Abstract
DNA sequences within heterochromatin are often selectively underrepresented during development of polyploid chromosomes, and DNA molecules of altered structure are predicted to form as a consequence of the underrepresentation process. We have identified heterochromatic DNAs of altered structure within sequences that are underrepresented in polyploid cells of Drosophila melanogaster. Specifically, restriction fragments that extend into centric heterochromatin of the minichromosome Dp(1;f)1187 are shortened in polyploid cells of both the ovary and salivary gland but not in the predominantly diploid cells of the embryo or larval imaginal discs and brains. Shortened DNA molecules were also identified within heterochromatic sequences of chromosome III. These results suggest that the structure of heterochromatic DNA is altered as a general consequence of polyploid chromosome formation and that the shortened molecules identified form as a consequence of heterochromatic underrepresentation. Finally, alteration of heterochromatic DNA structure on Dp(1;f)1187 was not correlated with changes in the variegated expression of the yellow gene located on the minichromosome.
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- Ahmad K., Golic K. G. Somatic reversion of chromosomal position effects in Drosophila melanogaster. Genetics. 1996 Oct;144(2):657–670. doi: 10.1093/genetics/144.2.657. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baksa K., Morawietz H., Dombrádi V., Axton M., Taubert H., Szabó G., Török I., Udvardy A., Gyurkovics H., Ször B. Mutations in the protein phosphatase 1 gene at 87B can differentially affect suppression of position-effect variegation and mitosis in Drosophila melanogaster. Genetics. 1993 Sep;135(1):117–125. doi: 10.1093/genetics/135.1.117. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Beermann S. The diminution of Heterochromatic chromosomal segments in Cyclops (Crustacea, Copepoda). Chromosoma. 1977 Apr 20;60(4):297–344. doi: 10.1007/BF00292858. [DOI] [PubMed] [Google Scholar]
- Brewer B. J., Fangman W. L. The localization of replication origins on ARS plasmids in S. cerevisiae. Cell. 1987 Nov 6;51(3):463–471. doi: 10.1016/0092-8674(87)90642-8. [DOI] [PubMed] [Google Scholar]
- Chu G., Vollrath D., Davis R. W. Separation of large DNA molecules by contour-clamped homogeneous electric fields. Science. 1986 Dec 19;234(4783):1582–1585. doi: 10.1126/science.3538420. [DOI] [PubMed] [Google Scholar]
- Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cléard F., Matsarskaia M., Spierer P. The modifier of position-effect variegation Suvar(3)7 of Drosophila: there are two alternative transcripts and seven scattered zinc fingers, each preceded by a tryptophan box. Nucleic Acids Res. 1995 Mar 11;23(5):796–802. doi: 10.1093/nar/23.5.796. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Csink A. K., Henikoff S. Genetic modification of heterochromatic association and nuclear organization in Drosophila. Nature. 1996 Jun 6;381(6582):529–531. doi: 10.1038/381529a0. [DOI] [PubMed] [Google Scholar]
- Dernburg A. F., Broman K. W., Fung J. C., Marshall W. F., Philips J., Agard D. A., Sedat J. W. Perturbation of nuclear architecture by long-distance chromosome interactions. Cell. 1996 May 31;85(5):745–759. doi: 10.1016/s0092-8674(00)81240-4. [DOI] [PubMed] [Google Scholar]
- Dernburg A. F., Sedat J. W., Hawley R. S. Direct evidence of a role for heterochromatin in meiotic chromosome segregation. Cell. 1996 Jul 12;86(1):135–146. doi: 10.1016/s0092-8674(00)80084-7. [DOI] [PubMed] [Google Scholar]
- Elgin S. C. Heterochromatin and gene regulation in Drosophila. Curr Opin Genet Dev. 1996 Apr;6(2):193–202. doi: 10.1016/s0959-437x(96)80050-5. [DOI] [PubMed] [Google Scholar]
- Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
- GEYER-DUSZYNSKA I. Experimental research on chromosome elimination in Cecidomyidae (Diptera). J Exp Zool. 1959 Aug;141:391–447. doi: 10.1002/jez.1401410302. [DOI] [PubMed] [Google Scholar]
- Gall J. G., Cohen E. H., Polan M. L. Reptitive DNA sequences in drosophila. Chromosoma. 1971;33(3):319–344. doi: 10.1007/BF00284948. [DOI] [PubMed] [Google Scholar]
- Garzino V., Pereira A., Laurenti P., Graba Y., Levis R. W., Le Parco Y., Pradel J. Cell lineage-specific expression of modulo, a dose-dependent modifier of variegation in Drosophila. EMBO J. 1992 Dec;11(12):4471–4479. doi: 10.1002/j.1460-2075.1992.tb05548.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Glaser R. L., Spradling A. C. Unusual properties of genomic DNA molecules spanning the euchromatic-heterochromatic junction of a Drosophila minichromosome. Nucleic Acids Res. 1994 Nov 25;22(23):5068–5075. doi: 10.1093/nar/22.23.5068. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hammond M. P., Laird C. D. Chromosome structure and DNA replication in nurse and follicle cells of Drosophila melanogaster. Chromosoma. 1985;91(3-4):267–278. doi: 10.1007/BF00328222. [DOI] [PubMed] [Google Scholar]
- Hammond M. P., Laird C. D. Control of DNA replication and spatial distribution of defined DNA sequences in salivary gland cells of Drosophila melanogaster. Chromosoma. 1985;91(3-4):279–286. doi: 10.1007/BF00328223. [DOI] [PubMed] [Google Scholar]
- Henikoff S. Position-effect variegation and chromosome structure of a heat shock puff in Drosophila. Chromosoma. 1981;83(3):381–393. doi: 10.1007/BF00327360. [DOI] [PubMed] [Google Scholar]
- Karpen G. H., Le M. H., Le H. Centric heterochromatin and the efficiency of achiasmate disjunction in Drosophila female meiosis. Science. 1996 Jul 5;273(5271):118–122. doi: 10.1126/science.273.5271.118. [DOI] [PubMed] [Google Scholar]
- Karpen G. H. Position-effect variegation and the new biology of heterochromatin. Curr Opin Genet Dev. 1994 Apr;4(2):281–291. doi: 10.1016/s0959-437x(05)80055-3. [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]
- Karpen G. H., Spradling A. C. Reduced DNA polytenization of a minichromosome region undergoing position-effect variegation in Drosophila. Cell. 1990 Oct 5;63(1):97–107. doi: 10.1016/0092-8674(90)90291-l. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kellum R., Alberts B. M. Heterochromatin protein 1 is required for correct chromosome segregation in Drosophila embryos. J Cell Sci. 1995 Apr;108(Pt 4):1419–1431. doi: 10.1242/jcs.108.4.1419. [DOI] [PubMed] [Google Scholar]
- LYON M. F. Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature. 1961 Apr 22;190:372–373. doi: 10.1038/190372a0. [DOI] [PubMed] [Google Scholar]
- Laird C. D. DNA of Drosophila chromosomes. Annu Rev Genet. 1973;7:177–204. doi: 10.1146/annurev.ge.07.120173.001141. [DOI] [PubMed] [Google Scholar]
- Le M. H., Duricka D., Karpen G. H. Islands of complex DNA are widespread in Drosophila centric heterochromatin. Genetics. 1995 Sep;141(1):283–303. doi: 10.1093/genetics/141.1.283. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lohe A. R., Hilliker A. J. Return of the H-word (heterochromatin). Curr Opin Genet Dev. 1995 Dec;5(6):746–755. doi: 10.1016/0959-437x(95)80007-r. [DOI] [PubMed] [Google Scholar]
- Lohe A. R., Hilliker A. J., Roberts P. A. Mapping simple repeated DNA sequences in heterochromatin of Drosophila melanogaster. Genetics. 1993 Aug;134(4):1149–1174. doi: 10.1093/genetics/134.4.1149. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lu B. Y., Bishop C. P., Eissenberg J. C. Developmental timing and tissue specificity of heterochromatin-mediated silencing. EMBO J. 1996 Mar 15;15(6):1323–1332. [PMC free article] [PubMed] [Google Scholar]
- Madireddi M. T., Coyne R. S., Smothers J. F., Mickey K. M., Yao M. C., Allis C. D. Pdd1p, a novel chromodomain-containing protein, links heterochromatin assembly and DNA elimination in Tetrahymena. Cell. 1996 Oct 4;87(1):75–84. doi: 10.1016/s0092-8674(00)81324-0. [DOI] [PubMed] [Google Scholar]
- Murphy T. D., Karpen G. H. Interactions between the nod+ kinesin-like gene and extracentromeric sequences are required for transmission of a Drosophila minichromosome. Cell. 1995 Apr 7;81(1):139–148. doi: 10.1016/0092-8674(95)90378-x. [DOI] [PubMed] [Google Scholar]
- Murphy T. D., Karpen G. H. Localization of centromere function in a Drosophila minichromosome. Cell. 1995 Aug 25;82(4):599–609. doi: 10.1016/0092-8674(95)90032-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nakai Y., Kubota S., Goto Y., Ishibashi T., Davison W., Kohno S. Chromosome elimination in three Baltic, south Pacific and north-east Pacific hagfish species. Chromosome Res. 1995 Aug;3(5):321–330. doi: 10.1007/BF00713071. [DOI] [PubMed] [Google Scholar]
- Prescott D. M. Cutting, splicing, reordering, and elimination of DNA sequences in hypotrichous ciliates. Bioessays. 1992 May;14(5):317–324. doi: 10.1002/bies.950140505. [DOI] [PubMed] [Google Scholar]
- Rudkin G. T. Non replicating DNA in Drosophila. Genetics. 1969;61(1 Suppl):227–238. [PubMed] [Google Scholar]
- Sabl J. F., Henikoff S. Copy number and orientation determine the susceptibility of a gene to silencing by nearby heterochromatin in Drosophila. Genetics. 1996 Feb;142(2):447–458. doi: 10.1093/genetics/142.2.447. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smith A. V., Orr-Weaver T. L. The regulation of the cell cycle during Drosophila embryogenesis: the transition to polyteny. Development. 1991 Aug;112(4):997–1008. doi: 10.1242/dev.112.4.997. [DOI] [PubMed] [Google Scholar]
- Spradling A. C. Position effect variegation and genomic instability. Cold Spring Harb Symp Quant Biol. 1993;58:585–596. doi: 10.1101/sqb.1993.058.01.065. [DOI] [PubMed] [Google Scholar]
- Spradling A., Orr-Weaver T. Regulation of DNA replication during Drosophila development. Annu Rev Genet. 1987;21:373–403. doi: 10.1146/annurev.ge.21.120187.002105. [DOI] [PubMed] [Google Scholar]
- Tobler H., Etter A., Müller F. Chromatin diminution in nematode development. Trends Genet. 1992 Dec;8(12):427–432. doi: 10.1016/0168-9525(92)90326-y. [DOI] [PubMed] [Google Scholar]
- Tower J., Karpen G. H., Craig N., Spradling A. C. Preferential transposition of Drosophila P elements to nearby chromosomal sites. Genetics. 1993 Feb;133(2):347–359. doi: 10.1093/genetics/133.2.347. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tschiersch B., Hofmann A., Krauss V., Dorn R., Korge G., Reuter G. The protein encoded by the Drosophila position-effect variegation suppressor gene Su(var)3-9 combines domains of antagonistic regulators of homeotic gene complexes. EMBO J. 1994 Aug 15;13(16):3822–3831. doi: 10.1002/j.1460-2075.1994.tb06693.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wallrath L. L., Guntur V. P., Rosman L. E., Elgin S. C. DNA representation of variegating heterochromatic P-element inserts in diploid and polytene tissues of Drosophila melanogaster. Chromosoma. 1996 Apr;104(7):519–527. doi: 10.1007/BF00352116. [DOI] [PubMed] [Google Scholar]
- Weiler K. S., Wakimoto B. T. Heterochromatin and gene expression in Drosophila. Annu Rev Genet. 1995;29:577–605. doi: 10.1146/annurev.ge.29.120195.003045. [DOI] [PubMed] [Google Scholar]
- Zhang P., Spradling A. C. Efficient and dispersed local P element transposition from Drosophila females. Genetics. 1993 Feb;133(2):361–373. doi: 10.1093/genetics/133.2.361. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhang P., Spradling A. C. Insertional mutagenesis of Drosophila heterochromatin with single P elements. Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3539–3543. doi: 10.1073/pnas.91.9.3539. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]