Skip to main content
Log in

Parental Imprinting in Drosophila

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Genetic imprinting is a form of epigenetic silencing. But with a twist. The twist is that while imprinting results in the silencing of genes, chromosome regions or entire chromosome sets, this silencing occurs only after transmission of the imprinted region by one sex of parent. Thus genetic imprinting reflects intertwined levels of epigenetic and developmental modulation of gene expression. Imprinting has been well documented and studied in Drosophila, however, these studies have remained largely unknown due to nothing more significant than differences in terminology. Imprinting in Drosophilais invariably associated with heterochromatin or regions with unusual chromatin structure. The imprint appears to spread from imprinted centers that reside within heterochromatin and these are, seemingly, the only regions that are normally imprinted in Drosophila. This is significant as it implies that while imprinting occurs in Drosophila, it is generally without phenotypic consequence. Hence the evolution of imprinting, at least in Drosophila, is unlikely to be driven by the function of specific imprinted genes. Thus, the study of imprinting in Drosophilahas the potential to illuminate the mechanism and biological function of imprinting, and challenge models based solely on imprinting of mammalian genes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Allen, N.D., D.G. Cran, S.C. Barton, S. Hettle, W. Reik & M.A. Surani, 1988. Transgenes as probes for active chromosomal domains in mouse development. Nature 333: 852–855.

    Article  PubMed  CAS  Google Scholar 

  • Baker, W.K., 1963. Genetic control of pigment differentiation in somatic cells. Am. Zool. 3: 57–69.

    Google Scholar 

  • Barlow, D.P., 1994. Imprinting: a gamete's point of view. Trends Genet. 10: 194–199.

    Article  PubMed  CAS  Google Scholar 

  • Bartolomei, M.S., A.C. Webber, M.E. Brunkow & S. M. Tilghman, 1993. Epigenetic mechanisms underlying the imprinting of the mouse H19gene. Genes Devel. 7: 1663–1673.

    PubMed  CAS  Google Scholar 

  • Beatty, R.A., 1957. Parthenogenesis and Polyploidy in Mammalian Development. Cambridge University Press, Cambridge.

    Google Scholar 

  • Berg, C.A. & A.C. Spradling, 1991. Studies on the rate and sitespecificity of P-element transposition. Genetics 127: 515–524.

    PubMed  CAS  Google Scholar 

  • Bishop, C.P. & C.M. Jackson, 1996. Genomic imprinting of chromatin in Drosophila melanogaster. Genetica 97: 33–37.

    Article  PubMed  CAS  Google Scholar 

  • Brannan, C.I. & M.S. Bartolomei, 1999. Mechanisms of genomic imprinting. Curr. Op. Gen. Dev. 9: 164–170.

    Article  CAS  Google Scholar 

  • Bruiting, K., S. Saitoh, S. Gross, B. Dittrich, S. Schwartz, R.D. Nicholls & B. Horsthhemke, 1995. Inherited microdeletions in the Angelman and Prader-Willi syndromes define an imprinting center on human chromosome 15. Nat. Genet. 9: 395–400.

    Article  Google Scholar 

  • Brun, L.O., P. Borsa, V. Gaudichon, J.J. Stuart, K. Aronstein, C. Coustau & R.H. FfrenchConstant, 1995. Functional haploidy. Nature 374: 506.

    Article  CAS  Google Scholar 

  • Carroll, L., 1872. Through the Looking Glass. Random House, NY, USA.

    Google Scholar 

  • Cavalli, G. & R. Paro, 1998. The Drosophila Fab-7chromosomal element conveys epigenetic inheritance during mitosis and meiosis. Cell 93: 505–518.

    Article  PubMed  CAS  Google Scholar 

  • Chandra, H.S. & S.W. Brown, 1975. Chromosome imprinting and the mammalian X chromosome. Nature 253: 165–168.

    Article  PubMed  CAS  Google Scholar 

  • Cockett, N.E., S.P. Jackson, T.L. Shay, F. Farnir, S. Berghmans, G.D. Snowder, D.M. Nielsen & M. Georges, 1996. Polar overdominance at the ovine callipygelocus. Science 273: 236–238.

    PubMed  CAS  Google Scholar 

  • Cohen, J., 1962. Position-effect variegation at several closely linked loci in Drosophila melanogaster. Genetics 47: 647–659.

    CAS  PubMed  Google Scholar 

  • Corley-Smith, G.E., C.J. Lim & B.P. Brandhorst, 1996. Production of androgenic zebrafish (Danio rerio). Genetics 142: 1265–1276.

    PubMed  CAS  Google Scholar 

  • Crouse, H.V., 1960. The controlling element in sex chromosome behavior in Sciara. Genetics 45: 1429–1443.

    PubMed  CAS  Google Scholar 

  • Demakova, O.V. & E.S. Belyaeva, 1988. Effect of mating direction on the position effect variegation of T(1;2)dor var7in Drosophila melanogaster. Dros. Info. Service. 67: 19–20.

    Google Scholar 

  • Dorn, R., V. Krauss, G. Reuter & H. Saumweber, 1993. The enhancer of position-effect variegation of Drosophila, E(var)3-93D, codes for a chromatin protein containing a conserved domain common to several transcriptional regulators. Proc. Natl. Acad. Sci. USA 90: 11376–11380.

    Article  PubMed  CAS  Google Scholar 

  • Ferguson-Smith, A.C., H. Sasaki, B.M. Cattanach & M. A. Surani, 1993. Parental-origin-specific epigenetic modification of the mouse H19gene. Nature 362: 751–755.

    Article  PubMed  CAS  Google Scholar 

  • Flybase: http://flybase.bio.indiana.edu.

  • Frevel, M.A.E., J.J. Hornberg & A.E. Reeve, 1999. A potential imprint control element. Identification of a conserved 42 bp sequence upstream of H19. Trends Genet. 15: 216–218.

    Article  PubMed  CAS  Google Scholar 

  • Fuyama, Y., 1984. Gynogenesis in Drosophila melanogaster. Jpn. J. Genetics 59: 91–96.

    Google Scholar 

  • Golic, K.G., M.M. Golic & S. Pimpinelli, 1998. Imprinted control of gene activity in Drosophila. Curr. Biol. 8: 1273–1276.

    Article  PubMed  CAS  Google Scholar 

  • Hall, J.G., 1990. Genomic Imprinting: Review and relevance to human diseases. Am. J. Hum. Genet. 46: 857–873.

    PubMed  CAS  Google Scholar 

  • Hark, A.T. & S.M. Tilghman, 1998. Chromatin conformation of the H19epigenetic mark. Hum. Mol. Genet. 7: 1979–1985.

    Article  PubMed  CAS  Google Scholar 

  • Hess, O., 1970. Independence between modification of genetic position effects and formation of lampbrush loops by the Y chromosome of Drosophila hydei. Mol. Gen. Genet. 107: 224–242.

    Article  Google Scholar 

  • Hessler, A.Y., 1961. A study of parental modification of variegated position effects. Genetics 46: 463–484.

    PubMed  CAS  Google Scholar 

  • Karpen, G.H. & A.C. Spradling, 1990. Reduced DNA polytenization of a minichromosome region undergoing position-effect variegation in Drosophila. Cell63: 97–107.

    Article  PubMed  CAS  Google Scholar 

  • Kermicle, J.L. & M. Alleman, 1990. Gametic imprinting in maize in relation to the angiosperm life cycle. pp. 9–14, in Genomic Imprinting (Development-supplement 1990) edited by M. Monk and A. Surani. Company of Biologists Ltd., Cambridge.

    Google Scholar 

  • Khesin, R.B. & V.N. Barshkirov, 1978. Maternal influence upon the V-type gene position effect in Drosophila melanogaster. Mol. Gen. Genet. 163: 327–334.

    Article  PubMed  CAS  Google Scholar 

  • Koide, T., J. Ainscough, M. Wijgerde & M.A. Surani, 1994. Comparative analysis of Igf-2/H19 imprinted domain: Identification of a highly conserved intergenic DNase I hypersensitive region. Genomics 24: 1–8.

    Article  PubMed  CAS  Google Scholar 

  • Komma, D.J. & S.A. Endow, 1995. Haploidy and androgenesis in Drosophila. Proc. Natl. Acad. Sci 92: 11884–11888.

    Article  PubMed  CAS  Google Scholar 

  • Kuhn, B.T. & B. Packert, 1988. Paternal imprinting of inversion Uab 1causes homeotic transformations in Drosophila. Genetics 118: 103–107.

    PubMed  CAS  Google Scholar 

  • Lindsley, D.L. & G.G. Zimm, 1992. The genome of Drosophila melanogaster. Academic Press, NY.

    Google Scholar 

  • Lloyd, V.K., D.A. Sinclair & T.A. Grigliatti, 1999. Genomic imprinting and position-effect variegation in Drosophila melanogaster. Genetics 151: 1503–1516.

    Google Scholar 

  • Lock, L.F., N. Takugi & G.R. Martin, 1987. Methylation of the Hprtgene in the inactive X occurs after chromosome inactivation. Cell 48: 39–46.

    Article  PubMed  CAS  Google Scholar 

  • Lorenz K., 1952. King Solomon's ring. Crowel, New York, USA.

    Google Scholar 

  • Lyko, F., J.K. Brenton, M.A. Surani & R. Paro, 1997. An imprinting element from the mouse H19locus functions as a silencer in Drosophila. Nat. Genet. 16: 171–173.

    Article  PubMed  CAS  Google Scholar 

  • Lyko, F., K. Bruiting, B. Horsthemke & R. Paro, 1998. Identification of a silencing element in human 15q11-q13 imprinting center by using transgenic Drosophila. Proc. Natl. Acad. Sci. 95: 1698–1702.

    Article  PubMed  CAS  Google Scholar 

  • Martin, C.C. & R. McGowan, 1995a. Genotype-specific modifiers of transgene methylation and expression in the zebrafish, Danio rerio. Genet. Res. 65: 21–28.

    Article  PubMed  CAS  Google Scholar 

  • Martin, C.C. & R. McGowan, 1995b. Parent-of-origin specific effects on the methylation of a transgene in the zebrafish, Danio rerio. Dev. Genet. 17: 233–239.

    Article  CAS  Google Scholar 

  • Mihaly, J., I. Hogga, S. Barges, M. Galloni, R.K. Mishra, K. Hagstrom, M. Muller, P. Schedl, L. Sipos, J. Gauszi, H. Gyorkovics & F. Karch, 1998. Chromatin domain boundaries in the Bithorax complex. Cell Mol. Life Sci. 54: 60–70.

    Article  PubMed  CAS  Google Scholar 

  • Moore, T. & D. Haig, 1991. Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet. 7: 45–49.

    PubMed  CAS  Google Scholar 

  • Monk, M. & M. Grant, 1990. Preferential X-chromosome inactivation, DNA methylation and imprinting, pp. 55–62 in Genomic Imprinting (Development-supplement 1990) edited by M. Monk & A. Surani. Company of Biologists Ltd., Cambridge.

    Google Scholar 

  • Muller, H.J., 1958. An androgenic homozygous male. Dros. Info. Service 61: 215.

    Google Scholar 

  • Nicholls, R.D., S. Saitoh & B. Horsthemke, 1998. Imprinting in Prader-Willi and Angelman syndromes. Trends Genet. 14: 194– 200.

    Google Scholar 

  • Noujdin, N.I., 1935. (An investigation of an unstable chromosome in Drosophila melanogasterand the mosaicism caused by it). Zoologishcheski Zh. 14: 317–352.

    Google Scholar 

  • Noujdin, N.I., 1944. (The regularities of the heterochromatin influence on mosaicism. The hypothesis of the structural homozygosity and heterozygosity). J. Gen. Biol. 5: 357–388.

    Google Scholar 

  • Noujdin, N.I., 1946. (Mosaics and its manifestation). Bull. de l'academie des sci. de l'urss. Serie biologique/Izvesti i a Akademii nauk SSSR. Seri i a biologicheska i a. 5: 357–388; 5: 519–545.

  • Nur, U., 1970. Translocations between eu-and heterochromatic chromosome, and spermatocytes lacking a heterochromatic set in male mealy bugs. Chromosoma 29: 42–61.

    Article  PubMed  CAS  Google Scholar 

  • Nur, U., 1990. Heterochromatinization and euchromatinization of whole genomes in scale insects (Coccoidea: Homoptera). pp. 29–34 in Genomic Imprinting (Development-supplement 1990) edited by M. Monk and A. Surani. Company of Biologists Ltd., Cambridge.

    Google Scholar 

  • Nur, U., J.H. Werren, D.G. Eichbrush, W.D. Burke & T.H. Eichbush, 1988. A 'selfish’ B chromosome that enhances its transmission by eliminating the paternal genomic. Science 240: 521–514.

    Google Scholar 

  • Patterson, G.I., C.J. Thorpe & V.L. Chandler, 1993. Paramutation, an allelic interaction, is associated with a stable and heritable reduction of transcription of the maize bregulatory gene. Genetics 135: 881–894.

    PubMed  CAS  Google Scholar 

  • Prokofyeva-Belgovskaya, A.A., 1947. Heterochromatinization as a change of chromosome cycle. J. Genetics 48: 80–98.

    Article  Google Scholar 

  • Sapienza, C., 1989. Genome imprinting and dominance modification. Ann. NY. Acad. Sci. 564: 24–38.

    PubMed  CAS  Google Scholar 

  • Sasaki, H., P.A. Jones, J.R. Chaillet, A.C. Ferguson-Smith, S.C. Barton, W. Reik & M.A. Surani, 1992. Parental imprinting: Potentially active chromatin of the repressed maternal allele of the mouse insulin-like growth factor II (Igf2) gene. Genes. Dev. 6: 1843–1856.

    PubMed  CAS  Google Scholar 

  • Sharman, G.B., 1971. Late DNA replication in the paternally derived X chromosome of female kangaroos. Nature 230: 231–232.

    Article  PubMed  CAS  Google Scholar 

  • Singh, P.B., 1994. Molecular mechanisms of cellular determination: their relation to chromatin structure and parental imprinting. J. Cell Sci. 107: 2653–2668.

    PubMed  CAS  Google Scholar 

  • Spofford, J.B., 1959. Parental control of position-effect variegation: I. Parental heterochromatin and expression of the whitelocus in compound-X Drosophila melanogaster. Proc. Natl. Acad. Sci. 45: 1003–1007.

    Article  PubMed  CAS  Google Scholar 

  • Spofford, J.B., 1961. Parental control of position-effect variegation. II. Effect of sex of parent contributing white-mottled rearrangement in Drosophila melanogaster. Genetics 46: 1151–1167.

    PubMed  CAS  Google Scholar 

  • Spofford, J.B., 1967. Single-locus modification of position-effect variegation in Drosophila melanogaster. 1. white variegation. Genetics 57: 751–766.

    PubMed  CAS  Google Scholar 

  • Streisinger, G., C. Walker, N. Dower, D. Knauber & F. Singer, 1981. Production of clones of homozygous diploid zebrafish (Brachydanio rerio). Nature 281: 293–296.

    Article  Google Scholar 

  • Surani, M.A., 1998. Imprinting and the initiation of gene silencing in the germ line. Cell 93: 309–312.

    Article  PubMed  CAS  Google Scholar 

  • Svensson, K., R. Mattsson, T.C. James, P., Wentzel, M. Pilartz, J. MacLaughlin, S.K. Miller, T. Olsson, U.J. Ereiksson & R. Ohlsson, 1998. The paternal allele of the H19gene is progressively silenced during early mouse development: The acetylation status of histones may be involved in the generation of variegation expression patterns. Cell 93: 309–312.

    Article  Google Scholar 

  • Takagi, N. & M. Sasaki, 1975. Preferential inactivation of the paternally derived X chromosome in the extra embryonic membranes of the mouse. Nature 256: 640–642.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lloyd, V. Parental Imprinting in Drosophila. Genetica 109, 35–44 (2000). https://doi.org/10.1023/A:1026592318341

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1026592318341

Navigation