar 

  • Atkinson PW, Pinkerton AC, O’Brochta DA (2001) Genetic transformation systems in insects. Annu Rev Entomol 46:317–346

    Article  PubMed  CAS  Google Scholar 

  • Aulard S, David JR, Lemeunier F (2002) Chromosomal inversion polymorphism in Afrotropical populations of Drosophila melanogaster. Genet Res 79:49–63

    Article  PubMed  Google Scholar 

  • Aulard S, Vaudin P, Ladevèze V, Chaminade N, Périquet G, Lemeunier L (2004) Maintenance of a large pericentric inversion generated by the hobo transposable element in a transgenic line of Drosophila melanogaster. Heredity 92:151–155

    Article  PubMed  CAS  Google Scholar 

  • Aziz RK, Breitbart M, Edwards RA (2010) Transposases are the most abundant, most ubiquitous genes in nature. Nucleic Acids Res 38:4207–4217

    Article  PubMed  CAS  Google Scholar 

  • Baker B, Schell J, Lörz H, Fedoroff N (1986) Transposition of the maize controlling element “Activator” in tobacco. Proc Natl Acad Sci USA 83:4844–4848

    Article  PubMed  CAS  Google Scholar 

  • Bartolomé C, Bello X, Maside X (2009) Widespread evidence for horizontal transfer of transposable elements across Drosophila genomes. Genome Biol 10:R22. doi:10.1186/gb-2009-10-2-r22

    Article  PubMed  CAS  Google Scholar 

  • Benjak A, Forneck A, Casacuberta JM (2008) Genome-wide analysis of the ‘‘cut-and-paste’’ transposons of grapevine. PLoS ONE 3(9):e3107. doi:10.1371/journal.pone.0003107

    Article  PubMed  CAS  Google Scholar 

  • Biémont C, Vieira C (2005) What transposable elements tell us about genome organization and evolution: the case of Drosophila. Cytogenet Genome Res 110:25–34

    Article  PubMed  CAS  Google Scholar 

  • Biessmann H, Valgeirsdottir K, Lofsky A, Chin C, Ginther B, Levis RW, Pardue ML (1992) HeT-A, a transposable element specifically involved in “healing” broken chromosome ends in Drosophila melanogaster. Mol Cell Biol 12:3910–3918

    Google Scholar 

  • Bigot Y, Augé-Gouillou C, Periquet G (1996) Computer analyses reveal a hobo-like element in the nematode Caenorhabditis elegans, which presents a conserved transposase domain common with the Tc1-Mariner transposon family. Gene 174:265–271

    Article  PubMed  CAS  Google Scholar 

  • Blackman RK, Grimalia R, Koehler MM, Gelbart WM (1987) Mobilization of hobo elements residing within the decapentaplegic gene complex: suggestion of a new hybrid dysgenesis system in Drosophila melanogaster. Cell 49:497–505

    Article  PubMed  CAS  Google Scholar 

  • Blackman RK, Koehler MM, Grimalia R, Gelbart WM (1989) Identification of a fully-functional hobo transposable element and its use for germ-line transformation of Drosophila. EMBO J 8:211–217

    PubMed  CAS  Google Scholar 

  • Bonnivard E, Bazin C, Denis B, Higuet D (2000) A scenario for the hobo transposable element invasion, deduced from the structure of natural populations of Drosophila melanogaster using tandem TPE repeats. Genet Res 75:13–23

    Article  PubMed  CAS  Google Scholar 

  • Bonnivard E, Bazin C, Higuet D (2002) High polymorphism of TPE repeats within natural populations of Drosophila melanogaster: a gradient of the 5TPE hobo element in Western Europe. Mol Biol Evol 19:2277–2284

    Article  PubMed  CAS  Google Scholar 

  • Boussy IA, Daniels SB (1991) hobo transposable elements in Drosophila melanogaster and D. simulans. Genet Res 58:27–34

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Bucheton A, Lavige J-M, Picard G, L’Héritier E (1976) Non-mendelian female sterility in Drosophila melanogaster: quantitative variations in the efficiency of inducer and reactive strains. Heredity 36:305–314

    Article  PubMed  CAS  Google Scholar 

  • Bundock P, Hooykaas P (2005) An Arabidopsis hAT-like transposase is essential for plant development. Nature 436:282–284

    Article  PubMed  CAS  Google Scholar 

  • Butter F, Kappei D, Buchholz F, Vermeulen M, Mann M (2010) A domesticated transposon mediates the effects of a single-nucleotide polymorphism responsible for enhanced muscle growth. EMBO Rep 11:305–311

    Article  PubMed  CAS  Google Scholar 

  • Cáceres M, Ranz JM, Barbadilla A, Long M, Ruiz A (1999) Generation of a widespread Drosophila inversion by a transposable element. Science 285:415–418

    Article  PubMed  Google Scholar 

  • Calvi BR, Gelbart WM (1994) The basis for germline specificity of the hobo transposable element in Drosophila melanogaster. EMBO J 13:1636–1644

    PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Capy P, Gasperi G, Biémont C, Bazin C (2000) Stress and transposable elements: co-evolution or useful parasites? Heredity 85:101–106

    Article  PubMed  CAS  Google Scholar 

  • Casals F, Cáceres M, Ruiz A (2003) The foldback-like transposon Galileo is involved in the generation of two different natural chromosomal inversions of Drosophila buzzatii. Mol Biol Evol 20:674–685

    Article  PubMed  CAS  Google Scholar 

  • Chuck G, Robbins T, Nijjar C, Ralston E, Courtney-Gutterson N, Dooner HK (1993) Tagging and cloning of a petunia flower color gene with the maize transposable element Activator. Plant Cell 5:371–378

    PubMed  CAS  Google Scholar 

  • Collins RA, Saville BJ (1990) Independent transfer of mitochondrial chromosomes and plasmids during unstable vegetative fusion in Neurospora. Nature 345:177–179

    Article  PubMed  CAS  Google Scholar 

  • Coyne JA, Aulard S, Berry A (1991) Lack of underdominance in a naturally occurring pericentric inversion in Drosophila melanogaster and its implications for chromosome evolution. Genetics 129:791–802

    PubMed  CAS  Google Scholar 

  • Coyne JA, Meyers W, Crittenden AP, Sniegowski P (1993) The fertility effects of pericentric inversions in Drosophila melanogaster. Genetics 134:487–496

    PubMed  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 Zool Syst Evol Res 45:47–63

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Danilevskaya ON, Slot F, Pavlova M, Pardue ML (1994) Structure of the Drosophila HeT-A transposon: A retrotransposon-like element forming telomeres. Chromosoma 103:215–224

    Article  PubMed  CAS  Google Scholar 

  • Danilevskaya ON, Tan C, Wong J, Alibhai M, Pardue ML (1998) Unusual features of the Drosophila melanogaster telomere transposable element HeT-A are conserved in Drosophila yakuba telomere elements. Proc Natl Acad Sci USA 95:3770–3775

    Article  PubMed  CAS  Google Scholar 

  • de Freitas OrtizM, Loreto EL (2009) Characterization of new hAT transposable element in 12 Drosophila genomes. Genetica 135:67–75

    Article  CAS  Google Scholar 

  • de Freitas OrtizM, Lorenzatto KR, Corrêa BR, Loreto EL (2010) hAT transposable elements and their derivatives: an analysis in the 12 Drosophila genomes. Genetica 138:649–655

    Article  CAS  Google Scholar 

  • Delprat A, Negre B, Puig M, Ruiz A (2009) The transposon Galileo generates natural chromosomal inversions in Drosophila by ectopic recombination. PLoS ONE 4:e7883

    Article  PubMed  CAS  Google Scholar 

  • Depra 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  CAS  Google Scholar 

  • DeVault JD, Hughes KJ, Leopold RA, Johnson OA, Narang SK (1996) Gene transfer into corn earworm (Helicoverpa zea) embryos. Genome Res 6:571–579

    Article  PubMed  CAS  Google Scholar 

  • Dooner HK, Belachew A (1989) Transposition pattern of the maize element Ac from the bz-m2(Ac) allele. Genetics 122:447–457

    PubMed  CAS  Google Scholar 

  • Dreyfus DH (1992) Evidence suggesting an evolutionary relationship between transposable elements and immune system recombination sequences. Mol Immunol 29:807–810

    Article  PubMed  CAS  Google Scholar 

  • Eggleston WB, Rim NR, Lim JK (1996) Molecular characterization of hobo-mediated inversions in Drosophila melanogaster. Genetics 144:647–656

    PubMed  CAS  Google Scholar 

  • Eickbush T, Eickbush D (2005) Transposable elements: evolution. Encyclopedia of life sciences. John Wiley and Sons Ltd, USA. doi:10.1038/npg.els.0005130

    Google Scholar 

  • Emelyanov A, Gao Y, Naqvi NI, Parinov S (2006) Trans-kingdom transposition of the maize dissociation element. Genetics 174:1095–1104

    Article  PubMed  CAS  Google Scholar 

  • Esposito E, Gianfrancesco F, Ciccodicola A, Montanini L, Mumm S, D’Urso M, Forabosco A (1999) A novel pseudoautosomal human gene encodes a putative protein similar to Ac-like transposases. Hum Mol Genet 8:61–67

    Article  PubMed  CAS  Google Scholar 

  • Essers L, Kunze R (1995) Transposable elements Bg (Zea mays) and Tag1 (Arabidopsis thaliana) encode protein sequences with homology to Ac like transposases. Maize Genet Coop Newsl 69:38–41

    Google Scholar 

  • Feschotte C (2008) Transposable elements and the evolution of regulatory networks. Nat Rev Genet 9:397–405

    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 

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

    Article  PubMed  CAS  Google Scholar 

  • Fouvry L, Ogereau D, Berger A, Gavory F, Montchamp-Moreau C (2011) Sequence analysis of the segmental duplication responsible for Paris sex-ratio drive in Drosophila simulans. Genes Genomes Genet (Bethesda) 1:401–410

  • Fowler TJ, Mitton MF (2000) Scooter, a new active transposon in Schizophyllum commune, has disrupted two genes regulating signal transduction. Genetics 156:1585–1594

    PubMed  CAS  Google Scholar 

  • Galindo MI, Bigot Y, Sánchez MD, Periquet G, Pascual L (2001) Sequences homologous to the hobo transposable element in E strains of Drosophila melanogaster. Mol Biol Evol 18:1532–1539

    Article  PubMed  CAS  Google Scholar 

  • Gardner MJ, Hall N, Fung E, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, Paulsen IT, James K, Eisen JA, Rutherford K, Salzberg SL, Craig A, Kyes S, Chan MS, Nene V, Shallom SJ, Suh B, Peterson J, Angiuoli S, Pertea M, Allen J, Selengut J, Haft D, Mather MW, Vaidya AB, Martin DM, Fairlamb AH, Fraunholz MJ, Roos DS, Ralph SA, McFadden GI, Cummings LM, Subramanian GM, Mungall C, Venter JC, Carucci DJ, Hoffman SL, Newbold C, Davis RW, Fraser CM, Barrell B (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:498–511

    Article  PubMed  CAS  Google Scholar 

  • Gelbart WM, Blackman RK (1989) The hobo element of Drosophila melanogaster. Prog Nucleic Acid Res Mol Biol 36:37–46

    Article  PubMed  CAS  Google Scholar 

  • Gentles AJ, Wakefield MJ, Kohany O, Gu W, Batzer MA, Pollock DD, Jurka J (2007) Evolutionary dynamics of transposable elements in the short-tailed opossum Monodelphis domestica. Genome Res 17:992–1004

    Article  PubMed  CAS  Google Scholar 

  • Gibbs RA, Weinstock GM, Metzker ML, Muzny DM, Sodergren EJ et al (2004) Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 428:493–521

    Article  PubMed  CAS  Google Scholar 

  • Gilbert C, Schaack S, Pace JK, Brindley PJ, Feschotte C (2010) A role for host–parasite interactions in the horizontal transfer of transposons across phyla. Nature 464:1347–1350

    Article  PubMed  CAS  Google Scholar 

  • Gilbert C, Hernandez SS, Benabib JF, Smith EN, Feschotte C (2012) Rampant horizontal transfer of SPIN transposons in squamate reptiles. Mol Biol Evol 29:503–515

    Article  PubMed  CAS  Google Scholar 

  • Gray YHM (2000) It takes two transposons to tango: transposable-element-mediated chromosomal rearrangements. TIG 16:461–468

    Article  PubMed  CAS  Google Scholar 

  • Handler AM, Gomez SP (1995) The hobo transposable element has transposase-dependent and -independent excision activity in drosophilid species. Mol Gen Genet 247:399–408

    Article  PubMed  CAS  Google Scholar 

  • Handler AM, Gomez SP (1996) The hobo transposable element excises and has related elements in tephritid species. Genetics 143:1339–1347

    PubMed  CAS  Google Scholar 

  • Hartl DL, Lohe AR, Lozovskaya ER (1997) Modern thoughts on an ancyent marinere: function, evolution, regulation. Annu Rev Genet 31:337–358

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hickman AB, Perez ZN, Zhou L, 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  PubMed  CAS  Google Scholar 

  • Hikosaka A, Koga A (2007) PCR detection of excision suggests mobility of the medaka fish Tol1 transposable element in the frog Xenopus laevis. Genet Res 89:201–206

    Article  PubMed  CAS  Google Scholar 

  • Hiom K, Melek M, Gellert M (1998) DNA transposition by the RAG1 and RAG2 proteins: a possible source of oncogenic translocations. Cell 94:463–470

    Article  PubMed  CAS  Google Scholar 

  • Kaminker JS, Bergman CM, Kronmiller B et al. (2002) The transposable elements of the Drosophila melanogaster euchromatin: a genomics perspective. http://genomebiology.com/2002/3/12/research/0084

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

    Article  PubMed  CAS  Google Scholar 

  • Kapitonov VV, Jurka J (2005) RAG1 core and V(D)J recombination signal sequences were derived from Transib transposons. PLoS Biol 3:e181

    Article  PubMed  CAS  Google Scholar 

  • Kawakami K (2007) Tol2: a versatile gene transfer vector in vertebrates. Genome Biol 8(Suppl 1):S7

    Article  PubMed  Google Scholar 

  • Kawakami K, Noda T (2004) Transposition of the Tol2 element, an Ac-like element from the Japanese medaka fish Oryzias latipes, in mouse embryonic stem cells. Genetics 166:895–899

    Article  PubMed  CAS  Google Scholar 

  • Kawakami K, Shima A (1999) Identification of the Tol2 transposase of the medaka fish Oryzias latipes that catalyzes excision of a nonautonomous Tol2 element in zebrafish Danio rerio. Gene 240:239–244

    Article  PubMed  CAS  Google Scholar 

  • Kawakami K, Koga A, Hori H, Shima A (1998) Excision of the Tol2 transposable element of the medaka fish, Oryzias latipes, in zebrafish, Danio rerio. Gene 225:17–22

    Article  PubMed  CAS  Google Scholar 

  • Kawakami K, Imanaka K, Itoh M, Taira M (2004) Excision of the Tol2 transposable element of the medaka fish Oryzias latipes in Xenopus laevis and Xenopus tropicalis. Gene 338:93–98

    Article  PubMed  CAS  Google Scholar 

  • Kempken F (1995) Horizontal transfer of a mitochondrial plasmid. Mol Gen Genet 248:89–94

    Article  PubMed  CAS  Google Scholar 

  • Kempken F, Kück U (1996) Restless, an active Ac-like transposon from the fungus Tolypocladium inflatum: structure, expression, and alternative RNA splicing. Mol Cell Biol 16:6563–6572

  • Kempken F, Kück U (1998) Evidence for circular transposition derivatives from the fungal hAT-transposon Restless. Curr Genet 34:200–203

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Kermicle JL, Alleman M, Dellaporta SD (1989) Sequential mutagenesis of a maize gene, using the transposable element dissociation. Genome 31:712–716

    Article  Google Scholar 

  • Kidwell MG (1984) Hybrid dysgenesis in Drosophila melanogaster: partial sterility associated with embryo lethality in the P-M system. Genet Res 44:11–28

    Article  PubMed  CAS  Google Scholar 

  • Kidwell MG (1992) Horizontal transfer of P elements and other short inverted repeat transposons. Genetica 86:275–286

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Kidwell MG, Kidwell JF, Sved JA (1977) Hybrid dysgenesis in Drosophila melanogaster: a syndrome of aberrant traits including mutation, sterility and male recombination. Genetics 86:813–833

    PubMed  CAS  Google Scholar 

  • Kikuno K, Tanaka K, Itoh M, Tanaka Y, Boussy IA, Gamo S (2006) Patterns of hobo elements and their effects in natural populations of Drosophila melanogaster in Japan. Heredity 96:426–433

    Article  PubMed  CAS  Google Scholar 

  • Kim JM, Kim W (1996) Hybrid dysgenesis and distribution of hobo elements in Korean populations of Drosophila melanogaster. Korean J Genet 18:83–92

    Google Scholar 

  • Kim JM, Kim W (1999) Identification of a full-size hobo element and deletion derivatives in Korean populations of Drosophila melanogaster. Mol Cells 9:127–132

    PubMed  Google Scholar 

  • Kim YJ, Hice RH, O’Brochta DA, Atkinson PW (2011) DNA sequence requirements for hobo transposable element transposition in Drosophila melanogaster. Genetica 139:985–997

    Article  PubMed  CAS  Google Scholar 

  • Kipling D, Warburton PE (1997) Centromeres, CENP-B and Tigger too. Trends Genet 13:141–145

    Article  PubMed  CAS  Google Scholar 

  • Kodama K, Takagi S, Koga A (2008) The Tol1 element of the medaka fish, a member of the hAT transposable element family, jumps in Caenorhabditis elegans. Heredity 101:222–227

    Article  PubMed  CAS  Google Scholar 

  • Koga A, Inagaki H, Bessho Y, Hori H (1995) Insertion of a novel transposable element in the tyrosinase gene is responsible for an albino mutation in the medaka fish, Oryzias latipes. Mol Gen Genet 249:400–405

    Article  PubMed  CAS  Google Scholar 

  • Koga A, Suzuki M, Inagaki H, Bessho Y, Hori H (1996) Transposable element in fish. Nature 383:30

    Article  PubMed  CAS  Google Scholar 

  • Koga A, Shimada A, Shima A, Sakaizumi M, Tachida H, Hori H (2000) Evidence for recent invasion of the medaka fish genome by the Tol2 transposable element. Genetics 155:273–281

    PubMed  CAS  Google Scholar 

  • Koga A, Higashide I, Hori H, Wakamatsu Y, Kyono-Hamaguchi Y, Hamaguchi S (2007a) The Tol1 element of medaka fish is transposed with only terminal regions and can deliver large DNA fragments into the chromosomes. J Hum Genet 52:1026–1030

    Article  PubMed  CAS  Google Scholar 

  • Koga A, Shimada A, Kuroki T, Hori H, Kusumi J, Kyono-Hamaguchi Y, Hamaguchi S (2007b) The Tol1 transposable element of the medaka fish moves in human and mouse cells. J Hum Genet 52:628–635

    Article  PubMed  CAS  Google Scholar 

  • Kusakabe S, Harada K, Mukai T (1990) The rare inversion with a P element at the breakpoint maintained in a natural population of Drosophila melanogaster. Genetica 82:111–115

    Article  PubMed  CAS  Google Scholar 

  • Ladevèze V, Galindo MI, Pascual L, Periquet G, Lemeunier L (1994) Invasion of the hobo transposable element studied by in situ hybridization on polytene chromosomes of Drosophila melanogaster. Genetica 93:91–100

    Article  PubMed  Google Scholar 

  • Ladevèze V, Galindo MI, Chaminade N, Pascual L, Periquet G, Lemeunier F (1998a) Transmission pattern of hobo transposable element in transgenic lines of Drosophila melanogaster. Genet Res 71:97–107

    Article  PubMed  Google Scholar 

  • Ladevèze V, Aulard S, Chaminade N, Periquet G, Lemeunier F (1998b) Hobo transposons causing chromosomal breakpoints. Proc R Soc Lond B 265:1157–1159

    Article  Google Scholar 

  • Ladevèze V, Aulard S, Chaminade N, Biémont C, Periquet G, Lemeunier F (2001) Dynamics of the hobo transposable element in transgenic lines of Drosophila melanogaster. Genet Res 77:135–142

    Article  PubMed  Google Scholar 

  • Lam WL, Lee TS, Gilbert W (1996) Active transposition in zebrafish. Proc Natl Acad Sci USA 93:10870–10875

    Article  PubMed  CAS  Google Scholar 

  • Lander ES, Linton LM, Birren B et al (2001) International human genome sequencing consortium, initial sequencing and analysis of the human genome. Nature 409:860–921

    Article  PubMed  CAS  Google Scholar 

  • Le Rouzic A, Capy P (2005) The first steps of transposable elements invasion: parasitic strategy vs. genetic drift. Genetics 169:1033–1043

    Article  PubMed  CAS  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  PubMed  Google Scholar 

  • Lemeunier F, Aulard S (1992) Inversion polymorphism in Drosophila melanogaster. In: Krimbas CB, Powell JT (eds) Inversion polymorphism in Drosophila. CRC Press, Boca Raton, pp 339–405

    Google Scholar 

  • Lim JK (1979) Sites-specific instability in Drosophila melanogaster: the origin of mutation and cytogenetic evidence for site specificity. Genetics 93:681–701

    PubMed  CAS  Google Scholar 

  • Lim JK (1988) Intrachromosomal rearrangements mediated by hobo transposons in Drosophila melanogaster. Proc Natl Acad Sci USA 85:9153–9157

    Article  PubMed  CAS  Google Scholar 

  • Lindblad-Toh K, Wade CM, Mikkelsen TS, Karlsson EK, Jaffe DB et al (2005) Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438:803–819

    Article  PubMed  CAS  Google Scholar 

  • Lohe AR, Moriyama EN, 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 

  • Long M, Betrán E, Thornton K, Wang W (2003) The origin of new genes: glimpses from the young and old. Nat Rev Genet 4:865–875

    Article  PubMed  CAS  Google Scholar 

  • Loreto ELS, da Silva LB, Zaha A, Valente VL (1997) Distribution of transposable elements in neotropical species of Drosophila. Genetica 101:153–165

    Article  PubMed  CAS  Google Scholar 

  • Loreto ELS, Zaha A, Valente VL (1998) Transposable element in South American populations of D. simulans. Genet Sel Evol 30:171–180

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lozovskaya ER, Nurminsky DI, Hartl DL, Sullivan DT (1996) Germline transformation of Drosophila virilis mediated by the transposable element hobo. Genetics 142:173–177

    PubMed  CAS  Google Scholar 

  • Lyttle TW, Haymer DS (1992) The role of the transposable element hobo in the origin of endemic inversions in wild populations of Drosophila melanogaster. Genetica 86:113–126

    Article  PubMed  CAS  Google Scholar 

  • Markljung E, Jiang L, Jaffe JD, Mikkelsen TS, Wallerman O, Larhammar M, Zhang X, Wang L, Saenz-Vash V, Gnirke An Lindroth AM, Barres R, Yan J, Stromberg S, De S, Ponten F, Lander AS, Carr SA, Zierath JR, Kullander K, Wadekius C, Linblad-Toh K, Anderson G, Hjalm G, Anderson L (2009) ZBED6, a novel transcription factor derived from a domesticated DNA transposons regulates IGF2 expression and muscle growth. PLoS Biol 7:e10000256

    Article  CAS  Google Scholar 

  • Marzo M, Puig M, Ruiz A (2008) The Foldback-like element Galileo belongs to the P superfamily of DNA transposons and is widespread within the Drosophila genus. Proc Natl Acad Sci USA 105:2957–2962

    Article  PubMed  CAS  Google Scholar 

  • Matzkin LM, Merritt TJS, Zhu CT, Eanes WF (2005) The structure and population genetics of the breakpoints associated with the cosmopolitan chromosomal inversion In(3R)Payne in Drosophila melanogaster. Genetics 170:1143–1152

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • McClintock B (1948) Mutable loci in maize. Carnegie Inst Wash Year Book 47:155–169

    Google Scholar 

  • McClintock B (1953) Induction of instability at selected loci in maize. Genetics 38:579–599

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Mikkelsen TS, Wakefield MJ, Aken B, Amemiya CT, Chang JL, Duke S, Garber M et al (2007) Genome of the marsupial Monodelphis domestica reveals innovation in noncoding sequences. Nature 447:167–177

    Article  PubMed  CAS  Google Scholar 

  • Miller WJ, McDonald JF, Pinsker W (1997) Molecular domestication of mobile elements. Genetica 100:261–270

    Article  PubMed  CAS  Google Scholar 

  • Muehlbauer GJ, Bhau BS, Syed NH, Heinen S, Cho S, Marshall D, Pateyron S, Buisine N, Chalhoub B, Flavell AJ (2006) A hAT superfamily transposase recruited by the cereal grass genome. Mol Genet Genomics 275:553–563

    Article  PubMed  CAS  Google Scholar 

  • Newfeld SJ, Takaesu NT (1999) Local transposition of a hobo element within the decapentaplegic locus of Drosophila. Genetics 151:177–187

    PubMed  CAS  Google Scholar 

  • O’Brochta DA, Stosic CD, Pilitt K, Subramanian RA, Hice RH, Atkinson PW (2009) Transpositionally active episomal hAT elements. BMC Mol Biol 10:108

    Article  PubMed  CAS  Google Scholar 

  • O’Brochta DA, Atkinson PW (1996) Transposable elements and gene transformation in non-Drosophilid insects. Insect Biochem Molec Biol 26:739–753

    Article  Google Scholar 

  • O’Brochta DA, Atkinson PW (2004) Transformation systems in insects. Methods Mol Biol 260:227–254

    PubMed  Google Scholar 

  • O’Brochta DA, Warren WD, Saville KJ, Atkinson PW (1994) Interplasmid transposition of Drosophila hobo elements in non-drosophilid insects. Mol Gen Genet 244:9–14

    Article  PubMed  Google Scholar 

  • Pace JK, Feschotte C (2007) The evolutionary history of human DNA transposons: evidence for intense activity in the primate lineage. Genome Res 17:422–432

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Pascual L, Periquet G (1991) Distribution of hobo transposable elements in natural populations of Drosophila melanogaster. Mol Biol Evol 8:282–296

    PubMed  CAS  Google Scholar 

  • Periquet G, Hamelin MH, Bigot Y, Kai H (1989a) Presence of the deleted hobo element Th in Eurasian populations of Drosophila melanogaster. Genet Sel Evol 21:107–111

    Article  CAS  Google Scholar 

  • Periquet G, Hamelin MH, Bigot Y, Lepissier A (1989b) Geographical and historical patterns of distribution of hobo elements in Drosophila melanogaster populations. J Evol Biol 2:223–229

    Article  Google Scholar 

  • Periquet G, Hamelin MH, Kalmes R, Eeken J (1990) Hobo elements and their deletion-derivative sequences in Drosophila melanogaster and its sibling species D. simulans, D. mauritiana and D. sechellia. Genet Sel Evol 22:393–402

    Article  CAS  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 melanogaster complex. Genetica 93:79–90

    Article  PubMed  CAS  Google Scholar 

  • Peterson PW, Yoder JI (1995) Amplification of Ac in tomato is correlated with high Ac transposition activity. Genome 38:265–276

    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 

  • Pinkerton AC, O’Brochta DA, Atkinson PW (1996) Mobility of hAT transposable elements in the Old World bollworm, Helicoverpa armigera. Insect Mol Biol 5:223–227

    Article  PubMed  CAS  Google Scholar 

  • Pinsker W, Haring E, Hagemann S, Miller WJ (2001) The evolutionary life history of P transposons: from horizontal invaders to domesticated neogenes. Chromosoma 110:148–158

    Article  PubMed  CAS  Google Scholar 

  • Plasterk R (1998) V(D)J recombination: ragtime jumping. Nature 394:718–719

    Article  PubMed  CAS  Google Scholar 

  • Pritham EJ, Feschotte C (2007) Massive amplification of rolling-circle transposons in the lineage of the bat Myotis lucifugus. Proc Natl Acad Sci USA 104:1895–1900

    Article  PubMed  CAS  Google Scholar 

  • Ranz JM, Maurin D, Chan YS, von Grotthuss M, Hillier LW, Roote J, Ashburner M, Bergman CM (2007) Principles of genome evolution in the Drosophila melanogaster species group. PLoS Biol 5:e152

    Article  PubMed  CAS  Google Scholar 

  • Ray DA, Pagan HJT, Thompson ML, Stevens RD (2007) Bats with hATs: evidence for recent DNA transposon activity in genus Myotis. Mol Biol Evol 24:632–639

    Article  PubMed  CAS  Google Scholar 

  • Ray DA, Feschotte C, Pagan HJT, Smith JD, Pritham EJ, Arensburger P, Atkinson PW, Craig NL (2008) Multiple waves of recent DNA transposon activity in the bat, Myotis lucifugus. Genome Res 18:717–728

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Sheen F, Lim JK, Simmons MJ (1993) Genetic instability in Drosophila melanogaster mediated by hobo transposable elements. Genetics 133:315–334

    PubMed  CAS  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 

  • Simmons GM (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 

  • Simmons GM, Plummer D, Simon A, Boussy IA, Frantsve J, Itoh M (1998) Horizontal and vertical transmission of hobo-related sequences between Drosophila melanogaster and Drosophila simulans. In: Syvanen M, Kado CI (eds) Horizontal Gene transfer. Chapman and Hall, New York, pp 285–294

    Google Scholar 

  • Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8:272–285

    Article  PubMed  CAS  Google Scholar 

  • Sorsa V (1998) Chromosome maps of Drosophila. vol 2. CRC Press, Boca Raton

    Google Scholar 

  • Souames S, Bonnivard E, Bazin C, Higuet D (2003a) High mutation rate of TPE repeats: a microsatellite in the putative transposase of the hobo element in Drosophila melanogaster. Mol Biol Evol 20:1826–1832

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Spradling AC, Rubin GM (1982) Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218:341–347

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Subramanian RA, Arensburger P, Atkinson PW, O’Brochta DA (2007) Transposable element dynamics of the hAT element Herves in the human malaria vector Anopheles gambiae s.s. Genetics 176:2477–2487

    Article  PubMed  CAS  Google Scholar 

  • Torres FP, Fonte LF, Valente VL, Loreto EL (2006) Mobilization of a hobo-related sequence in the genome of Drosophila simulans. Genetica 126:101–110

    Article  PubMed  CAS  Google Scholar 

  • Torti C, Malacrida AR, Yannopoulos G, Louis C, Gasperi G (1994) Hybrid dysgenesis-like phenomena in the medfly, Ceratitis capitata (Diptera, Tephritidae). J Hered 85:92–99

    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 

  • Tsutsumi M, Imai S, Kyono-Hamaguchi Y, Hamaguchi S, Koga A, Hori H (2006) Color reversion of the albino medaka fish associated with spontaneous somatic excision of the Tol-1 transposable element from the tyrosinase gene. Pigment Cell Res 19:243–247

    Article  PubMed  CAS  Google Scholar 

  • Volff JN (2006) Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes. BioEssays 28:913–922

    Article  PubMed  CAS  Google Scholar 

  • Volff JN (2010) Tame affairs: domesticated transposase and domestic pigs. EMBO Rep 11:241–242

    Article  PubMed  CAS  Google Scholar 

  • Vollbrecht E, Duvick J, Schares JP et al (2010) Genome-wide distribution of transposed Dissociation elements in maize. Plant Cell 22:1667–1685

    Article  PubMed  CAS  Google Scholar 

  • Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF et al (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420:520–562

    Article  PubMed  CAS  Google Scholar 

  • Weil CF, Kunze R (2000) Transposition of maize Ac/Ds transposable elements in the yeast Saccharomyces cerevisiae. Nat Genet 26:187–190

    Article  PubMed  CAS  Google Scholar 

  • Wesley CS, Eanes WF (1994) Isolation and analysis of the breakpoint sequences of chromosome inversion In(3L)Payne in Drosophila melanogaster. Proc Natl Acad Sci USA 91:3132–3136

    Article  PubMed  CAS  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. Nature Rev Genetics 8:973–982

    Article  CAS  Google Scholar 

  • Woodruff RC, Thompson JN (2003) Transposons as natural and experimental mutagens. Encyclopedia of life sciences. John Wiley and Sons, Ltd, USA. doi:10.1038/npg.els.0000841

    Google Scholar 

  • Yamashita D, Komori H, Higuchi Y, Yamaguchi T, Osumi T, Hirose F (2007) Human DNA replication-related element binding factor (hDREF) self-association via hATC domain is necessary for its nuclear accumulation and DNA binding. J Biol Chem 282:7563–7575

    Article  PubMed  CAS  Google Scholar 

  • Yannopoulos G, Stamatis N, Monastirioti M, Hatzopoulos P, Louis C (1987) hobo is responsible for the induction of hybrid dysgenesis by strains of Drosophila melanogaster bearing the male recombination factor 23.5MRF. Cell 49:487–495

    Article  PubMed  CAS  Google Scholar 

  • Yannopoulos G, Zabalou G, Alahiotis SN (1994) Distribution of P and hobo mobile elements in environmentally manipulated long-term Drosophila melanogaster cage populations. Hereditas 121:87–102

    Article  PubMed  CAS  Google Scholar 

  • Yuan Y-W, Wessler SR (2011) The catalytic domain of all eukaryotic cut-and-paste transposase superfamilies. Proc Natl Acad Sci USA 108:7884–7889

    Article  PubMed  CAS  Google Scholar 

  • Zabalou S, Alahiotis SN, Yannopoulos G (1991) Seasonal analysis of 23.5 MRF (hobo) and P-M hybrid dysgenesis determinants in a Greek natural population of Drosophila melanogaster. Hereditas 114:1–13

    Article  PubMed  CAS  Google Scholar 

  • Zabalou S, Alahiotis SN, Yannopoulos G (1994) A three-season comparative analysis of the chromosomal distribution of P and hobo mobile element in a natural population of Drosophila melanogaster. Hereditas 120:127–140

    Article  PubMed  CAS  Google Scholar 

  • Zakharenko LP, Gracheva EM, Romanova OA, Zakharov IK, Voloshina MA, Kochieva EZ, Simonova OB, Golubovsky MD, Georgiev P (2000) hobo-induced rearrangements are responsible for mutation bursts at the yellow locus in a natural population of Drosophila melanogaster. Mol Gen Genet 263:335–341

    Article  PubMed  CAS  Google Scholar 

  • Zakharenko LP, Kovalenko LV, Mai S (2007) Fluorescence in situ hybridization analysis of hobo, mdg1 and Dm412 transposable elements reveals genomic instability following the Drosophila melanogaster genome sequencing. Heredity 99:525–530

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Zhang F, Peterson T (2006) Transposition of reversed Ac element ends generates novel chimeric genes in maize. PLoS Genet 2:e164

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Yu C, Pulletikurti V, Lamb J, Danilova T, Weber DF, Birchler J, Peterson T (2009) Alternative Ac/Ds transposition induces major chromosomal rearrangements in maize. Genes Dev 23:755–765

    Article  PubMed  CAS  Google Scholar 

  • Zhou L, Mitra R, Atkinson PW, Hickman AB, Dyda F, Craig NL (2004) Transposition of hAT elements links transposable elements and V(D)J recombination. Nature 432:995–1001

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors wish to thank Christian Biémont for helpful comments and discussion. Thanks are also due to anonymous referees for their comments. This work was partially supported by grants from GDR 2157 and GDR 3047 (Centre National de la Recherche Scientifique).

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Authors and Affiliations

  1. UMR 6187 CNRS, Institut de Physiologie et Biologie Cellulaires, Université de Poitiers, 86022, Poitiers Cedex, France

    Véronique Ladevèze

  2. Laboratoire Evolution, Génomes et Spéciation, UPR 9034 CNRS, Avenue de la Terrasse, 91198, Gif-sur-Yvette Cedex, France

    Nicole Chaminade, Françoise Lemeunier & Sylvie Aulard

  3. Université Paris-Sud, 91405, Orsay Cedex, France

    Nicole Chaminade, Françoise Lemeunier & Sylvie Aulard

  4. UMR CNRS 7261, Faculté des Sciences et Techniques, Institut de Recherche sur la Biologie de l’Insecte, Parc Grandmont, 37200, Tours, France

    Georges Periquet

  5. Université Pierre et Marie Curie, 75252, Paris Cedex 05, France

    Sylvie Aulard

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  1. Véronique Ladevèze
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Correspondence to Sylvie Aulard.

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Ladevèze, V., Chaminade, N., Lemeunier, F. et al. General survey of hAT transposon superfamily with highlight on hobo element in Drosophila . Genetica 140, 375–392 (2012). https://doi.org/10.1007/s10709-012-9687-0

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