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. 1998 Aug;149(4):1857–1866. doi: 10.1093/genetics/149.4.1857

Repression of hybrid dysgenesis in Drosophila melanogaster by combinations of telomeric P-element reporters and naturally occurring P elements.

S Ronsseray 1, L Marin 1, M Lehmann 1, D Anxolabéhère 1
PMCID: PMC1460266  PMID: 9691042

Abstract

In Drosophila melanogaster, hybrid dysgenesis occurs in the germline of flies produced by crosses between females lacking P elements and males carrying 25-55 P elements. We have previously shown that a complete maternally inherited repression of P transposition in the germline (P cytotype) can be elicited by only two autonomous P elements located at the X chromosome telomere (cytological site 1A). We have tested whether P transgenes at 1A, unable to code for a P-repressor, may contribute to the repression of P elements. Females carrying a P-lacZ transgene at 1A ["P-lacZ(1A)"], crossed with P males, do not repress dysgenic sterility in their progeny. However, these P-lacZ(1A) insertions, maternally or paternally inherited, contribute to P-element repression when they are combined with other regulatory P elements. This combination effect is not seen when the P-lacZ transgene is located in pericentromeric heterochromatin or in euchromatin; however a P-w,ry transgene located at the 3R chromosome telomere exhibits the combination effect. The combination effect with the P-lacZ(1A) transgene is impaired by a mutant Su(var)205 allele known to impair the repression ability of the autonomous P elements at 1A. We hypothesized that the combination effect is due to modification of the chromatin structure or nuclear location of genomic P elements.

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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. 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]
  3. 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]
  4. 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]
  5. 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]
  6. Corish P., Black D. M., Featherston D. W., Merriam J., Dover G. A. Natural repressors of P-induced hybrid dysgenesis in Drosophila melanogaster: a model for repressor evolution. Genet Res. 1996 Apr;67(2):109–121. doi: 10.1017/s0016672300033577. [DOI] [PubMed] [Google Scholar]
  7. Daniels S. B., Clark S. H., Kidwell M. G., Chovnick A. Genetic transformation of Drosophila melanogaster with an autonomous P element: phenotypic and molecular analyses of long-established transformed lines. Genetics. 1987 Apr;115(4):711–723. doi: 10.1093/genetics/115.4.711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. 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]
  10. 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]
  11. Hazelrigg T., Levis R., Rubin G. M. Transformation of white locus DNA in drosophila: dosage compensation, zeste interaction, and position effects. Cell. 1984 Feb;36(2):469–481. doi: 10.1016/0092-8674(84)90240-x. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. 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]
  14. James T. C., Elgin S. C. Identification of a nonhistone chromosomal protein associated with heterochromatin in Drosophila melanogaster and its gene. Mol Cell Biol. 1986 Nov;6(11):3862–3872. doi: 10.1128/mcb.6.11.3862. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Karess R. E., Rubin G. M. Analysis of P transposable element functions in Drosophila. Cell. 1984 Aug;38(1):135–146. doi: 10.1016/0092-8674(84)90534-8. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. 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]
  18. 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]
  19. Lee C. C., Mul Y. M., Rio D. C. The Drosophila P-element KP repressor protein dimerizes and interacts with multiple sites on P-element DNA. Mol Cell Biol. 1996 Oct;16(10):5616–5622. doi: 10.1128/mcb.16.10.5616. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. 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]
  23. 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]
  24. O'Hare K., Driver A., McGrath S., Johnson-Schiltz D. M. Distribution and structure of cloned P elements from the Drosophila melanogaster P strain pi 2. Genet Res. 1992 Aug;60(1):33–41. doi: 10.1017/s0016672300030640. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Pal-Bhadra M., Bhadra U., Birchler J. A. Cosuppression in Drosophila: gene silencing of Alcohol dehydrogenase by white-Adh transgenes is Polycomb dependent. Cell. 1997 Aug 8;90(3):479–490. doi: 10.1016/s0092-8674(00)80508-5. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Preston C. R., Engels W. R. Spread of P transposable elements in inbred lines of Drosophila melanogaster. Prog Nucleic Acid Res Mol Biol. 1989;36:71–85. doi: 10.1016/s0079-6603(08)60162-2. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Rio D. C., Laski F. A., Rubin G. M. Identification and immunochemical analysis of biologically active Drosophila P element transposase. Cell. 1986 Jan 17;44(1):21–32. doi: 10.1016/0092-8674(86)90481-2. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. 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]
  33. 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]
  34. 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]
  35. 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]
  36. 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]
  37. 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]
  38. 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]
  39. Wakimoto B. T., Hearn M. G. The effects of chromosome rearrangements on the expression of heterochromatic genes in chromosome 2L of Drosophila melanogaster. Genetics. 1990 May;125(1):141–154. doi: 10.1093/genetics/125.1.141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. 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]
  41. Wilson C., Pearson R. K., Bellen H. J., O'Kane C. J., Grossniklaus U., Gehring W. J. P-element-mediated enhancer detection: an efficient method for isolating and characterizing developmentally regulated genes in Drosophila. Genes Dev. 1989 Sep;3(9):1301–1313. doi: 10.1101/gad.3.9.1301. [DOI] [PubMed] [Google Scholar]
  42. 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]
  43. Zhang P., Spradling A. C. The Drosophila salivary gland chromocenter contains highly polytenized subdomains of mitotic heterochromatin. Genetics. 1995 Feb;139(2):659–670. doi: 10.1093/genetics/139.2.659. [DOI] [PMC free article] [PubMed] [Google Scholar]

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