Abstract
Position-effect variegation (PEV) is the mosaic expression of a euchromatic gene brought into juxtaposition with heterochromatin. Fourteen different transformedDrosophila melanogaster lines with variegating P-element inserts were used to examine the DNA levels of these transgenes. Insert sites include pericentric, telomeric and fourth chromosome regions. Southern blot analyses showed that the heterochromatichsp26 transgenes are underrepresented 1.3- to 33-fold in polytene tissue relative to the endogenous euchromatichsp26 gene. In contrast, the heterochromatichsp26 transgenes are present in approximately the same copy number as the endogenous euchromatichsp26 gene in diploid tissue. It appears unlikely that DNA loss could account for the lack of gene expression in diploid tissues seen with these examples of PEV.
Similar content being viewed by others
References
AnanievEV, GvozdevVA (1974) Changed pattern of transcription and replication in polytene chromosomes ofDrosophila melanogaster resulting from eu-heterochromatin rearrangement. Chromosoma 45: 173–191
AparicioOM, GottschlingDE (1994) Overcoming telomeric silencing: a trans-activator competes to establish gene expression in a cell cycle-dependent way. Genes Dev 8: 1133–1146
BakerBS, GormanM, MarínI (1994) Dosage compensation inDrosophila. Annu Rev Genet 28: 491–521
BelyaevaES, ZhimulevIF (1991) Cytogenetic and molecular aspects of position effect variegation inDrosophila III. Continuous and discontinuous compaction of chromosomal material as a result of position effect variegation. Chromosoma 100: 453–466
BelyaevaES, DemakovaOV, UmbetovaGH, ZhimulevIF (1993) Cytogenetic and molecular aspects of position-effect variegation inDrosophila melanogaster V. Heterochromatin-associated protein HP1 appears in euchromatic chromosomal regions that are inactivated as a result of position-effect variegation. Chromosoma 102: 583–590
BenderW, SpiererP, HognessDS (1983) chromosomal walking and jumping to isolate DNA from the Ace and rosy loci and the bithorax complex inDrosophila melanogaster. J Mol Biol 168: 17–33
BishopCP (1992) Evidence for intrinsic differences in the formation of chromatin domains inDrosophila melanogaster. Genetics 132: 1063–1069
DanilevskayaO, LofskyA, KurenovaE, PardueM-L (1993) The Y chromosome ofDrosophila melanogaster contains a distinctive subclass of Het-A-related repeats. Genetics 134: 531–543
DiFrancoC, PisanoC, DimitriP, GigliottiS, JunakovicN (1989) Genomic distribution of copia-like transposable elements in somatic tissues and during development ofDrosophila melanogaster. Chromosoma 98: 402–410
FeinbergAP, VogelsteinB (1984) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 137: 266–267
GallJC, CohenEH, PolanML (1971) Repetitive DNA sequences inDrosophila. Chromosoma 33: 319–344
GlaserRL, SpradlingAC (1994) Unusual properties of genomic DNA molecules spanning the euchromatic-heterochromatic junction of aDrosophila minichromosome. Nucleic Acids Res 22: 5068–5075
GlaserRL, KarpenGH, SpardlingAC (1992) Replication forks are not found in aDrosophila minichromosome demonstrating a gradient of polytenization. Chromosoma 102: 15–19
Hartmann-Goldstein IJ, Cowell JK (1976) Position effect on the DNA content of chromosome regions inDrosophila. In: Jones K, Brandham PE (eds) Current chromosome research. Elsevier/North Holland Biomedical Press, pp 43–50
HayashiS, RuddellA, SinclairD, GrigliattiT (1990) Chromosomal structure is altered by mutations that suppress or enhance position effect variegation. Chromosoma 99: 391–400
HazelriggT, LevisR, RubinGM (1984) Transformation of white locus DNA inDrosophila: dosage compensation, zeste interaction, and position effects. Cell 36: 469–481
HeitzE (1928) Das heterochromatin der moose. Jahrb Wiss Bot 69: 381–393
HenikoffS (1981) Position-effect variegation and chromosome structure of a heat shock puff inDrosophila. Chromosoma 83: 381–393
HeuikoffS (1990) Position-effect variegation after 60 years. Trends Genet 6: 422–426
HochmanB (1973) Analysis of a whole chromosome inDrosophila. Cold Spring Harbor Symp Quant Biol 38: 581–589
HoweM, DimitriP, BerlocoM, WakimotoBT (1995) Cis-effects of heterochromatin on heterochromatic and euchromatic gene activity inDrosophila melanogaster. Genetics 140: 1033–1045
KarpenGH (1994) Position-effect variegation and the new biology of heterochromatin. Curr Opin Genet Dev 4: 281–291
KarpenGH, SpradlingAC (1990) Reduced DNA polytenization of a minichromosome region undergoing position-effect variegation inDrosophila. Cell 63: 97–197
KarpenGH, SpradlingAC (1992) Analysis of subtelomeric heterochromatin in theDrosophila minichromosomeDp1187 by single P element insertional mutagenesis. Genetics 132: 737–753
KornherJS, KauffmanSA (1986) Variegated expression of theSgs-4 locus inDrosophila melanogaster. Chromosoma 94: 205–216
KubotaS, Kuro-oM, MizunoS, KohnoS (1993) Germ line-restricted, highly repeated DNA sequences and their chromosomal localization in Japanese hagfish (Eptatretus okinoseamus). Chromosoma 102: 163–173
KyrionGK, LiuC, LustigAJ (1993) RAP1 and telomere structure regulate telomere position effects inSaccharomyces cervisieae. Genes Dev 7: 1146–1159
HairdCD (1973) DNA ofDrosophila chromosomes. Annu Rev Genet 7: 177–204
HewisEB (1950) The phenomenon of position effect. Adv Genet 3: 73–15
LoheAR, HillikerAJ, RobertsPA (1993) Mapping simple repeated DNa sequences in heterochromatin ofDrosophila melanogaster. Genetics 134: 1149–1174
LuQ, WallrathLL, AllanBD, GlaserRL, LisJT, ElginSCR (1992) A promoter sequence containing (CT)n·(GA)n repeats is critical for the formation of the DNase I hypersensitive sites in theDrosophila melanogaster gene. J Mol Biol 225: 985–998
MeyerGF, LippsHJ (1981) The formation of polytene chromosomes during macronuclear development of the hypotrichous ciliateStylonychia mytilus. Chromosoma 82: 309–314
MiklosGLG, CotsellJN (1990) Chromosome structure at interfaces between major chromatin types: alpha- and beta-heterochromatin. BioEssays 12: 1–6
MullerHJ (1930) Types of visible variation induced by X-rays inDrosophila. J Genet 22: 299–335
MullerHJ (1938) The remaking of chromosomes. Collect. Net XIII: 181–195, 198
NaglW (1983) Heterochromatin elimination in the orchidDendrobium. Protoplasma 118: 234–237
NimmoER, CranstonG, AllshireFC (1994) Telomere-associated chromosome breakage in fission yeast results in variegated expression of adjacent genes. EMBO J 13: 3801–3811
PardueM-L (1995)Drosophila telomeres: another way to end it all. In: BlackburnEH, GreiderCW (eds) Telomeres. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, pp. 339–370
PimpinelliS, SantiniG, GattiM (1976) Characterization ofDrosophila heterochromatin. II C- and N-banding. Chromosoma 57: 377–386
RenauldH, AparicioOM, ZierathPD, BilingtonBL, ChhablaniSK, GottschlingDE (1983) Silent domains are assembled continuously from the telomere and are defined by promoter distance and strength, and by SIR3 dosage. Genes Dev 7: 1133–1145
RobertsPA (1972) A possible case of position effect on DNA replication inDrosophila melanogaster. Genetics 72: 607–614
RobertsonHM, PrestonCR, PhillisRW, Johnson-SchultzDM, BenzWK, EnglesWR (1988) A stable genomic source of P element transposase inDrosophila melanogaster. Genetics 118: 461–470
RudkinGT (1969) Non-replicating DNa inDrosophila. Genetics [Suppl] 61: 227–238
RushlowCA, BenderW, ChovnickA (1984) Studies on the mechanism of heterochromatic position effect at the rosy locus ofDrosophila melanogaster. Genetics 108: 603–615
SambrookJ, FritschEF, ManiatisT (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Press Cold Spring Harbor New York
SchultzJ (1936) Variegation inDrosophila and the inert chromosome regions. Proc Natl Acad Sci USA 22: 27–33
ShafferDC, WullerJM, ElginSCR (1994) Raising large quantities ofDrosophila embryos for biochemical experiments. Methods Cell Biol 44: 99–108
SpoffordJB (1976) Iosotion-effect variegation inDrosophila. In: AshburnerM, NovitskiE (eds) The genetics and biology ofDrosophila Vol 1. Academic Press, New York, pp 955–1018
SpradlingAC (1993) Position effect variegation and genomic instability. Cold Spring Harbor Symp Quant Biol LVIII: 585–596
SpradlingAC, KarpenGH (1990) Sixty years of mystery. Genetics 126: 779–784
ToblerH, EtterA, MüllerF (1992) Chromatin diminution in nematode development. Trends Genet 8: 427–432
TraverseKL, PardueML (1989) Studies of He-T DNA sequences in the pericentric regions ofDrosophila chromosomes. Chromosoma 97: 261–271
UmbetovaGH, BelyaevaES, BarichevaEM, ZhimulevIF (1991) Cytogenetic and molecular aspects of position effect variegation inDrosophila melanogaster. IV. Underreplication of chromosomal material as a result of gene inactivation. Chromosoma 101: 56–61
ValgeirsdóttirK, TraverseKL, PardueML (1990). HeT DNA: A family of mosaic repeated sequences specific for heterochromatin inDrosophila melanogaster. Proc Natl Acad Sci USA 87: 7998–8002
WakimotoBT, HearnMG (1990) The effects of chromosome rearrangements on the expression of heterochromatic genes in chromosome 2L ofDrosophila melanogaster. Genetics 125: 141–154
WallrathLL, ElginSCR (1995) Position effect variegation inDrosophila is associated with an altered chromatin structure. Genes Dev 9: 1263–1277
WeilerKS, WakimotoBT (1995) Heterochromatin and gene expression inDrosophila. Annu Rev Genet 29: 577–605
ZhangP, SpradlingAC (1995) TheDrosophila salivary gland chromocenter contains highly polytenized subdomains of mitotic heterochromatin. Genetics 139: 659–667
ZhimulevIF, BelayaevaES, FominaOV, ProtopopovMO, BolshakovVN (1986) Cytogenetic and molecular aspects of position effect variagion inDrosophila melanogaster. I. Morphology and genetic activity of the 2AB region in chromosome rearrangement T(1:2)dorvar7. Chromosoma 94: 492–504
ZhimulevIF, BelyaevaES, BgatovAV, BarichevaEM, VlassovaIE (1988) Cytogenetic and molecular aspects of position effect variegation inDrosophila melanogaster II. Peculiarities of morphology and genetic activity of the 2B region in the T(1;2)dorvar7 chromosome in males. Chromosoma 96: 255–261
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Wallrath, L.L., Guntur, V.P., Rosman, L.E. et al. DNA representation of variegating heterochromatic P-element inserts in diploid and polytene tissues ofDrosophila melanogaster . Chromosoma 104, 519–527 (1996). https://doi.org/10.1007/BF00352116
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00352116