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. 2002 Dec;162(4):1641–1654. doi: 10.1093/genetics/162.4.1641

Telomeric P elements associated with cytotype regulation of the P transposon family in Drosophila melanogaster.

Jeremy R Stuart 1, Kevin J Haley 1, Douglas Swedzinski 1, Samuel Lockner 1, Paul E Kocian 1, Peter J Merriman 1, Michael J Simmons 1
PMCID: PMC1462367  PMID: 12524339

Abstract

P elements inserted at the left end of the Drosophila X chromosome were isolated genetically from wild-type P strains. Stocks carrying these elements were tested for repression of P-strain-induced gonadal dysgenesis in females and for repression of transposase-catalyzed P-element excision in males and females. Both traits were repressed by stocks carrying either complete or incomplete P elements inserted near the telomere of the X chromosome in cytological region 1A, but not by stocks carrying only nontelomeric X-linked P elements. All three of the telomeric P elements that were analyzed at the molecular level were inserted in one of the 1.8-kb telomere-associated sequence (TAS) repeats near the end of the X chromosome. Stocks with these telomeric P elements strongly repressed P-element excision induced in the male germline by a P strain or by the transposase-producing transgenes H(hsp/CP)2, H(hsp/CP)3, a combination of these two transgenes, and P(ry(+), delta2-3)99B. For H(hsp/CP)2 and P(ry(+), delta2-3)99B, the repression was also effective when the flies were subjected to heat-shock treatments. However, these stocks did not repress the somatic transposase activity of P(ry(+), delta2-3)99B. Repression of transposase activity in the germline required maternal transmission of the telomeric P elements themselves. Paternal transmission of these elements, or maternal transmission of the cytoplasm from carriers, both were insufficient to repress transposase activity. Collectively, these findings indicate that the regulatory abilities of telomeric P elements are similar to those of the P cytotype.

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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. 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]
  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. 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]
  6. Engels W. R. Extrachromosomal control of mutability in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1979 Aug;76(8):4011–4015. doi: 10.1073/pnas.76.8.4011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Engels W. R. Invasions of P elements. Genetics. 1997 Jan;145(1):11–15. doi: 10.1093/genetics/145.1.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Engels W. R., Preston C. R., Johnson-Schlitz D. M. Long-range cis preference in DNA homology search over the length of a Drosophila chromosome. Science. 1994 Mar 18;263(5153):1623–1625. doi: 10.1126/science.8128250. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Gloor G. B., Nassif N. A., Johnson-Schlitz D. M., Preston C. R., Engels W. R. Targeted gene replacement in Drosophila via P element-induced gap repair. Science. 1991 Sep 6;253(5024):1110–1117. doi: 10.1126/science.1653452. [DOI] [PubMed] [Google Scholar]
  11. Jackson M. S., Black D. M., Dover G. A. Amplification of KP elements associated with the repression of hybrid dysgenesis in Drosophila melanogaster. Genetics. 1988 Dec;120(4):1003–1013. doi: 10.1093/genetics/120.4.1003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. 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]
  14. 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]
  15. 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]
  16. Kocur G. J., Drier E. A., Simmons M. J. Sterility and hypermutability in the P-M system of hybrid dysgenesis in Drosophila melanogaster. Genetics. 1986 Dec;114(4):1147–1163. doi: 10.1093/genetics/114.4.1147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lander E. S., Linton L. M., Birren B., Nusbaum C., Zody M. C., Baldwin J., Devon K., Dewar K., Doyle M., FitzHugh W. Initial sequencing and analysis of the human genome. Nature. 2001 Feb 15;409(6822):860–921. doi: 10.1038/35057062. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Lee C. C., Beall E. L., Rio D. C. DNA binding by the KP repressor protein inhibits P-element transposase activity in vitro. EMBO J. 1998 Jul 15;17(14):4166–4174. doi: 10.1093/emboj/17.14.4166. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Marin L., Lehmann M., Nouaud D., Izaabel H., Anxolabéhère D., Ronsseray S. P-Element repression in Drosophila melanogaster by a naturally occurring defective telomeric P copy. Genetics. 2000 Aug;155(4):1841–1854. doi: 10.1093/genetics/155.4.1841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Misra S., Rio D. C. Cytotype control of Drosophila P element transposition: the 66 kd protein is a repressor of transposase activity. Cell. 1990 Jul 27;62(2):269–284. doi: 10.1016/0092-8674(90)90365-l. [DOI] [PubMed] [Google Scholar]
  23. Nassif N., Engels W. DNA homology requirements for mitotic gap repair in Drosophila. Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1262–1266. doi: 10.1073/pnas.90.4.1262. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. 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]
  27. 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]
  28. 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]
  29. Roiha H., Rubin G. M., O'Hare K. P element insertions and rearrangements at the singed locus of Drosophila melanogaster. Genetics. 1988 May;119(1):75–83. doi: 10.1093/genetics/119.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. 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]
  32. 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]
  33. Simmons M. J., Bucholz L. M. Transposase titration in Drosophila melanogaster: a model of cytotype in the P-M system of hybrid dysgenesis. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8119–8123. doi: 10.1073/pnas.82.23.8119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Simmons M. J., Raymond J. D., Culbert T. P., Laverty T. R. Analysis of dysgenesis-induced lethal mutations on the X chromosome of a Q strain of Drosophila melanogaster. Genetics. 1984 May;107(1):49–63. doi: 10.1093/genetics/107.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. 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]
  36. Simmons Michael J., Haley Kevin J., Grimes Craig D., Raymond John D., Fong Joseph C. L. Regulation of P-element transposase activity in Drosophila melanogaster by hobo transgenes that contain KP elements. Genetics. 2002 May;161(1):205–215. doi: 10.1093/genetics/161.1.205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Simmons Michael J., Haley Kevin J., Grimes Craig D., Raymond John D., Niemi Jarad B. A hobo transgene that encodes the P-element transposase in Drosophila melanogaster: autoregulation and cytotype control of transposase activity. Genetics. 2002 May;161(1):195–204. doi: 10.1093/genetics/161.1.195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Spradling A. C., Stern D. M., Kiss I., Roote J., Laverty T., Rubin G. M. Gene disruptions using P transposable elements: an integral component of the Drosophila genome project. Proc Natl Acad Sci U S A. 1995 Nov 21;92(24):10824–10830. doi: 10.1073/pnas.92.24.10824. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. 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]
  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]

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