Abstract
Genomic imprinting is a process that marks DNA, causing a change in gene or chromosome behavior, depending on the sex of the transmitting parent. In mammals, most examples of genomic imprinting affect the transcription of individual or small clusters of genes whereas in insects, genomic imprinting tends to silence entire chromosomes. This has been interpreted as evidence of independent evolutionary origins for imprinting. To investigate how these types of imprinting are related, we performed a phenotypic, molecular, and cytological analysis of an imprinted chromosome in Drosophila melanogaster. Analysis of this chromosome reveals that the imprint results in transcriptional silencing. Yet, the domain of transcriptional silencing is very large, extending at least 1.2 Mb and encompassing over 100 genes, and is associated with decreased somatic polytenization of the entire chromosome. We propose that repression of somatic replication in polytenized cells, as a secondary response to the imprint, acts to extend the size of the imprinted domain to an entire chromosome. Thus, imprinting in Drosophila has properties of both typical mammalian and insect imprinting which suggests that genomic imprinting in Drosophila and mammals is not fundamentally different; imprinting is manifest as transcriptional silencing of a few genes or silencing of an entire chromosome depending on secondary processes such as differences in gene density and polytenization.
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Aagaard L, Laible G, Selenko P, Schmid M, Dorn R, Schotta G, Kuhfittig S, Wolf A, Lebersorger A, Singh P, Reuter G, Jenuwein T (1999) Functional mammalian homologues of the Drosophila PEV-modifier Su(var)3–9 encode centromere-associated proteins which complex with the heterochromatin component M31. EMBO J 18:1923–1938
Alleman M, Doctor J (2000) Genomic imprinting in plants: observations and evolutionary implications. Plant Mol Biol 43:147–161
Bean CJ, Schaner CE, Kelly WG (2004) Meiotic pairing and imprinted X chromatin assembly in Caenorhabditis elegans. Nat Genet 36:100–105
Bongiorni S, Prantera G (2003) Imprinted facultative heterochromatization in mealybugs. Genetica 117:271–279
Bultman S, Magnuson T (2000) Molecular and genetic analysis of the mouse homolog of the Drosophila suppressor of position-effect variegation 3–9 gene. Mamm Genome 11:251–254
Crosby MA, Goodman JL, Strelets VB, Zhang P, Gelbart WM, FlyBase Consortium (2007) FlyBase: genomes by the dozen. Nucleic Acids Res 35:D486–D491
de la Casa-Esperon E, Sapienza C (2003) Natural selection and the evolution of genome imprinting. Annu Rev Genet 37:349–370
Delaval K, Feil R (2004) Epigenetic regulation of mammalian genomic imprinting. Curr Opin Genet Dev 14:188–195
Demakova OV, Belyaeva ES (1988) Effect of mating direction on the position-effect variegation of T(1;2)dor var7 in D. melanogaster. Dros Info Serv 67:19–20
Ebert A, Schotta G, Lein S, Kubicek S, Krauss V, Jenuwein T, Reuter G (2004) Su(var) genes regulate the balance between euchromatin and heterochromatin in Drosophila. Genes Dev 18:2973–2983
Erhardt S, Lyko F, Ainscough JF, Surani MA, Paro R (2003) Polycomb-group proteins are involved in silencing processes caused by a transgenic element from the murine imprinted H19/Igf2 region in Drosophila. Dev Genes Evol 213:336–344
Feil R, Berger F (2007) Convergent evolution of genomic imprinting in plants and mammals. Trends Genet 23:192–199
Feinberg AP (2007) Phenotypic plasticity and the epigenetics of human disease. Nature 447:433–440
Fitch KR, Yasuda GK, Owens KN, Wakimoto BT (1998) Paternal effects in Drosophila: implications for mechanisms of early development. Curr Topics Dev Biol 38:1–34
Goday C, Esteban MR (2001) Chromosome elimination in sciarid flies. Bioessays 23:242–250
Grewal SIS, Elgin SCR (2007) Transcription and RNA interference in the formation of heterochromatin. Nature 447:399–406
Hardy RW, Lindsley DL, Livak KJ, Lewis B, Siversten AL, Joslyn GL, Edwards J, Bonaccorsi S (1984) Cytogenetic analysis of a segment of the Y chromosome of Drosophila melanogaster. Genetics 107:591–610
Hoskins RA, Smith CD, Carlson JW, de Carvalho AB, Halpern A, Kaminker JS, Kennedy C, Mungall CJ, Sullivan BA, Sutton GG, Yasuhara JC, Wakimoto BT, Myers EW, Celniker SE, Rubin GM, Karpen GH (2002) Heterochromatic sequences in a Drosophila whole-genome shotgun assembly. Genome Biol 3:research0085
Hurst LD, McVean GT (1998) Do we understand the evolution of genomic imprinting? Curr Opin Genet Dev 8:701–708
Joanis V, Lloyd VK (2002) Genomic imprinting in Drosophila is maintained by the products of Suppressor of variegation and trithorax group, but not Polycomb group, genes. Mol Genet Genomics 268:103–112
Karpen GH, Spradling AC (1990) Reduced DNA polytenization of a minichromosome region undergoing position-effect variegation in Drosophila. Cell 63:97–107
Kennison J (2000) Preparation and analysis of polytene chromosomes. In: Sullivan W, Ashburner M, Hawley R (eds) Drosophila protocols. Cold Spring Harbor Laboratory, Cold Spring Harbor New York, pp 111–117
Killian JK, Nolan CM, Stewart N, Munday BL, Andersen NA, Nicol S, Jirtle RL (2001) Monotreme IGF2 expression and ancestral origin of genomic imprinting. J Exp Zool 291:205–212
Lippman Z, Martienssen R (2004) The role of RNA interference in heterochromatic silencing. Nature 431:364–370
Lloyd V (2000) Parental imprinting in Drosophila. Genetica 109:35–44
Lloyd VK, Sinclair DA, Grigliatti TA (1999a) Genomic imprinting and position-effect variegation in Drosophila melanogaster. Genetics 151:1503–1516
Lloyd VK, Sinclair DA, Wennberg R, Warner TS, Honda BM, Grigliatti TA (1999b) A genetic and molecular characterization of the garnet gene of Drosophila melanogaster. Genome 42:1–11
Loppin B, Bonnefoy E, Anselme C, Laurencon A, Karr TL, Couble P (2005) The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. Nature 437:1386–1390
Lyko F, Paro R (1999) Chromosomal elements conferring epigenetic inheritance. Bioessays 21:824–832
Lyko F, Brenton JK, Surani MA, Paro R (1997) An imprinting element from the mouse H19 locus functions as a silencer in Drosophila. Nature Genet 16:171–173
Lyko F, Bruiting K, Horsthemke B, Paro R (1998) Identification of a silencing element in human 15q11–q13 imprinting center by using transgenic Drosophila. Proc Nat Acad Sci 95:1698–1702
Martin CC, McGowan R (1995a) Parent-of-origin specific effects on the methylation of a transgene in the zebrafish, Danio rerio. Dev Genet 17:233–239
Martin CC, McGowan R (1995b) Genotype-specific modifiers of transgene methylation and expression in the zebrafish, Danio rerio. Genet Res 65:21–28
McGrath J, Solter D (1984) Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37:179–183
Morison IM, Ramsay JP, Spencer HG (2005) A census of mammalian imprinting. Trends Genet 21:457–65
Nagl W (1978) Occurrence and characterization of endopolyploid nuclei. In: Nagl W (ed) Endopolyploidy and polyteny in differentiation and evolution. North-Holland, Amsterdam, pp 13–65
Normark BB (2003) The evolution of alternate genetic systems in insects. Annu Rev Entomol 48:397–423
Norwood LE, Grade SK, Cryderman DE, Hines KA, Furiasse N, Toro R, Li Y, Dhasarathy A, Kladde MP, Hendrix MJ, Kirschmann DA, Wallrath LL (2004) Conserved properties of HP1(Hsalpha). Gene 336:37–46
Pardo-Manuel de Villena F, de la Casa-Esperon E, Sapienza C (2000) Natural selection and the function of genome imprinting: beyond the silenced minority. Trends Genet 16:573–579
Pfaffl MW, Horgan GW, Dempfle L (2002) Relative Expression Software Tool (REST©) for group wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:E36
Prokofyeva-Belgovskaya AA (1947) Heterochromatization as a change of chromosome cycle. J Genet 48:80–98
Ramakers C, Ruijter JM, Deprez RH, Moorman AF (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339:62–66
Schotta G, Ebert A, Krauss V, Fischer A, Hoffmann J, Rea S, Jenuwein T, Dorn R, Reuter G (2002) Central role of Drosophila SU(VAR)3–9 in histone H3-K9 methylation and heterochromatic gene silencing. EMBO J 21:1121–1131
Sharman GB (1971) Late DNA replication in the paternally derived X chromosome of female kangaroos. Nature 230:231–232
Singh PB (1994) Molecular mechanisms of cellular determination: their relation to chromatin structure and parental imprinting. J Cell Sci 107:2653–2668
Spofford J (1961) Parental control of position-effect variegation. II. Effect of sex of parent contributing white-mottled rearrangement in Drosophila melanogaster. Genetics 46:1151–1167
Surani MA, Barton SC (1983) Development of gynogenetic eggs in the mouse: implications for parthenogenetic embryos. Science 222:1034–1036
Takagi N, Sasaki M (1975) Preferential inactivation of the paternally derived X chromosome in the extra embryonic membranes of the mouse. Nature 256:640–642
Tourte Y, Kuligowski-Andres J, Barbier-Ramond C (1980) Different behavior of maternal and paternal genomes during embryogenesis in the fern, Marsilea. Eur J Cell Biol 21:28–36
Valenzuela L, Kamakaka RT (2006) Chromatin insulators. Annu Rev Genet 40:107–138
Verona RI, Mann MR, Bartolomei MS (2003) Genomic imprinting: intricacies of epigenetic regulation in clusters. Annu Rev Cell Dev Biol 19:237–259
Wreggett KA, Hill F, James PS, Hutchings A, Butcher GW, Singh PB (1994) A mammalian homologue of Drosophila heterochromatin protein 1 (HP1) is a component of constitutive heterochromatin. Cytogenet Cell Genet 66:99–103
Acknowledgements
We thank S. Scovil, L. McEachern, D. Kent, K. Fitzpatrick, and D. Sinclair for discussion and the Bloomington Stock Center for stocks. This work was funded by a Natural Sciences and Engineering Research Council grant to VKL.
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Anaka, M., Lynn, A., McGinn, P. et al. Genomic Imprinting in Drosophila has properties of both mammalian and insect imprinting. Dev Genes Evol 219, 59–66 (2009). https://doi.org/10.1007/s00427-008-0267-3
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DOI: https://doi.org/10.1007/s00427-008-0267-3