, 115:403 | Cite as

Abundance and chromosomal distribution of six Drosophila buzzatii transposons: BuT1, BuT2, BuT3, BuT4, BuT5, and BuT6

  • Ferran Casals
  • Josefa González
  • Alfredo RuizEmail author
Research article


The abundance and chromosomal distribution of six class-II transposable elements (TEs) of Drosophila buzzatii have been analyzed by Southern blotting and in situ hybridization. These six transposons had been previously found at the breakpoints of inversions 2j and 2q 7 of D. buzzatii. These two polymorphic inversions were generated by an ectopic recombination event between two copies of Galileo, a Foldback element. The four breakpoints became hotspots for TE insertions after the generation of the inversion and the transposons analyzed in this work are considered to be secondary invaders of these regions. Insertions of the six transposons are present in the euchromatin but show an increased density in the pericentromeric euchromatin–heterochromatin transition region and the dot chromosome. They are also more abundant in the inverted segments of chromosome 2 rearrangements. We further observed that the accumulation of TE insertions varies between elements and is correlated between dot, proximal regions, and inverted segments. These observations fully agree with previous data in Drosophila melanogaster and support recombination rate as the chief force explaining the chromosomal distribution of TEs.


Long Terminal Repeat Proximal Region Basal Density Chromosomal Distribution Chromosomal Inversion 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This work was supported by grant BMC2002-01708 from the Dirección General de Enseñanza Superior e Investigación Científica (Ministerio de Educación y Cultura, Spain), which was awarded to A.R.

Supplementary material

412_2006_71_MOESM5_ESM.jpg (39 kb)
Fig. S1

Southern blot hybridization of (a) BuT1, (b) BuT2, (c) BuT3, (d) BuT4, (e) BuT5 and (f) BuT6 probes to genomic DNA of the following D. buzzatii lines (from left to right): st-1, st-3, st-7, st-10, j-2, j-9, j-19, j-23, j-24, jq7-1, jq7-4, jz3-6, jz3-7, y3-1 and s-1 (JPEG 39 kb)


  1. Andolfatto P, Depaulis F, Navarro A (2001) Inversion polymorphisms and nucleotide variability in Drosophila. Genet Res 77:1–8PubMedCrossRefGoogle Scholar
  2. Ashburner M (1989) Drosophila. A laboratory handbook. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NYGoogle Scholar
  3. Bachtrog D (2003) Accumulation of Spock and Worf, two novel non-LTR retrotransposons, on the neo-Y chromosome of Drosophila miranda. Mol Biol Evol 20:173–181PubMedCrossRefGoogle Scholar
  4. Bartolomé C, Maside X (2004) The lack of recombination drives the fixation of transposable elements on the fourth chromosome of Drosophila melanogaster. Genet Res 83:91–100PubMedCrossRefGoogle Scholar
  5. Bartolomé C, Maside X, Charlesworth B (2002) On the abundance and distribution of transposable elements in the genome of Drosophila melanogaster. Mol Biol Evol 19:926–937PubMedGoogle Scholar
  6. Biemont C, Cizeron G (1999) Distribution of transposable elements in Drosophila species. Genetica 105:43–62PubMedCrossRefGoogle Scholar
  7. Cáceres M, Barbadilla A, Ruiz A (1999a) Recombination rate predicts inversion size in Diptera. Genetics 153:251–259PubMedGoogle Scholar
  8. Cáceres M, Ranz JM, Barbadilla A, Long M, Ruiz A (1999b) Generation of a widespread Drosophila inversion by a transposable element. Science 285:415–418PubMedCrossRefGoogle Scholar
  9. Cáceres M, Puig M, Ruiz A (2001) Molecular characterization of two natural hotspots in the Drosophila buzzatii genome induced by transposon insertions. Genome Res 11:1353–1364PubMedCrossRefGoogle Scholar
  10. Carmena M, González C (1995) Transposable elements map in a conserved pattern of distribution extending from beta-heterochromatin to centromeres in Drosophila melanogaster. Chromosoma 103:676–684PubMedCrossRefGoogle Scholar
  11. 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 20:674–685PubMedCrossRefGoogle Scholar
  12. Casals F, Cáceres M, Manfrin MH, González J, Ruiz A (2005) Molecular characterization and chromosomal distribution of Galileo, Kepler and Newton, three foldback transposable elements of the Drosophila buzzatii species complex. Genetics 169:2047–2059PubMedCrossRefGoogle Scholar
  13. Charlesworth B (1996) Background selection and patterns of genetic diversity in Drosophila melanogaster. Genet Res 68:131–149PubMedGoogle Scholar
  14. Charlesworth B, Langley CH (1989) The population genetics of Drosophila transposable elements. Annu Rev Genet 23:251–287PubMedCrossRefGoogle Scholar
  15. Charlesworth B, Lapid A, Canada D (1992) The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. II. Inferences on the nature of selection against elements. Genet Res 60:115–130PubMedGoogle Scholar
  16. Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215–220PubMedCrossRefGoogle Scholar
  17. Craig NL (1997) Target site selection in transposition. Annu Rev Biochem 66:437–474PubMedCrossRefGoogle Scholar
  18. Daveran-Mingot ML, Campo N, Ritzenthaler P, Le Bourgeois P (1998) A natural large chromosomal inversion in Lactococcus lactis is mediated by homologous recombination between two insertion sequences. J Bacteriol 180:4834–4842PubMedGoogle Scholar
  19. Dimitri P (1997) Constitutive heterochromatin and transposable elements in Drosophila melanogaster. Genetica 100:85–93PubMedCrossRefGoogle Scholar
  20. Dimitri P, Junakovic N, Arca B (2003) Colonization of heterochromatic genes by transposable elements in Drosophila. Mol Biol Evol 20:503–512PubMedCrossRefGoogle Scholar
  21. Eanes WF, Wesley C, Charlesworth B (1992) Accumulation of P elements in minority inversions in natural populations of Drosophila melanogaster. Genet Res 59:1–9PubMedGoogle Scholar
  22. Evgen’ev MB, Zelentsova H, Poluectova H, Lyozin GT, Veleikodvorskaja V, Pyatkov KI, Zhivotovsky LA, Kidwell MG (2000) Mobile elements and chromosomal evolution in the virilis group of Drosophila. Proc Natl Acad Sci U S A 97:11337–11342PubMedCrossRefGoogle Scholar
  23. Francino O, Cabré O, Fontdevila A (1993) Distribution of the copia transposable element in the repleta group of Drosophila. Genet Sel Evol 25:501–516CrossRefGoogle Scholar
  24. Goldman AS, Lichten M (1996) The efficiency of meiotic recombination between dispersed sequences in Saccharomyces cerevisiae depends upon their chromosomal location. Genetics 144:43–55PubMedGoogle Scholar
  25. Gordo I, Charlesworth B (2001) Genetic linkage and molecular evolution. Curr Biol 11:R684–686PubMedCrossRefGoogle Scholar
  26. Hill WG, Robertson A (1966) The effect of linkage on limits to artificial selection. Genet Res 8:269–294PubMedCrossRefGoogle Scholar
  27. Hoskins RA, Smith CD, Carlson JW, Carvalho AB, Halpern A, Kaminker JS, Kennedy C, Mungall CJ, Sullivan BA, Sutton GG, Yasuhara JC, Wakimoto BT, Myers EW, Celniker SE, Rubin GM, Karpen GH (2002) Heterochromatic sequences in a Drosophila whole-genome shotgun assembly. Genome Biol 3:research 0085.1–85.16Google Scholar
  28. Junakovic N, Terrinoni A, Di Franco C, Vieira C, Loevenbruck C (1998) Accumulation of transposable elements in the heterochromatin and on the Y chromosome of Drosophila simulans and Drosophila melanogaster. J Mol Evol 46:661–668PubMedCrossRefGoogle Scholar
  29. Kaminker JS, Bergman CM, Kronmiller B, Carlson J, Svirskas R, Patel S, Frise E, Wheeler DA, Lewis SE, Rubin GM, Ashburner M, Celniker SE (2002) The transposable elements of the Drosophila melanogaster euchromatin: a genomics perspective. Genome Biol 3:research0084.1–84.2Google Scholar
  30. Kim JM, Vanguri S, Boeke JD, Gabriel A, Voytas DF (1998) Transposable elements and genome organization: a comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence. Genome Res 8:464–478PubMedGoogle Scholar
  31. Labrador M, Fontdevila A (1994) High transposition rates of Osvaldo, a new Drosophila buzzatii retrotransposon. Mol Gen Genet 245:661–674PubMedCrossRefGoogle Scholar
  32. Langley CH, Montgomery E, Hudson R, Kaplan N, Charlesworth B (1988) On the role of unequal exchange in the containment of transposable element copy number. Genet Res 52:223–235PubMedGoogle Scholar
  33. Lathe WC 3rd, Burke WD, Eickbush DG, Eickbush TH (1995) Evolutionary stability of the R1 retrotransposable element in the genus Drosophila. Mol Biol Evol 12:1094–1105Google Scholar
  34. Locke J, Podemski L, Roy K, Pilgrim D, Hodgetts RR (1999) Analysis of two cosmid clones from chromosome 4 of Drosophila melanogaster reveals two new genes amid an unusual arrangement of repeated sequences. Genome Res. 9:137–149PubMedGoogle Scholar
  35. Maside X, Bartolome C, Assimacopoulos S, Charlesworth B (2001) Rates of movement and distribution of transposable elements in Drosophila melanogaster: in situ hybridization vs Southern blotting data. Genet Res 78:121–136PubMedCrossRefGoogle Scholar
  36. Montgomery E, Charlesworth B, Langley CH (1987) A test for the role of natural selection in the stabilization of transposable element copy number in a population of Drosophila melanogaster. Genet Res 49:31–41PubMedGoogle Scholar
  37. Montgomery EA, Huang SM, Langley CH, Judd BH (1991) Chromosome rearrangement by ectopic recombination in Drosophila melanogaster: genome structure and evolution. Genetics 129:1085–1098PubMedGoogle Scholar
  38. Navarro A, Betran E, Barbadilla A, Ruiz A (1997) Recombination and gene flux caused by gene conversion and crossing over in inversion heterokaryotypes. Genetics 146:695–709PubMedGoogle Scholar
  39. Naveira H, Fontdevila A (1985) The evolutionary history of Drosophila buzzatii. IX. High frequencies of new chromosome rearrangements induced by introgressive hybridization. Chromosoma 91:87–94PubMedCrossRefGoogle Scholar
  40. Petrov DA, Aminetzach YT, Davis JC, Bensasson D, Hirsh AE (2003) Size matters: non-LTR retrotransposable elements and ectopic recombination in Drosophila. Mol Biol Evol 20:880–892PubMedCrossRefGoogle Scholar
  41. 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 U S A 92:3804–3808PubMedCrossRefGoogle Scholar
  42. Quesneville H, Bergman CM, Andrieu O, Autard D, Nouaud D, Ashburner M, Anxolabehere D (2005) Combined evidence annotation of transposable elements in genome sequences. PLoS Comput Biol 1:166–175PubMedCrossRefGoogle Scholar
  43. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  44. Rizzon C, Marais G, Gouy M, Biemont C (2002) Recombination rate and the distribution of transposable elements in the Drosophila melanogaster genome. Genome Res 12:400–407PubMedCrossRefGoogle Scholar
  45. Ruiz A, Wasserman M (1993) Evolutionary cytogenetics of the Drosophila buzzatii species complex. Heredity 70(Pt 6):582–596PubMedCrossRefGoogle Scholar
  46. Sambrook J, Fritsch E, Maniatis T (1989) Molecular cloning, a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NYGoogle Scholar
  47. SanMiguel P, Tikhonov A, Jin YK, Motchoulskaia N, Zakharov D, Melake-Berhan A, Springer PS, Edwards KJ, Lee M, Avramova Z, Bennetzen JL (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765–768CrossRefGoogle Scholar
  48. SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20:43–45PubMedCrossRefGoogle Scholar
  49. Schwartz A, Chan DC, Brown LG, Alagappan R, Pettay D, Disteche C, McGillivray B, de la Chapelle A, Page DC (1998) Reconstructing hominid Y evolution: X-homologous block, created by X-Y transposition, was disrupted by Yp inversion through LINE–LINE recombination. Hum Mol Genet 7:1–11PubMedCrossRefGoogle Scholar
  50. Steinemann M, Steinemann S (1991) Preferential Y chromosomal location of TRIM, a novel transposable element of Drosophila miranda, obscura group. Chromosoma 101:169–179PubMedCrossRefGoogle Scholar
  51. Steinemann M, Steinemann S (1997) The enigma of Y chromosome degeneration: TRAM, a novel retrotransposon is preferentially located on the Neo-Y chromosome of Drosophila miranda. Genetics 145:261–266PubMedGoogle Scholar
  52. Wharton L (1942) Analysis of the repleta group of Drosophila. Tex Univ Publ 4228:23–52Google Scholar
  53. Wilder J, Hollocher H (2001) Mobile elements and the genesis of microsatellites in dipterans. Mol Biol Evol 18:384–392PubMedGoogle Scholar
  54. Zelentsova H, Poluectova H, Mnjoian L, Lyozin G, Veleikodvorskaja V, Zhivotovsky L, Kidwell MG, Evgen’ev MB (1999) Distribution and evolution of mobile elements in the virilis species group of Drosophila. Chromosoma 108:443–456PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Ferran Casals
    • 1
    • 2
  • Josefa González
    • 1
    • 3
  • Alfredo Ruiz
    • 1
    Email author
  1. 1.Departament de Genètica i de MicrobiologiaUniversitat Autònoma de BarcelonaBellaterraSpain
  2. 2.Unitat de Biologia Evolutiva, Facultat de Ciències de la Salut i de la VidaUniversitat Pompeu FabraBarcelonaSpain
  3. 3.Department of Biological SciencesStanford UniversityStanfordUSA

Personalised recommendations