Abstract
In Drosophila, clusters of P transgenes (P-lac-w) display a variegating phenotype for the w marker. In addition, X-ray-induced rearrangements of chromosomes bearing such clusters may lead to enhancement of the variegated phenotype. Since P-lacZ transgenes in subtelomeric heterochromatin have some P-element repression abilities, we tested whether P-lac-w clusters also have the capacity to repress P-element activity in the germline. One cluster (T-1), located on a rearranged chromosome (T2;3) and derived from a line bearing a variegating tandem array of seven P-lac-w elements, partially represses the dysgenic sterility (GD sterility) induced by P elements. This cluster also strongly represses in trans the expression of P-lacZ elements in the germline. This latter suppression shows a maternal effect. Finally, the combination of variegating P-lac-w clusters and a single P-lacZ reporter inserted in subtelomeric heterochromatic sequences at the X chromosome telomere (cytological site 1A) leads to strong repression of dysgenic sterility. These results show that repression of P-induced dysgenic sterility can be elicited in the absence of P elements encoding a polypeptide repressor and that a transgene cluster can repress the expression of a single homologous transgene at a nonallelic position. Implications for models of transposable element silencing are discussed.
Full Text
The Full Text of this article is available as a PDF (512.2 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Aravin A. A., Naumova N. M., Tulin A. V., Vagin V. V., Rozovsky Y. M., Gvozdev V. A. Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline. Curr Biol. 2001 Jul 10;11(13):1017–1027. doi: 10.1016/s0960-9822(01)00299-8. [DOI] [PubMed] [Google Scholar]
- Bier E., Vaessin H., Shepherd S., Lee K., McCall K., Barbel S., Ackerman L., Carretto R., Uemura T., Grell E. Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes Dev. 1989 Sep;3(9):1273–1287. doi: 10.1101/gad.3.9.1273. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- 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]
- 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]
- Dorer D. R., Henikoff S. Expansions of transgene repeats cause heterochromatin formation and gene silencing in Drosophila. Cell. 1994 Jul 1;77(7):993–1002. doi: 10.1016/0092-8674(94)90439-1. [DOI] [PubMed] [Google Scholar]
- Dorer D. R., Henikoff S. Transgene repeat arrays interact with distant heterochromatin and cause silencing in cis and trans. Genetics. 1997 Nov;147(3):1181–1190. doi: 10.1093/genetics/147.3.1181. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Fanti L., Dorer D. R., Berloco M., Henikoff S., Pimpinelli S. Heterochromatin protein 1 binds transgene arrays. Chromosoma. 1998 Nov;107(5):286–292. doi: 10.1007/s004120050310. [DOI] [PubMed] [Google Scholar]
- 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]
- Golubovsky M. D., Konev A. Y., Walter M. F., Biessmann H., Mason J. M. Terminal retrotransposons activate a subtelomeric white transgene at the 2L telomere in Drosophila. Genetics. 2001 Jul;158(3):1111–1123. doi: 10.1093/genetics/158.3.1111. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- Pal-Bhadra M., Bhadra U., Birchler J. A. Cosuppression of nonhomologous transgenes in Drosophila involves mutually related endogenous sequences. Cell. 1999 Oct 1;99(1):35–46. doi: 10.1016/s0092-8674(00)80060-4. [DOI] [PubMed] [Google Scholar]
- 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]
- Robinson D. N., Cooley L. Examination of the function of two kelch proteins generated by stop codon suppression. Development. 1997 Apr;124(7):1405–1417. doi: 10.1242/dev.124.7.1405. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- Slatis H M. A Reconsideration of the Brown-Dominant Position Effect. Genetics. 1955 Mar;40(2):246–251. doi: 10.1093/genetics/40.2.246. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Thummel C. S., Boulet A. M., Lipshitz H. D. Vectors for Drosophila P-element-mediated transformation and tissue culture transfection. Gene. 1988 Dec 30;74(2):445–456. doi: 10.1016/0378-1119(88)90177-1. [DOI] [PubMed] [Google Scholar]
- Voinnet O., Vain P., Angell S., Baulcombe D. C. Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell. 1998 Oct 16;95(2):177–187. doi: 10.1016/s0092-8674(00)81749-3. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]