Skip to main content
Log in

The maize b1 paramutation control region causes epigenetic silencing in Drosophila melanogaster

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Paramutation is an epigenetic process in which a combination of alleles in a heterozygous organism results in a meiotically stable change in expression of one of the alleles. The mechanisms underlying paramutation are being actively investigated, and examples have been described in both plants and mammals, suggesting that it may utilize epigenetic mechanisms that are widespread and evolutionarily conserved. Paramutation at the well-studied maize b1 locus requires a control region consisting of seven 853 bp tandem repeats. To study the conservation of the epigenetic mechanisms underlying seemingly unique epigenetic processes such as paramutation, we created transgenic Drosophila melanogaster carrying the maize b1 control region adjacent to the Drosophila white reporter gene. We show that the b1 tandem repeats cause silencing of the white reporter in Drosophila. A single copy of the tandem repeat sequence is sufficient to cause silencing, and silencing strength increases as the number of tandem repeats increases. Additionally, transgenic lines with the full seven tandem repeats demonstrate evidence of either pairing-sensitive silencing and silencing in trans, or epigenetic activation in trans. These trans-interactions are dependent on repeat number, similar to maize b1 paramutation. Also, as in maize, the tandem repeats are bidirectionally transcribed in Drosophila. These results indicate that the maize b1 tandem repeats function as an epigenetic silencer and mediate trans-interactions in Drosophila, and support the hypothesis that the mechanisms underlying such epigenetic processes are conserved.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Alleman M, Sidorenko L, McGinnis K, Seshadri V, Dorweiler JE, White J, Sikkink K, Chandler VL (2006) An RNA-dependent RNA polymerase is required for paramutation in maize. Nature 442:295–298

    Article  PubMed  CAS  Google Scholar 

  • Arteaga-Vazquez MA, Chandler VL (2010) Paramutation in maize: RNA mediated trans-generational gene silencing. Curr Opin Genet Dev 20:156–163

    Article  PubMed  CAS  Google Scholar 

  • Arteaga-Vazquez M, Sidorenko L, Rabanal FA, Shrivistava R, Nobuta K, Green PJ, Meyers BC, Chandler VL (2010) RNA-mediated trans-communication can establish paramutation at the b1 locus in maize. Proc Natl Acad Sci USA 107:12986–12991

    Article  PubMed  CAS  Google Scholar 

  • Chandler VL (2007) Paramutation: from maize to mice. Cell 128:641–645

    Article  PubMed  CAS  Google Scholar 

  • Chandler V, Alleman M (2008) Paramutation: epigenetic instructions passed across generations. Genetics 178:1839–1844

    PubMed  CAS  Google Scholar 

  • Chandler VL, Stam M (2004) Chromatin conversations: mechanisms and implications of paramutation. Nat Rev Genet 5:532–544

    Article  PubMed  CAS  Google Scholar 

  • Chandler VL, Radicella JP, Robbins TP, Chen J, Turks D (1989) Two regulatory genes of the maize anthocyanin pathway are homologous: isolation of B utilizing R genomic sequences. Plant Cell 1:1175–1183

    PubMed  CAS  Google Scholar 

  • Chandler VL, Eggleston WB, Dorweiler JE (2000) Paramutation in maize. Plant Mol Biol 43:121–145

    Article  PubMed  CAS  Google Scholar 

  • Coe EH (1966) The properties, origin, and mechanism of conversion-type inheritance at the B locus in maize. Genetics 53:1035–1063

    PubMed  CAS  Google Scholar 

  • Dejardin J, Rappailles A, Cuvier O, Grimaud C, Decoville M, Locker D, Cavalli G (2005) Recruitment of Drosophila Polycomb group proteins to chromatin by DSP1. Nature 434:533–538

    Article  PubMed  CAS  Google Scholar 

  • DeVido SK, Kwon D, Brown JL, Kassis JA (2008) The role of Polycomb-group response elements in regulation of engrailed transcription in Drosophila. Development 135:669–676

    Article  PubMed  CAS  Google Scholar 

  • Djupedal I, Ekwall K (2009) Epigenetics: heterochromatin meets RNAi. Cell Res 19:282–295

    Article  PubMed  CAS  Google Scholar 

  • Dorweiler JE, Carey CC, Kubo KM, Hollick JB, Kermicle JL, Chandler VL (2000) Mediator of paramutation1 is required for establishment and maintenance of paramutation at multiple maize loci. Plant Cell 12:2101–2118

    PubMed  CAS  Google Scholar 

  • Drewell RA, Brenton JD, Ainscough JF, Barton SC, Hilton KJ, Arney KL, Dandolo L, Surani MA (2000) Deletion of a silencer element disrupts H19 imprinting independently of a DNA methylation epigenetic switch. Development 127:3419–3428

    PubMed  CAS  Google Scholar 

  • Erhard KF Jr, Stonaker JL, Parkinson SE, Lim JP, Hale CJ, Hollick JB (2009) RNA polymerase IV functions in paramutation in Zea mays. Science 323:1201–1205

    Article  PubMed  CAS  Google Scholar 

  • Fujioka M, Yusibova GL, Zhou J, Jaynes JB (2008) The DNA-binding Polycomb-group protein Pleiohomeotic maintains both active and repressed transcriptional states through a single site. Development 135:4131–4139

    Article  PubMed  CAS  Google Scholar 

  • Golic KG, Lindquist S (1989) The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 59:499–509

    Article  PubMed  CAS  Google Scholar 

  • Haring M, Bader R, Louwers M, Schwabe A, van Driel R, Stam M (2010) The role of DNA methylation, nucleosome occupancy and histone modifications in paramutation. Plant J 63:366–378

    Article  CAS  Google Scholar 

  • Haynes KA, Caudy AA, Collins L, Elgin SC (2006) Element 1360 and RNAi components contribute to HP1-dependent silencing of a pericentric reporter. Curr Biol 16:2222–2227

    Article  PubMed  CAS  Google Scholar 

  • Hollick JB, Chandler VL (1998) Epigenetic allelic states of a maize transcriptional regulatory locus exhibit overdominant gene action. Genetics 150:891–897

    PubMed  CAS  Google Scholar 

  • Hollick JB, Patterson GI, Coe EH Jr, Cone KC, Chandler VL (1995) Allelic interactions heritably alter the activity of a metastable maize pl allele. Genetics 141:709–719

    PubMed  CAS  Google Scholar 

  • Hollick JB, Kermicle JL, Parkinson SE (2005) Rmr6 maintains meiotic inheritance of paramutant states in Zea mays. Genetics 171:725–740

    Article  PubMed  CAS  Google Scholar 

  • Huang AM, Rehm EJ, Rubin GM (2000) Recovery of DNA sequences flanking P-element insertions: inverse PCR and plasmid rescue. In: Sullivan W, Ashburner M, Hawley RS (eds) Drosophila protocols. CSHL, Cold Spring Harbor, pp 429–439

    Google Scholar 

  • Kassis JA (2002) Pairing-sensitive silencing, polycomb group response elements, and transposon homing in Drosophila. Adv Genet 46:421–438

    Article  PubMed  CAS  Google Scholar 

  • Khesin RB, Leibovitch BA (1978) Influence of deficiency of the histone gene-containing 38B–40 region on X-chromosome template activity and the white gene position effect variegation in Drosophila melanogaster. Mol Gen Genet 162:323–328

    Article  PubMed  CAS  Google Scholar 

  • Kurenova E, Champion L, Biessmann H, Mason JM (1998) Directional gene silencing induced by a complex subtelomeric satellite from Drosophila. Chromosoma 107:311–320

    Article  PubMed  CAS  Google Scholar 

  • Louwers M, Bader R, Haring M, van Driel R, de Laat W, Stam M (2009) Tissue- and expression level-specific chromatin looping at maize b1 epialleles. Plant Cell 21:832–842

    Article  PubMed  CAS  Google Scholar 

  • Lyko F, Brenton JD, Surani MA, Paro R (1997) An imprinting element from the mouse H19 locus functions as a silencer in Drosophila. Nat Genet 16:171–173

    Article  PubMed  CAS  Google Scholar 

  • Matzke MA, Birchler JA (2005) RNAi-mediated pathways in the nucleus. Nat Rev Genet 6:24–35

    Article  PubMed  CAS  Google Scholar 

  • McEachern LA (2012) Transgenic epigenetics: using transgenic organisms to examine epigenetic phenomena. Genet Res Int. doi:10.1155/2012/689819

  • Patterson GI, Thorpe CJ, Chandler VL (1993) Paramutation, an allelic interaction, is associated with a stable and heritable reduction of transcription of the maize b regulatory gene. Genetics 135:881–894

    PubMed  CAS  Google Scholar 

  • Rassoulzadegan M, Grandjean V, Gounon P, Cuzin F (2007) Inheritance of an epigenetic change in the mouse: a new role for RNA. Biochem Soc Trans 35:623–625

    Article  PubMed  CAS  Google Scholar 

  • Robertson HM, Preston CR, Phillis RW, Johnson-Schlitz DM, Benz WK, Engels WR (1988) A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118:461–470

    PubMed  CAS  Google Scholar 

  • Schoenfelder S, Smits G, Fraser P, Reik W, Paro R (2007) Non-coding transcripts in the H19 imprinting control region mediate gene silencing in transgenic Drosophila. EMBO Rep 8:1068–1073

    Article  PubMed  CAS  Google Scholar 

  • Shpiz S, Kwon D, Rozovsky Y, Kalmykova A (2009) rasiRNA pathway controls antisense expression of Drosophila telomeric retrotransposons in the nucleus. Nucleic Acids Res 37:268–278

    Article  PubMed  CAS  Google Scholar 

  • Sidorenko L, Dorweiler JE, Cigan AM, Arteaga-Vazquez M, Vyas M, Kermicle J, Jurcin D, Brzeski J, Cai Y, Chandler VL (2009) A dominant mutation in mediator of paramutation2, one of three second-largest subunits of a plant-specific RNA polymerase, disrupts multiple siRNA silencing processes. PLoS Genet 5:e1000725

    Article  PubMed  Google Scholar 

  • Spradling AC, Rubin GM (1982) Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218:341–347

    Article  PubMed  CAS  Google Scholar 

  • Stam M (2009) Paramutation: a heritable change in gene expression by allelic interactions in trans. Mol Plant 2:578–588

    Article  PubMed  CAS  Google Scholar 

  • Stam M, Belele C, Dorweiler JE, Chandler VL (2002) Differential chromatin structure within a tandem array 100 kb upstream of the maize b1 locus is associated with paramutation. Genes Dev 16:1906–1918

    Article  PubMed  CAS  Google Scholar 

  • Stonaker JL, Lim JP, Erhard KF Jr, Hollick JB (2009) Diversity of Pol IV function is defined by mutations at the maize rmr7 locus. PLoS Genet 5:e1000706

    Article  PubMed  Google Scholar 

  • Suter CM, Martin DI (2010) Paramutation: the tip of an epigenetic iceberg? Trends Genet 26:9–14

    Article  PubMed  CAS  Google Scholar 

  • Teixeira FK, Colot V (2010) Repeat elements and the Arabidopsis DNA methylation landscape. Heredity 105:14–23

    Article  PubMed  CAS  Google Scholar 

  • Tweedie S, Ashburner M, Falls K, Leyland P, McQuilton P, Marygold S, Millburn G, Osumi-Sutherland D, Schroeder A, Seal R, Zhang H (2009) FlyBase: enhancing Drosophila gene ontology annotations. Nucleic Acids Res 37:D555–D559

    Article  PubMed  CAS  Google Scholar 

  • Wagner KD, Wagner N, Ghanbarian H, Grandjean V, Gounon P, Cuzin F, Rassoulzadegan M (2008) RNA induction and inheritance of epigenetic cardiac hypertrophy in the mouse. Dev Cell 14:962–969

    Article  PubMed  CAS  Google Scholar 

  • Yin H, Lin H (2007) An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogaster. Nature 450:304–308

    Article  PubMed  CAS  Google Scholar 

  • Zaratiegui M, Irvine DV, Martienssen RA (2007) Noncoding RNAs and gene silencing. Cell 128:763–776

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Vicki Chandler for the maize b1 tandem repeat vector, J. Sekelsky for the pP{WhiteOut2} vector, the Bloomington Drosophila Stock Center, the Lett Fund, the Killam Trusts, and NSERC Canada for a Discovery grant to V.K. Lloyd and a postgraduate scholarship to L.A. McEachern.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Vett K. Lloyd.

Additional information

Communicated by G. Reuter.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 57 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

McEachern, L.A., Lloyd, V.K. The maize b1 paramutation control region causes epigenetic silencing in Drosophila melanogaster . Mol Genet Genomics 287, 591–606 (2012). https://doi.org/10.1007/s00438-012-0702-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-012-0702-z

Keywords

Navigation