Abstract
P element transposition in Drosophila is controlled by the cytotype regulatory state: in P cytotype, transposition is repressed, whereas in M cytotype, transposition can occur. P cytotype is determined by a combination of maternally inherited factors and chromosomal P elements in the zygote. Transformant strains containing single elements that encoded the 66-kD P element protein zygotically repressed transposition, but did not display the maternal repression characteristic of P cytotype. Upon mobilization to new genomic positions, some of these repressor elements showed significant maternal repression of transposition in genetic assays, involving a true maternal effect. Thus, the genomic position of repressor elements can determine the maternal vs. zygotic inheritance of P cytotype. Immunoblotting experiments indicate that this genomic position effect does not operate solely by controlling the expression level of the 66-kD repressor protein during oogenesis. Likewise, P element derivatives containing the hsp26 maternal regulator sequence expressed high levels of the 66-kD protein during oogenesis, but showed no detectable maternal repression. These data suggest that the location of a repressor element in the genome may determine maternal inheritance of P cytotype by a mechanism involving more than the overall level of expression of the 66-kD protein in the ovary.
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- Bellen H. J., O'Kane C. J., Wilson C., Grossniklaus U., Pearson R. K., Gehring W. J. P-element-mediated enhancer detection: a versatile method to study development in Drosophila. Genes Dev. 1989 Sep;3(9):1288–1300. doi: 10.1101/gad.3.9.1288. [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]
- Bownes M. Preferential insertion of P elements into genes expressed in the germ-line of Drosophila melanogaster. Mol Gen Genet. 1990 Jul;222(2-3):457–460. doi: 10.1007/BF00633856. [DOI] [PubMed] [Google Scholar]
- Case C. C., Simons E. L., Simons R. W. The IS10 transposase mRNA is destabilized during antisense RNA control. EMBO J. 1990 Apr;9(4):1259–1266. doi: 10.1002/j.1460-2075.1990.tb08234.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chain A. C., Zollman S., Tseng J. C., Laski F. A. Identification of a cis-acting sequence required for germ line-specific splicing of the P element ORF2-ORF3 intron. Mol Cell Biol. 1991 Mar;11(3):1538–1546. doi: 10.1128/mcb.11.3.1538. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cheung H. K., Serano T. L., Cohen R. S. Evidence for a highly selective RNA transport system and its role in establishing the dorsoventral axis of the Drosophila egg. Development. 1992 Mar;114(3):653–661. doi: 10.1242/dev.114.3.653. [DOI] [PubMed] [Google Scholar]
- Dalby B., Glover D. M. 3' non-translated sequences in Drosophila cyclin B transcripts direct posterior pole accumulation late in oogenesis and peri-nuclear association in syncytial embryos. Development. 1992 Aug;115(4):989–997. doi: 10.1242/dev.115.4.989. [DOI] [PubMed] [Google Scholar]
- Driever W., Nüsslein-Volhard C. A gradient of bicoid protein in Drosophila embryos. Cell. 1988 Jul 1;54(1):83–93. doi: 10.1016/0092-8674(88)90182-1. [DOI] [PubMed] [Google Scholar]
- Driever W., Siegel V., Nüsslein-Volhard C. Autonomous determination of anterior structures in the early Drosophila embryo by the bicoid morphogen. Development. 1990 Aug;109(4):811–820. doi: 10.1242/dev.109.4.811. [DOI] [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]
- 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]
- Engels W. R., Preston C. R. Hybrid dysgenesis in Drosophila melanogaster: the biology of female and male sterility. Genetics. 1979 May;92(1):161–174. doi: 10.1093/genetics/92.1.161. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Engels W. R. The estimation of mutation rates when premeiotic events are involved. Environ Mutagen. 1979;1(1):37–43. doi: 10.1002/em.2860010110. [DOI] [PubMed] [Google Scholar]
- Frank L. H., Cheung H. K., Cohen R. S. Identification and characterization of Drosophila female germ line transcriptional control elements. Development. 1992 Feb;114(2):481–491. doi: 10.1242/dev.114.2.481. [DOI] [PubMed] [Google Scholar]
- Grossniklaus U., Bellen H. J., Wilson C., Gehring W. J. P-element-mediated enhancer detection applied to the study of oogenesis in Drosophila. Development. 1989 Oct;107(2):189–200. doi: 10.1242/dev.107.2.189. [DOI] [PubMed] [Google Scholar]
- Heath E. M., Simmons M. J. Genetic and molecular analysis of repression in the P-M system of hybrid dysgenesis in Drosophila melanogaster. Genet Res. 1991 Jun;57(3):213–226. doi: 10.1017/s0016672300029360. [DOI] [PubMed] [Google Scholar]
- Hedley M. L., Maniatis T. Sex-specific splicing and polyadenylation of dsx pre-mRNA requires a sequence that binds specifically to tra-2 protein in vitro. Cell. 1991 May 17;65(4):579–586. doi: 10.1016/0092-8674(91)90090-l. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Kaufman P. D., Rio D. C. Germline transformation of Drosophila melanogaster by purified P element transposase. Nucleic Acids Res. 1991 Nov 25;19(22):6336–6336. doi: 10.1093/nar/19.22.6336. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kidwell M. G. Hybrid dysgenesis in Drosophila melanogaster: the genetics of cytotype determination in a neutral strain. Genetics. 1981 Jun;98(2):275–290. doi: 10.1093/genetics/98.2.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kidwell M. G., Novy J. B. Hybrid Dysgenesis in DROSOPHILA MELANOGASTER: Sterility Resulting from Gonadal Dysgenesis in the P-M System. Genetics. 1979 Aug;92(4):1127–1140. doi: 10.1093/genetics/92.4.1127. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Ma C., Simons R. W. The IS10 antisense RNA blocks ribosome binding at the transposase translation initiation site. EMBO J. 1990 Apr;9(4):1267–1274. doi: 10.1002/j.1460-2075.1990.tb08235.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mismer D., Rubin G. M. Analysis of the promoter of the ninaE opsin gene in Drosophila melanogaster. Genetics. 1987 Aug;116(4):565–578. doi: 10.1093/genetics/116.4.565. [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]
- O'Kane C. J., Gehring W. J. Detection in situ of genomic regulatory elements in Drosophila. Proc Natl Acad Sci U S A. 1987 Dec;84(24):9123–9127. doi: 10.1073/pnas.84.24.9123. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Raff J. W., Whitfield W. G., Glover D. M. Two distinct mechanisms localise cyclin B transcripts in syncytial Drosophila embryos. Development. 1990 Dec;110(4):1249–1261. doi: 10.1242/dev.110.4.1249. [DOI] [PubMed] [Google Scholar]
- Rasmusson K. E., Simmons M. J., Raymond J. D., McLarnon C. F. Quantitative effects of P elements on hybrid dysgenesis in Drosophila melanogaster. Genetics. 1990 Mar;124(3):647–662. doi: 10.1093/genetics/124.3.647. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Raymond J. D., Ojala T. A., White J., Simmons M. J. Inheritance of P-element regulation in Drosophila melanogaster. Genet Res. 1991 Jun;57(3):227–234. doi: 10.1017/s0016672300029372. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- 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]
- 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]
- Siebel C. W., Fresco L. D., Rio D. C. The mechanism of somatic inhibition of Drosophila P-element pre-mRNA splicing: multiprotein complexes at an exon pseudo-5' splice site control U1 snRNP binding. Genes Dev. 1992 Aug;6(8):1386–1401. doi: 10.1101/gad.6.8.1386. [DOI] [PubMed] [Google Scholar]
- 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]
- Steller H., Pirrotta V. P transposons controlled by the heat shock promoter. Mol Cell Biol. 1986 May;6(5):1640–1649. doi: 10.1128/mcb.6.5.1640. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Whitfield W. G., González C., Sánchez-Herrero E., Glover D. M. Transcripts of one of two Drosophila cyclin genes become localized in pole cells during embryogenesis. Nature. 1989 Mar 23;338(6213):337–340. doi: 10.1038/338337a0. [DOI] [PubMed] [Google Scholar]