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. 2000 Aug;155(4):1841–1854. doi: 10.1093/genetics/155.4.1841

P-Element repression in Drosophila melanogaster by a naturally occurring defective telomeric P copy.

L Marin 1, M Lehmann 1, D Nouaud 1, H Izaabel 1, D Anxolabéhère 1, S Ronsseray 1
PMCID: PMC1461209  PMID: 10924479

Abstract

In Drosophila melanogaster, hybrid dysgenesis occurs in progeny from crosses between females lacking P elements and males carrying P elements scattered throughout the genome. We have genetically isolated a naturally occurring P insertion at cytological location 1A, from a Tunisian population. The Nasr'Allah-P(1A) element [NA-P(1A)] has a deletion of the first 871 bp including the P promoter. It is flanked at the 3' end by telomeric associated sequences and at the 5' end by a HeT-A element sequence. The NA-P(1A) element strongly represses dysgenic sterility and P transposition. However, when testing P-promoter repression, NA-P(1A) was unable to repress a germinally expressed P-lacZ construct bearing no 5'-homology with it. Conversely, a second P-lacZ construct, in which the fusion with lacZ takes place in exon 3 of P, was successfully repressed by NA-P(1A). This suggests that NA-P(1A) repression involves a homology-dependent component.

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Selected References

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  1. Andrews J. D., Gloor G. B. A role for the KP leucine zipper in regulating P element transposition in Drosophila melanogaster. Genetics. 1995 Oct;141(2):587–594. doi: 10.1093/genetics/141.2.587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Beall E. L., Rio D. C. Drosophila P-element transposase is a novel site-specific endonuclease. Genes Dev. 1997 Aug 15;11(16):2137–2151. doi: 10.1101/gad.11.16.2137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Belenkaya T., Soldatov A., Nabirochkina E., Biryukova I., Birjukova I., Georgieva S., Georgiev P. P-Element insertion at the polyhomeotic gene leads to formation of a novel chimeric protein that negatively regulates yellow gene expression in P-element-induced alleles of Drosophila melanogaster. Genetics. 1998 Oct;150(2):687–697. doi: 10.1093/genetics/150.2.687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Biessmann H., Champion L. E., O'Hair M., Ikenaga K., Kasravi B., Mason J. M. Frequent transpositions of Drosophila melanogaster HeT-A transposable elements to receding chromosome ends. EMBO J. 1992 Dec;11(12):4459–4469. doi: 10.1002/j.1460-2075.1992.tb05547.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Biessmann H., Mason J. M., Ferry K., d'Hulst M., Valgeirsdottir K., Traverse K. L., Pardue M. L. Addition of telomere-associated HeT DNA sequences "heals" broken chromosome ends in Drosophila. Cell. 1990 May 18;61(4):663–673. doi: 10.1016/0092-8674(90)90478-w. [DOI] [PubMed] [Google Scholar]
  6. Biessmann H., Valgeirsdottir K., Lofsky A., Chin C., Ginther B., Levis R. W., Pardue M. L. HeT-A, a transposable element specifically involved in "healing" broken chromosome ends in Drosophila melanogaster. Mol Cell Biol. 1992 Sep;12(9):3910–3918. doi: 10.1128/mcb.12.9.3910. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bingham P. M., Kidwell M. G., Rubin G. M. The molecular basis of P-M hybrid dysgenesis: the role of the P element, a P-strain-specific transposon family. Cell. 1982 Jul;29(3):995–1004. doi: 10.1016/0092-8674(82)90463-9. [DOI] [PubMed] [Google Scholar]
  8. Biémont C., Ronsseray S., Anxolabéhère D., Izaabel H., Gautier C. Localization of P elements, copy number regulation, and cytotype determination in Drosophila melanogaster. Genet Res. 1990 Aug;56(1):3–14. doi: 10.1017/s0016672300028822. [DOI] [PubMed] [Google Scholar]
  9. Black D. M., Jackson M. S., Kidwell M. G., Dover G. A. KP elements repress P-induced hybrid dysgenesis in Drosophila melanogaster. EMBO J. 1987 Dec 20;6(13):4125–4135. doi: 10.1002/j.1460-2075.1987.tb02758.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Coen D., Lemaitre B., Delattre M., Quesneville H., Ronsseray S., Simonelig M., Higuet D., Lehmann M., Montchamp C., Nouaud D. Drosophila P element: transposition, regulation and evolution. Genetica. 1994;93(1-3):61–78. doi: 10.1007/BF01435240. [DOI] [PubMed] [Google Scholar]
  11. Cryderman D. E., Morris E. J., Biessmann H., Elgin S. C., Wallrath L. L. Silencing at Drosophila telomeres: nuclear organization and chromatin structure play critical roles. EMBO J. 1999 Jul 1;18(13):3724–3735. doi: 10.1093/emboj/18.13.3724. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Danilevskaya O. N., Arkhipova I. R., Traverse K. L., Pardue M. L. Promoting in tandem: the promoter for telomere transposon HeT-A and implications for the evolution of retroviral LTRs. Cell. 1997 Mar 7;88(5):647–655. doi: 10.1016/s0092-8674(00)81907-8. [DOI] [PubMed] [Google Scholar]
  13. Danilevskaya O. N., Petrov D. A., Pavlova M. N., Koga A., Kurenova E. V., Hartl D. L. A repetitive DNA element, associated with telomeric sequences in Drosophila melanogaster, contains open reading frames. Chromosoma. 1992 Dec;102(1):32–40. doi: 10.1007/BF00352288. [DOI] [PubMed] [Google Scholar]
  14. Eissenberg J. C., Morris G. D., Reuter G., Hartnett T. The heterochromatin-associated protein HP-1 is an essential protein in Drosophila with dosage-dependent effects on position-effect variegation. Genetics. 1992 Jun;131(2):345–352. doi: 10.1093/genetics/131.2.345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Engels W. R. A trans-acting product needed for P factor transposition in Drosophila. Science. 1984 Dec 7;226(4679):1194–1196. doi: 10.1126/science.6095450. [DOI] [PubMed] [Google Scholar]
  16. Engels W. R., Benz W. K., Preston C. R., Graham P. L., Phillis R. W., Robertson H. M. Somatic effects of P element activity in Drosophila melanogaster: pupal lethality. Genetics. 1987 Dec;117(4):745–757. doi: 10.1093/genetics/117.4.745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Fanti L., Giovinazzo G., Berloco M., Pimpinelli S. The heterochromatin protein 1 prevents telomere fusions in Drosophila. Mol Cell. 1998 Nov;2(5):527–538. doi: 10.1016/s1097-2765(00)80152-5. [DOI] [PubMed] [Google Scholar]
  18. Gloor G. B., Preston C. R., Johnson-Schlitz D. M., Nassif N. A., Phillis R. W., Benz W. K., Robertson H. M., Engels W. R. Type I repressors of P element mobility. Genetics. 1993 Sep;135(1):81–95. doi: 10.1093/genetics/135.1.81. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Higuet D., Anxolabéhère D., Nouaud D. A particular P-element insertion is correlated to the P-induced hybrid dysgenesis repression in Drosophila melanogaster. Genet Res. 1992 Aug;60(1):15–24. doi: 10.1017/s0016672300030627. [DOI] [PubMed] [Google Scholar]
  20. James T. C., Eissenberg J. C., Craig C., Dietrich V., Hobson A., Elgin S. C. Distribution patterns of HP1, a heterochromatin-associated nonhistone chromosomal protein of Drosophila. Eur J Cell Biol. 1989 Oct;50(1):170–180. [PubMed] [Google Scholar]
  21. James T. C., Eissenberg J. C., Craig C., Dietrich V., Hobson A., Elgin S. C. Distribution patterns of HP1, a heterochromatin-associated nonhistone chromosomal protein of Drosophila. Eur J Cell Biol. 1989 Oct;50(1):170–180. [PubMed] [Google Scholar]
  22. Jensen S., Gassama M. P., Heidmann T. Cosuppression of I transposon activity in Drosophila by I-containing sense and antisense transgenes. Genetics. 1999 Dec;153(4):1767–1774. doi: 10.1093/genetics/153.4.1767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Jensen S., Gassama M. P., Heidmann T. Taming of transposable elements by homology-dependent gene silencing. Nat Genet. 1999 Feb;21(2):209–212. doi: 10.1038/5997. [DOI] [PubMed] [Google Scholar]
  24. Karpen G. H., Spradling A. C. Analysis of subtelomeric heterochromatin in the Drosophila minichromosome Dp1187 by single P element insertional mutagenesis. Genetics. 1992 Nov;132(3):737–753. doi: 10.1093/genetics/132.3.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kaufman P. D., Doll R. F., Rio D. C. Drosophila P element transposase recognizes internal P element DNA sequences. Cell. 1989 Oct 20;59(2):359–371. doi: 10.1016/0092-8674(89)90297-3. [DOI] [PubMed] [Google Scholar]
  26. Kidwell M. G. Evolution of hybrid dysgenesis determinants in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1983 Mar;80(6):1655–1659. doi: 10.1073/pnas.80.6.1655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kidwell M. G., Kidwell J. F., Sved J. A. Hybrid Dysgenesis in DROSOPHILA MELANOGASTER: A Syndrome of Aberrant Traits Including Mutation, Sterility and Male Recombination. Genetics. 1977 Aug;86(4):813–833. doi: 10.1093/genetics/86.4.813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Laski F. A., Rio D. C., Rubin G. M. Tissue specificity of Drosophila P element transposition is regulated at the level of mRNA splicing. Cell. 1986 Jan 17;44(1):7–19. doi: 10.1016/0092-8674(86)90480-0. [DOI] [PubMed] [Google Scholar]
  29. Lemaitre B., Coen D. P regulatory products repress in vivo the P promoter activity in P-lacZ fusion genes. Proc Natl Acad Sci U S A. 1991 May 15;88(10):4419–4423. doi: 10.1073/pnas.88.10.4419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lemaitre B., Ronsseray S., Coen D. Maternal repression of the P element promoter in the germline of Drosophila melanogaster: a model for the P cytotype. Genetics. 1993 Sep;135(1):149–160. doi: 10.1093/genetics/135.1.149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Levis R. W., Ganesan R., Houtchens K., Tolar L. A., Sheen F. M. Transposons in place of telomeric repeats at a Drosophila telomere. Cell. 1993 Dec 17;75(6):1083–1093. doi: 10.1016/0092-8674(93)90318-k. [DOI] [PubMed] [Google Scholar]
  32. Matzke A. J., Neuhuber F., Park Y. D., Ambros P. F., Matzke M. A. Homology-dependent gene silencing in transgenic plants: epistatic silencing loci contain multiple copies of methylated transgenes. Mol Gen Genet. 1994 Aug 2;244(3):219–229. doi: 10.1007/BF00285449. [DOI] [PubMed] [Google Scholar]
  33. Miller W. J., Hagemann S., Reiter E., Pinsker W. P-element homologous sequences are tandemly repeated in the genome of Drosophila guanche. Proc Natl Acad Sci U S A. 1992 May 1;89(9):4018–4022. doi: 10.1073/pnas.89.9.4018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Miller W. J., Paricio N., Hagemann S., Martínez-Sebastián M. J., Pinsker W., de Frutos R. Structure and expression of clustered P element homologues in Drosophila subobscura and Drosophila guanche. Gene. 1995 Apr 24;156(2):167–174. doi: 10.1016/0378-1119(95)00013-v. [DOI] [PubMed] [Google Scholar]
  35. Misra S., Buratowski R. M., Ohkawa T., Rio D. C. Cytotype control of Drosophila melanogaster P element transposition: genomic position determines maternal repression. Genetics. 1993 Nov;135(3):785–800. doi: 10.1093/genetics/135.3.785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Mullins M. C., Rio D. C., Rubin G. M. cis-acting DNA sequence requirements for P-element transposition. Genes Dev. 1989 May;3(5):729–738. doi: 10.1101/gad.3.5.729. [DOI] [PubMed] [Google Scholar]
  37. Nouaud D., Anxolabéhère D. P element domestication: a stationary truncated P element may encode a 66-kDa repressor-like protein in the Drosophila montium species subgroup. Mol Biol Evol. 1997 Nov;14(11):1132–1144. doi: 10.1093/oxfordjournals.molbev.a025723. [DOI] [PubMed] [Google Scholar]
  38. Nouaud D., Boëda B., Levy L., Anxolabéhère D. A P element has induced intron formation in Drosophila. Mol Biol Evol. 1999 Nov;16(11):1503–1510. doi: 10.1093/oxfordjournals.molbev.a026062. [DOI] [PubMed] [Google Scholar]
  39. O'Hare K., Rubin G. M. Structures of P transposable elements and their sites of insertion and excision in the Drosophila melanogaster genome. Cell. 1983 Aug;34(1):25–35. doi: 10.1016/0092-8674(83)90133-2. [DOI] [PubMed] [Google Scholar]
  40. Paricio N., Pérez-Alonso M., Martínez-Sebastián M. J., de Frutos R. P sequences of Drosophila subobscura lack exon 3 and may encode a 66 kd repressor-like protein. Nucleic Acids Res. 1991 Dec 25;19(24):6713–6718. doi: 10.1093/nar/19.24.6713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Park Y. D., Papp I., Moscone E. A., Iglesias V. A., Vaucheret H., Matzke A. J., Matzke M. A. Gene silencing mediated by promoter homology occurs at the level of transcription and results in meiotically heritable alterations in methylation and gene activity. Plant J. 1996 Feb;9(2):183–194. doi: 10.1046/j.1365-313x.1996.09020183.x. [DOI] [PubMed] [Google Scholar]
  42. Rasmusson K. E., Raymond J. D., Simmons M. J. Repression of hybrid dysgenesis in Drosophila melanogaster by individual naturally occurring P elements. Genetics. 1993 Mar;133(3):605–622. doi: 10.1093/genetics/133.3.605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Rio D. C. Molecular mechanisms regulating Drosophila P element transposition. Annu Rev Genet. 1990;24:543–578. doi: 10.1146/annurev.ge.24.120190.002551. [DOI] [PubMed] [Google Scholar]
  44. Robertson H. M., Engels W. R. Modified P elements that mimic the P cytotype in Drosophila melanogaster. Genetics. 1989 Dec;123(4):815–824. doi: 10.1093/genetics/123.4.815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Robertson H. M., Preston C. R., Phillis R. W., Johnson-Schlitz D. M., Benz W. K., Engels W. R. A stable genomic source of P element transposase in Drosophila melanogaster. Genetics. 1988 Mar;118(3):461–470. doi: 10.1093/genetics/118.3.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Roche S. E., Rio D. C. Trans-silencing by P elements inserted in subtelomeric heterochromatin involves the Drosophila Polycomb group gene, Enhancer of zeste. Genetics. 1998 Aug;149(4):1839–1855. doi: 10.1093/genetics/149.4.1839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Roche S. E., Schiff M., Rio D. C. P-element repressor autoregulation involves germ-line transcriptional repression and reduction of third intron splicing. Genes Dev. 1995 May 15;9(10):1278–1288. doi: 10.1101/gad.9.10.1278. [DOI] [PubMed] [Google Scholar]
  48. Ronsseray S., Anxolabéhère D., Périquet G. Hybrid dysgenesis in Drosophila melanogaster: influence of temperature on cytotype determination in the P-M system. Mol Gen Genet. 1984;196(1):17–23. doi: 10.1007/BF00334086. [DOI] [PubMed] [Google Scholar]
  49. Ronsseray S., Lehmann M., Anxolabéhère D. Copy number and distribution of P and I mobile elements in Drosophila melanogaster populations. Chromosoma. 1989 Sep;98(3):207–214. doi: 10.1007/BF00329685. [DOI] [PubMed] [Google Scholar]
  50. Ronsseray S., Lehmann M., Anxolabéhère D. The maternally inherited regulation of P elements in Drosophila melanogaster can be elicited by two P copies at cytological site 1A on the X chromosome. Genetics. 1991 Oct;129(2):501–512. doi: 10.1093/genetics/129.2.501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Ronsseray S., Lehmann M., Nouaud D., Anxolabéhère D. P element regulation and X-chromosome subtelomeric heterochromatin in Drosophila melanogaster. Genetica. 1997;100(1-3):95–107. [PubMed] [Google Scholar]
  52. Ronsseray S., Lehmann M., Nouaud D., Anxolabéhère D. The regulatory properties of autonomous subtelomeric P elements are sensitive to a Suppressor of variegation in Drosophila melanogaster. Genetics. 1996 Aug;143(4):1663–1674. doi: 10.1093/genetics/143.4.1663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Ronsseray S., Lemaitre B., Coen D. Maternal inheritance of P cytotype in Drosophila melanogaster: a "pre-P cytotype" is strictly extra-chromosomally transmitted. Mol Gen Genet. 1993 Oct;241(1-2):115–123. doi: 10.1007/BF00280208. [DOI] [PubMed] [Google Scholar]
  54. Ronsseray S., Marin L., Lehmann M., Anxolabéhère D. Repression of hybrid dysgenesis in Drosophila melanogaster by combinations of telomeric P-element reporters and naturally occurring P elements. Genetics. 1998 Aug;149(4):1857–1866. doi: 10.1093/genetics/149.4.1857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Schaefer R. E., Kidwell M. G., Fausto-Sterling A. Hybrid Dysgenesis in DROSOPHILA MELANOGASTER: Morphological and Cytological Studies of Ovarian Dysgenesis. Genetics. 1979 Aug;92(4):1141–1152. doi: 10.1093/genetics/92.4.1141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Sheen F. M., Levis R. W. Transposition of the LINE-like retrotransposon TART to Drosophila chromosome termini. Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12510–12514. doi: 10.1073/pnas.91.26.12510. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Siebel C. W., Rio D. C. Regulated splicing of the Drosophila P transposable element third intron in vitro: somatic repression. Science. 1990 Jun 8;248(4960):1200–1208. doi: 10.1126/science.2161558. [DOI] [PubMed] [Google Scholar]
  58. Simmons G. M. Sterility-mutability correlation. On the correlation between sterility and mutability during P-M hybrid dysgenesis in Drosophila melanogaster. Genet Res. 1987 Aug;50(1):73–76. doi: 10.1017/s0016672300023363. [DOI] [PubMed] [Google Scholar]
  59. Simmons M. J., Raymond J. D., Grimes C. D., Belinco C., Haake B. C., Jordan M., Lund C., Ojala T. A., Papermaster D. Repression of hybrid dysgenesis in Drosophila melanogaster by heat-shock-inducible sense and antisense P-element constructs. Genetics. 1996 Dec;144(4):1529–1544. doi: 10.1093/genetics/144.4.1529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Simmons M. J., Raymond J. D., Rasmusson K. E., Miller L. M., McLarnon C. F., Zunt J. R. Repression of P element-mediated hybrid dysgenesis in Drosophila melanogaster. Genetics. 1990 Mar;124(3):663–676. doi: 10.1093/genetics/124.3.663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Sved J. A. Hybrid dysgenesis in Drosophila melanogaster: evidence from sterility and southern hybridization tests that P cytotype is not maintained in the absence of chromosomal P factors. Genetics. 1987 Jan;115(1):121–127. doi: 10.1093/genetics/115.1.121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Valgeirsdóttir K., Traverse K. L., Pardue M. L. HeT DNA: a family of mosaic repeated sequences specific for heterochromatin in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1990 Oct;87(20):7998–8002. doi: 10.1073/pnas.87.20.7998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Vaslet C. A., O'Connell P., Izquierdo M., Rosbash M. Isolation and mapping of a cloned ribosomal protein gene of Drosophila melanogaster. Nature. 1980 Jun 26;285(5767):674–676. doi: 10.1038/285674a0. [DOI] [PubMed] [Google Scholar]
  64. Wallrath L. L., Elgin S. C. Position effect variegation in Drosophila is associated with an altered chromatin structure. Genes Dev. 1995 May 15;9(10):1263–1277. doi: 10.1101/gad.9.10.1263. [DOI] [PubMed] [Google Scholar]
  65. Wustmann G., Szidonya J., Taubert H., Reuter G. The genetics of position-effect variegation modifying loci in Drosophila melanogaster. Mol Gen Genet. 1989 Jun;217(2-3):520–527. doi: 10.1007/BF02464926. [DOI] [PubMed] [Google Scholar]

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