Advertisement

Molecular and General Genetics MGG

, Volume 248, Issue 4, pp 423–433 | Cite as

Characterization ofGandalf, a new inverted-repeat transposable element ofDrosophila koepferae

  • Ignacio Marín
  • Antonio Fontdevila
Original paper

Abstract

The cloning and characterization ofGandalf, a new DNA-transposing mobile element obtained from theDrosophila koepferae (repleta group) genome is described. A fragment ofGandalf was found in a middle repetitive clone that shows variable chromosomal localization. Restriction, Southern blot, PCR and sequencing analyses have shown that mostGandalf copies are about 1 kb long, are flanked by 12 by inverted terminal repeats and contain subterminal repetitive regions on both sides of the element. As with other elements of the DNA-transposing type (known as the ‘Ac family’), theGandalf element generates 8 by direct duplications at the insertion point. Coding region analysis has shown that the longer open reading frame found inGandalf copies could encode part of a protein. However, whether or not the 1 kb copies of the element are actually the active transposons remains to be elucidated.Gandalf shows a very low copy number inD. buzzatii, a sibling species ofD. koepferae. An attempt to induce interspecific hybrid dysgenesis in hybrids of these two species has been unsuccessful.

Key words

Drosophila Transposable elements repleta group Ac family Hybrid instability 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Blackman RK, Grimalia R, Koehler MMD, Gelbart WM (1987) Mobilization ofhobo elements residing within thedecapentaplegic gene complex: suggestion of a new hybrid dysgenesis system inDrosophila melanogaster. Cell 49:497–505Google Scholar
  2. Blackman RK, Koehler MMD, Grimalia R, Gelbart WM (1989) Identification of a fully-functionalhobo transposable element and its use for germ-like transformation ofDrosophila. EMBO J, 8:211–217Google Scholar
  3. Brennan MD, Rowan RG, Dickinson WJ (1984) Introduction of a functionalP element into the germ-line ofDrosophila hawaiiensis. Cell 38:147–151Google Scholar
  4. Brezinsky L, Wang GLV, Humphreys T, Hunt J (1990) The transposable element Uhu from HawaiianDrosophila — member of the widely dispersed class ofTcl-like transposons. Nucleic Acids Res 18:2053–2059Google Scholar
  5. Bucheton A, Paro R, Sang HM, Pelisson A, Finnegan DJ (1984) The molecular basis of I-R hybrid dysgenesis inDrosophila melanogaster: identification, cloning and properties of the 1 factor. Cell 38:153–163Google Scholar
  6. Bullock P, Miller J, Botchan M (1986) Effects of poly(d(pGpT)d(pApC)) and poly(d(pCpG)-d(pCpG)) repeats on homologous recombination in somatic cells. Mol Cell Biol 6:3948–3953Google Scholar
  7. Calvi BR, Hong TJ, Findley SD, Gelbart WM (1990) Evidence for a common evolutionary origin of inverted repeat transposons inDrosophila and plants:hobo, Activator andTam3. Cell 66:465–471Google Scholar
  8. Capy P, Koga A, David JR, Hard DL (1992) Sequence analysis of active mariner elements in natural populations ofDrosophila simulans. Genetics 130:499–506Google Scholar
  9. Charlesworth B, Langley CH, Stephen W (1986) The evolution of restricted recombination and the accumulation of repeated sequences. Genetics 112:947–962Google Scholar
  10. Chomet P, Lisch D, Hardeman KJ, Chandler VL, Freeling M (1991) Identification of a regulatory transposon that controls theMutator transposable element system in maize. Genetics 129: 261–270Google Scholar
  11. Coupland G, Baker B, Schelland J, Starlinger P (1988) Characterization of the maize transposable elementAc by internal deletions. EMBO J 7:3653–3659Google Scholar
  12. Coupland G, Plum C, Chatterjee S, Post A, Starlinger P (1989) Sequences near the termini are required for transposition of the maize transposonAc in transgenic tobacco plants. Proc Natl Acad Sci USA 86:9385–9388Google Scholar
  13. Daniels SB, Strausbaugh LD, Armstrong RA (1985) Molecular analysis ofP element behavior inDrosophila simulans transformants. Mol Gen Genet 200:258–265Google Scholar
  14. Devereux J, Haeberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395Google Scholar
  15. Doak TG, Doerder FP, Jahn CL, Herrick G (1994) A proposed superfamily of transposase genes: transposon-like elements in ciliated protozoa and a common ‘D35Ers motif. Proc Natl Acad Sci USA 91:942–946Google Scholar
  16. Engels WR (1989)P elements inDrosophila melanogaster. In: Berg DE, Howe MM (eds) Mobile DNA. American Society for Microbiology, Washington pp 437–484Google Scholar
  17. Fickett JW (1982) Recognition of protein coding regions in DNA sequences. Nucleic Acids Res 10:5303–5318Google Scholar
  18. Finnegan DJ (1989) Eukaryotic transposable elements and genome evolution. Trends Genet 5:103–107Google Scholar
  19. Fontdevila A, Pla C, Hasson E, Wasserman M, Sánchez A, Naveira H, Ruíz A (1988)Drosophila koepferae: a new member of theDrosophila serido (Diptera: Drosophilidae) superspecies toxon. Ann Entomol Soc Am 81:380–385Google Scholar
  20. Francino O, Cabre O, Fontdevila A (1994) Distribution of thecopia transposable element in therepleta group ofDrosophila. Genet Sel Evol 25:501–516Google Scholar
  21. Franz G, Sauakis C (1991)Minos, a new transposable element fromDrosophila hydei, is a member of the Tcl-like family of transposons. Nucleic Acids Res 19:6646Google Scholar
  22. Frey M, Reinecke J, Grant S, Saedler H, Gierl A (1990) Excision of the EnISpm transposable element of Zea mays requires two element-encoded proteins. EMBO J 9:4037–4044Google Scholar
  23. Garza D, Medhora M, Koga A, Hartl DL (1991) Introduction of the transposable elementmariner into the germline ofDrosophila melanogaster. Genetics, 128: 303–310Google Scholar
  24. Genetics Computer Group (1991) Program manual for the GCG package, version 7, April 1991, 575 Science Drive, Madison, Wisconsin, USA 53711Google Scholar
  25. Gierl A (1990) How maize transposable elements escape negative selection. Trends Genet 6:155–158Google Scholar
  26. Gierl A, Lütticke S, Saedler H (1988) TnpA product encoded by the transposable elementEn-1 ofZea mays is a DNA binding protein. EMBO J 7:4045–4053Google Scholar
  27. Gierl A, Saedler H, Peterson PA (1989) Maize transposable elements. Annu Rev Genet 23:71–85Google Scholar
  28. Harris LJ, Baillie DL, Rose AM (1988) Sequence identity between an inverted repeat family of transposable elements inDrosophila andCaenorhabditis. Nucleic Acids Res 16: 5991–5998Google Scholar
  29. Hehl R, Nacken WKF, Krause A, Saedler H, Sommer H (1991) Structural analysis ofTam3, a transposable element fromAntirrhinum majus, reveals homologies to theAc element from maize. Plant Mol Biol 16:369–371Google Scholar
  30. Hellman L, Steen M-L, Sundvall M, Pettersson U (1988) A rapidly evolving region in the immunoglobin heavy chain loci of rat and mouse: postulated role of (dC-dA)n-(dG-dT)n sequences. Gene 68:93–100Google Scholar
  31. Jacobson JW, Medhora MM, Hartl DL (1986) Molecular structure of a somatically unstable transposable element inDrosophila. Proc Natl Acad Sci USA 83:8684–8688Google Scholar
  32. Karess RE, Rubin GM (1984) Analysis ofP transposable element functions inDrosophila. Cell 38:135–146Google Scholar
  33. Kaufman PD, Doll RF, Rio DC (1989)Drosophila P element transposase recognizes internalP element DNA sequences. Cell 59:359–371Google Scholar
  34. Kaufman PD, Rio DC (1991)Drosophila P-element transposase is a transcriptional repressorin vitro. Proc Natl Acad Sci USA 88:2613–2617Google Scholar
  35. Kay BK, Dawid IB (1983) The1723 element: a long, homogeneous, highly repeated DNA unit interspersed in the genome ofXenopus laevis. J Mol Biol 170:583–596Google Scholar
  36. Kozak M (1983) Comparison of initiation of protein synthesis in procaryotes, eucaryotes and organelles. Microbiol Rev 47:1–45Google Scholar
  37. Kunze R, Starlinger P (1989) The putative transposase of transposable elementAc fromZea mays L. interacts with subterminal sequences ofAc. EMBO J 8:3177–3185Google Scholar
  38. Labrador M, Fontdevila A (1994) High transposition rates ofOsvaldo, a newDrosophila buzzatii retrotransposon. Mol Gen Genet 245:661–674Google Scholar
  39. Labrador M, Naveira H, Fontdevila A (1990) Genetic mapping of theAdh locus in theRepleta group ofDrosophila byin situ hybridization. J Hered 81: 83–86Google Scholar
  40. 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 52:223–235Google Scholar
  41. Li M-G, Starlinger P (1990) Mutational analysis of the N-terminus of the protein of maize transposable elementAc. Proc Natl Acad Sci USA 87:6044–6048Google Scholar
  42. Lowenhaupt K, Rich A, Pardue ML, (1989) Nonrandom distribution of long mono- and dinucleotide repeats inDrosophila chromosomes: correlations with dosage compensation, heterochromatin, and recombination. Mol Cell Biol 9:1173–1182Google Scholar
  43. Marin I, Labrador M, Fontdevila A (1992) The evolutionary history ofD. buzzatii. XXIII. High content of nonsatellite repetitive DNA inD. buzzatii and in its siblingD. koepferae. Genome 35:967–974Google Scholar
  44. Marin I, Ruiz A, Pla C, Fontdevila A (1993) Evolution 47:1616–1624Google Scholar
  45. Maruyama K, Schoor KD, Hartl DL (1991) Identification of nucleotide substitutions necessary for trans-activation ofmariner transposable elements inDrosophila: analysis of naturally occurring elements. Genetics 128:777–784Google Scholar
  46. Medhora MM, MacPeek AH, Hard DL (1988) Excision of theDrosophila transposable elementmariner: identification and characterization of theMos factor. EMBO J 7:2185–2189Google Scholar
  47. Medhora M, Maruyama K, Hard DL (1991) Molecular and functional analysis of the mariner mutator elementMosl inDrosophila. Genetics 128:311–318Google Scholar
  48. Montgomery EA, Huang S-M, Langley CH, Judd BH (1991) Chromosome rearrangement by ectopic recombination inDrosophila melanogaster: genome structure and evolution. Genetics 129:1085–1098Google Scholar
  49. Morgan GT, Middleton KM (1990) Short interspersed repeats fromXenopus that contain multiple octamer motifs are related to known transposable elements. Nucleic Acids Res 18: 5781–5786Google Scholar
  50. Mori I, Moerman DG, Waterston RH (1988) Analysis of a mutator activity necessary for germline transposition and excision of Tel transposable elements inCaenorhabditis elegans. Genetics 120: 397–407Google Scholar
  51. Mount SM, Burks C, Hertz G, Stormo GD, White O, Fields C (1992) Splicing signals inDrosophila: intron size, information content and consensus sequences. Nucleic Acids Res 20:4255–4262Google Scholar
  52. Müllller-Neumann M, Yoder JI, Starlinger P (1984) The DNA sequence of the transposable elementAc ofZea mays L. Mol Gen Genet 198: 19–24Google Scholar
  53. Nacken WKF, Piotrowiak R, Saedler H, Sommer H (1991) The transposable elementTaml fromAnthirrhinum majus shows structural homology to the maize transposonEn/Spm and has no sequence specificity of insertion. Mol Gen Genet 228:201–208Google Scholar
  54. Naveira H, Fontdevila A (1985) The evolutionary history ofDrosophila buzzatii. IX. High frequencies of new chromosome rearrangements induced by introgressive hybridization. Chromosoma 91:87–94Google Scholar
  55. Naveira H, Pla C, Fontdevila A (1986) The evolutionary history ofDrosophila buzzatii. XI. A new method for cytogenetic localization based on asynapsis of polytene chromosomes in interspecific hybrids ofDrosophila. Genetica 71:199–212Google Scholar
  56. O'Brochta DA, Handler AM (1988) Mobility ofP elements in drosophilids and nondrosophilids. Proc Natl Acad Sci USA 85:6052–6056Google Scholar
  57. O'Brochta DA, Gomez SP, Handler AM (1991)P element excision inDrosophila melanogaster and related drosophilids. Mol Gen Genet 225:387–394Google Scholar
  58. O'Hare K, Rubin GM (1983) Structures ofP transposable elements and their sites of insertion and excision in theDrosophila melanogaster genome. Cell 34:25–35Google Scholar
  59. Pereira A, Schwarz-Sommer Z, Gierl A, Bertram I, Peterson PA, Saedler H (1985) Genetic and molecular analysis of theEnhancer (En) transposable element system ofZea mays. EMBO J 4:17–23Google Scholar
  60. Prasad SS, Harris LJ, Baillie DL, Rose AM (1991) Evolutionarily conserved regions inCaenorhabditis transposable elements deduced by sequence comparison. Genome 34:6–12Google Scholar
  61. Rhodes PR, Vodkin LO (1988) Organization of theTgm family of transposable elements in soybean. Genetics 120: 597–604Google Scholar
  62. Rio DC (1990) Molecular mechanisms regulatingDrosophila P element transposition. Annu Rev Genet 24: 543–578Google Scholar
  63. Rio DC (1991) Regulation ofDrosophila P element transposition. Trends Genet 7:282–287Google Scholar
  64. Rio DC, Rubin GM (1988) Identification and purification of aDrosophila protein that binds to the terminal 31-base-pair inverted repeats of theP transposable element. Proc Natl Acad Sci USA 85:8929–8933Google Scholar
  65. Rio DC, Laski FA, Rubin GM (1986) Identification and immunochemical analysis of biologically activeDrosophila P element transposase. Cell 44:21–32Google Scholar
  66. Rosenzweig B, Liao LW, Hirsh D (1983) Sequence of theC. elegans transposable elementTcl. Nucleic Acids Res 11:4201–4209Google Scholar
  67. Rubin GM, Kidwell MG, Bingham PM (1982) The molecular basis of P-M hybrid dysgenesis: the nature of induced mutations. Cell 29:987–994Google Scholar
  68. Ryden TA, Beeman K (1989) Avian retroviral long terminal repeats bind CCAAT/Enhancer-binding protein. Mol Cell Biol 9: 1155–1164Google Scholar
  69. Scavarda NJ, Hard DL (1984) Interspecific DNA transformation inDrosophila. Proc Natl Acad Sci USA 81:7515–7519Google Scholar
  70. Schafer DJ, Fredline DK, Knibb WR, Green MM, Barker JSF (1993) Genetics and linkage mapping ofDrosophila buzzatii. J Hered 84:188–194Google Scholar
  71. Sommer H, Carpenter R, Harrison BJ, Saedler H (1985) The transposable elementTam3 ofAntirrhinum majus generates a novel type of sequence alterations upon excision. Mol Gen Genet 199:225–231Google Scholar
  72. Streck RD, MacGaffey JE, Beckendorf SK (1986) The structure ofhobo transposable elements and their insertion sites. EMBO J 5:3615–3623Google Scholar
  73. Templeton NS, Potter SS (1989) Completefoldback transposable elements encode a novel protein found inDrosophila melanogaster. EMBO J 8:1887–1894Google Scholar
  74. Tolkien JRR (1954) The Lord of the Rings. Allen and Unwin, LondonGoogle Scholar
  75. Treco D, Arnheim N (1986) The evolutionary conserved repetitive sequence d(TG-AC)n promotes reciprocal exchange and generates unusual recombinant tetrads during yeast meiosis. Mol Cell Biol 6: 3934–3947Google Scholar
  76. Ueda H, Mizuno S, Shimura K (1986) Transposable genetic element found in the 5′-flanking region of the fibroin H-chain in a genomic clone from the silkwormBombyx mori. J Mol Biol 190:319–327Google Scholar
  77. Van Sluys MA, Tempé J, Fedoroff N (1987) Studies on the introduction and mobility of the maizeActivator element inArabidopsis thaliana andDaucus carota. EMBO J 6:3881–3889Google Scholar
  78. Wasserman M (1992) Cytological evolution of theDrosophila repleta species group. In: Krimbas CB, Powell JR (eds)Drosophila inversion polymorphism. CRC Press, Boca Ratón, pp 455–552Google Scholar
  79. Wetmur JG (1991) DNA probes: applications of the principles of nucleic acid hybridization. Crit Rev Biochem Mot Biol 26: 227–259Google Scholar
  80. Wobus U, Bäumlein H, Bogachev SS, Borisevich IV, Panitz R, Kolesnikov NN (1990) A new transposable element inChironomus thummi. Mol Gen Genet 222:311–316Google Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  • Ignacio Marín
    • 1
  • Antonio Fontdevila
    • 1
  1. 1.Departamento de Genética y MicrobiologiaUniversidad Autónoma de BarcelonaBarcelonaSpain

Personalised recommendations