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Polycomb-Mediated Gene Silencing in Arabidopsis thaliana

  • Kim, Dong-Hwan ;
  • Sung, Sibum
  • Received : 2014.09.12
  • Accepted : 2014.09.15
  • Published : 2014.12.31

Abstract

Polycomb group (PcG) proteins are conserved chromatin regulators involved in the control of key developmental programs in eukaryotes. They collectively provide the transcriptional memory unique to each cell identity by maintaining transcriptional states of developmental genes. PcG proteins form multi-protein complexes, known as Polycomb repressive complex 1 (PRC1) and Polycomb repressive complex 2 (PRC2). PRC1 and PRC2 contribute to the stable gene silencing in part through catalyzing covalent histone modifications. Components of PRC1 and PRC2 are well conserved from plants to animals. PcG-mediated gene silencing has been extensively investigated in efforts to understand molecular mechanisms underlying developmental programs in eukaryotes. Here, we describe our current knowledge on PcG-mediated gene repression which dictates developmental programs by dynamic layers of regulatory activities, with an emphasis given to the model plant Arabidopsis thaliana.

Keywords

chromatin looping;epigenetics;gene silencing;polycomb;trithorax

References

  1. Akasaka, T., Kanno, M., Balling, R., Mieza, M.A., Taniguchi, M., and Koseki, H. (1996). A role for mel-18, a Polycomb group-related vertebrate gene, during theanteroposterior specification of the axial skeleton. Development 122, 1513-1522.
  2. Bantignies, F., and Cavalli, G. (2011). Polycomb group proteins: repression in 3D. Trends Genet. 27, 454-464. https://doi.org/10.1016/j.tig.2011.06.008
  3. Bardos, J.I., Saurin, A.J., Tissot, C., Duprez, E., and Freemont, P.S. (2000). HPC3 is a new human polycomb orthologue that interacts and associates with RING1 and Bmi1 and has transcriptional repression properties. J. Biol. Chem. 275, 28785-28792. https://doi.org/10.1074/jbc.M001835200
  4. Barrero, J.M., Gonzalez-Bayon, R., del Pozo, J.C., Ponce, M.R., and Micol, J.L. (2007). INCURVATA2 encodes the catalytic subunit of DNA Polymerase alpha and interacts with genes involved in chromatin-mediated cellular memory in Arabidopsis thaliana. Plant Cell 19, 2822-2838. https://doi.org/10.1105/tpc.107.054130
  5. Bastow, R., Mylne, J.S., Lister, C., Lippman, Z., Martienssen, R.A., and Dean, C. (2004). Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427, 164-167. https://doi.org/10.1038/nature02269
  6. Beh, L.Y., Colwell, L.J., and Francis, N.J. (2012). A core subunit of Polycomb repressive complex 1 is broadly conserved in function but not primary sequence. Proc. Natl. Acad. Sci. USA 109, E1063-1071. https://doi.org/10.1073/pnas.1118678109
  7. Ben-Saadon, R., Zaaroor, D., Ziv, T., and Ciechanover, A. (2006). The polycomb protein Ring1B generates self atypical mixed ubiquitin chains required for its in vitro histone H2A ligase activity. Mol. Cell 24, 701-711. https://doi.org/10.1016/j.molcel.2006.10.022
  8. Berger, N., Dubreucq, B., Roudier, F., Dubos, C., and Lepiniec, L. (2011). Transcriptional regulation of Arabidopsis LEAFY COTYLEDON2 involves RLE, a cis-element that regulates trimethylation of histone H3 at lysine-27. Plant Cell 23, 4065-4078. https://doi.org/10.1105/tpc.111.087866
  9. Bernstein, B.E., Mikkelsen, T.S., Xie, X., Kamal, M., Huebert, D.J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K., et al. (2006a). A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315-326. https://doi.org/10.1016/j.cell.2006.02.041
  10. Bernstein, E., Duncan, E.M., Masui, O., Gil, J., Heard, E., and Allis, C.D. (2006b). Mouse polycomb proteins bind differentially to methylated histone H3 and RNA and are enriched in facultative heterochromatin. Mol. Cell. Biol. 26, 2560-2569. https://doi.org/10.1128/MCB.26.7.2560-2569.2006
  11. Berr, A., Xu, L., Gao, J., Cognat, V., Steinmetz, A., Dong, A., and Shen, W.H. (2009). SET DOMAIN GROUP25 encodes a histone methyltransferase and is involved in FLOWERING LOCUS C activation and repression of flowering. Plant Physiol. 151, 1476-1485. https://doi.org/10.1104/pp.109.143941
  12. Buchenau, P., Hodgson, J., Strutt, H., and Arndt-Jovin, D.J. (1998). The distribution of polycomb-group proteins during cell division and development in Drosophila embryos: impact on models for silencing. J. Cell Biol. 141, 469-481. https://doi.org/10.1083/jcb.141.2.469
  13. Bouyer, D., Roudier, F., Heese, M., Andersen, E.D., Gey, D., Nowack, M.K., Goodrich, J., Renou, J.P., Grini, P.E., Colot, V., et al. (2011). Polycomb repressive complex 2 controls the embryo-to-seedling phase transition. PLoS Genet. 7, e1002014. https://doi.org/10.1371/journal.pgen.1002014
  14. Bowman, J.L., Smyth, D.R., and Meyerowitz, E.M. (1989). Genes directing flower development in Arabidopsis. Plant Cell 1, 37-52. https://doi.org/10.1105/tpc.1.1.37
  15. Bratzel, F., Lopez-Torrejon, G., Koch, M., Del Pozo, J.C., and Calonje, M. (2010). Keeping cell identity in arabidopsis requires PRC1 RING-finger homologs that catalyze H2A monoubiquitination. Curr. Biol. 20, 1853-1859. https://doi.org/10.1016/j.cub.2010.09.046
  16. Buchwald, G., van der Stoop, P., Weichenrieder, O., Perrakis, A., van Lohuizen, M., and Sixma, T.K. (2006). Structure and E3-ligase activity of the Ring-Ring complex of polycomb proteins Bmi1 and Ring1b. EMBO J. 25, 2465-2474. https://doi.org/10.1038/sj.emboj.7601144
  17. Byrne, M.E., Barley, R., Curtis, M., Arroyo, J.M., Dunham, M., Hudson, A., and Martienssen, R.A. (2000). Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408, 967-971. https://doi.org/10.1038/35050091
  18. Calonje, M., Sanchez, R., Chen, L., and Sung, Z.R. (2008). EMBRYONIC FLOWER1 participates in polycomb group-mediated AG gene silencing in Arabidopsis. Plant Cell 20, 277-291.
  19. Cao, R., Wang, L., Wang, H., Xia, L., Erdjument-Bromage, H., Tempst, P., Jones, R.S., and Zhang, Y. (2002). Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298, 1039-1043. https://doi.org/10.1126/science.1076997
  20. Cao, R., Tsukada, Y., and Zhang, Y. (2005). Role of Bmi-1 and Ring1A in H2A ubiquitylation and Hox gene silencing. Mol. Cell 20, 845-854. https://doi.org/10.1016/j.molcel.2005.12.002
  21. Carles, C.C., and Fletcher, J.C. (2009). The SAND domain protein ULTRAPETALA1 acts as a trithorax group factor to regulate cell fate in plants. Genes Dev. 23, 2723-2728. https://doi.org/10.1101/gad.1812609
  22. Chanvivattana, Y., Bishopp, A., Schubert, D., Stock, C., Moon, Y.H., Sung, Z.R., and Goodrich, J. (2004). Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development 131, 5263-5276. https://doi.org/10.1242/dev.01400
  23. Cheutin, T., and Cavalli, G. (2014). Polycomb silencing: from linear chromatin domains to 3D chromosome folding. Curr. Opin. Genet. Dev. 25, 30-37. https://doi.org/10.1016/j.gde.2013.11.016
  24. Chua, Y.L., Channeliere, S., Mott, E., and Gray, J.C. (2005). The bromodomain protein GTE6 controls leaf development in Arabidopsis by histone acetylation at ASYMMETRIC LEAVES1. Genes Dev. 19, 2245-2254. https://doi.org/10.1101/gad.352005
  25. Crevillen, P., Sonmez, C., Wu, Z., and Dean, C. (2013). A gene loop containing the floral repressor FLC is disrupted in the early phase of vernalization. EMBO J. 32, 140-148.
  26. Cui, H., and Benfey, P.N. (2009). Interplay between SCARECROW, GA and LIKE HETEROCHROMATIN PROTEIN 1 in ground tissue patterning in the Arabidopsis root. Plant J. 58, 1016-1027. https://doi.org/10.1111/j.1365-313X.2009.03839.x
  27. Czermin, B., Melfi, R., McCabe, D., Seitz, V., Imhof, A., and Pirrotta, V. (2002). Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111, 185-196. https://doi.org/10.1016/S0092-8674(02)00975-3
  28. De Lucia, F., Crevillen, P., Jones, A.M., Greb, T., and Dean, C. (2008). A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc. Natl. Acad. Sci. USA 105, 16831-16836. https://doi.org/10.1073/pnas.0808687105
  29. Dekker, J., Rippe, K., Dekker, M., and Kleckner, N. (2002). Capturing chromosome conformation. Science 295, 1306-1311. https://doi.org/10.1126/science.1067799
  30. Eskeland, R., Leeb, M., Grimes, G.R., Kress, C., Boyle, S., Sproul, D., Gilbert, N., Fan, Y., Skoultchi, A.I., Wutz, A., et al. (2010). Ring1B compacts chromatin structure and represses gene expression independent of histone ubiquitination. Mol. Cell 38, 452-464. https://doi.org/10.1016/j.molcel.2010.02.032
  31. del Olmo, I., Lopez-Gonzalez, L., Martin-Trillo, M.M., Martinez-Zapater, J.M., Pineiro, M., and Jarillo, J.A. (2010). EARLY IN SHORT DAYS 7 (ESD7) encodes the catalytic subunit of DNA polymerase epsilon and is required for flowering repression through a mechanism involving epigenetic gene silencing. Plant J. 61, 623-636. https://doi.org/10.1111/j.1365-313X.2009.04093.x
  32. Deng, W., Buzas, D.M., Ying, H., Robertson, M., Taylor, J., Peacock, W.J., Dennis, E.S., and Helliwell, C. (2013). Arabidopsis polycomb repressive complex 2 binding sites contain putative GAGA factor binding motifs within coding regions of genes. BMC Genomics 14, 593. https://doi.org/10.1186/1471-2164-14-593
  33. Derkacheva, M., Steinbach, Y., Wildhaber, T., Mozgova, I., Mahrez, W., Nanni, P., Bischof, S., Gruissem, W., and Hennig, L. (2013). Arabidopsis MSI1 connects LHP1 to PRC2 complexes. EMBO J. 32, 2073-2085. https://doi.org/10.1038/emboj.2013.145
  34. Exner, V., Aichinger, E., Shu, H., Wildhaber, T., Alfarano, P., Caflisch, A., Gruissem, W., Kohler, C., and Hennig, L. (2009). The chromodomain of LIKE HETEROCHROMATIN PROTEIN 1 is essential for H3K27me3 binding and function during Arabidopsis development. PLoS One 4, e5335. https://doi.org/10.1371/journal.pone.0005335
  35. Gomez, J.A., Wapinski, O.L., Yang, Y.W., Bureau, J.F., Gopinath, S., Monack, D.M., Chang, H.Y., Brahic, M., and Kirkegaard, K. (2013). The NeST long ncRNA controls microbial susceptibility and epigenetic activation of the interferon-gamma locus. Cell 152, 743-754. https://doi.org/10.1016/j.cell.2013.01.015
  36. Goodrich, J., Puangsomlee, P., Martin, M., Long, D., Meyerowitz, E.M., and Coupland, G. (1997). A Polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386, 44-51. https://doi.org/10.1038/386044a0
  37. Grimaud, C., Bantignies, F., Pal-Bhadra, M., Ghana, P., Bhadra, U., and Cavalli, G. (2006). RNAi components are required for nuclear clustering of Polycomb group response elements. Cell 124, 957-971. https://doi.org/10.1016/j.cell.2006.01.036
  38. Guo, M., Thomas, J., Collins, G., and Timmermans, M.C. (2008). Direct repression of KNOX loci by the ASYMMETRIC LEAVES1 complex of Arabidopsis. Plant Cell 20, 48-58. https://doi.org/10.1105/tpc.107.056127
  39. He, Y., Yu, Y., Zhang, Y., Song, J., Mitra, A., Zhang, Y., Wang, Y., Sun, D., and Zhang, S. (2012). Genome-wide bovine H3K27me3 modifications and the regulatory effects on genes expressions in peripheral blood lymphocytes. PLoS One 7, e39094. https://doi.org/10.1371/journal.pone.0039094
  40. He, C., Huang, H., and Xu, L. (2013). Mechanisms guiding Polycomb activities during gene silencing in Arabidopsis thaliana. Front. Plant Sci. 4, 454.
  41. Heo, J.B., and Sung, S. (2011). Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331, 76-79. https://doi.org/10.1126/science.1197349
  42. Iwakawa, H., Ueno, Y., Semiarti, E., Onouchi, H., Kojima, S., Tsukaya, H., Hasebe, M., Soma, T., Ikezaki, M., Machida, C., et al. (2002). The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana, required for formation of a symmetric flat leaf lamina, encodes a member of a novel family of proteins characterized by cysteine repeats and a leucine zipper. Plant Cell Physiol. 43, 467-478. https://doi.org/10.1093/pcp/pcf077
  43. Jegu, T., Latrasse, D., Delarue, M., Hirt, H., Domenichini, S., Ariel, F., Crespi, M., Bergounioux, C., Raynaud, C., and Benhamed, M. (2014). The BAF60 subunit of the SWI/SNF chromatin-remodeling complex directly controls the formation of a gene loop at FLOWERING LOCUS C in Arabidopsis. Plant Cell 26, 538-551. https://doi.org/10.1105/tpc.113.114454
  44. Jiang, D., Wang, Y., and He, Y. (2008). Repression of FLOWERING LOCUS C and FLOWERING LOCUS T by the Arabidopsis Polycomb repressive complex 2 components. PLoS One 3, e3404. https://doi.org/10.1371/journal.pone.0003404
  45. Kim, D.H., Doyle, M.R., Sung, S., and Amasino, R.M. (2009). Vernalization: winter and the timing of flowering in plants. Annu. Rev. Cell Dev. Biol. 25, 277-299. https://doi.org/10.1146/annurev.cellbio.042308.113411
  46. Kanhere, A., Viiri, K., Araujo, C.C., Rasaiyaah, J., Bouwman, R.D., Whyte, W.A., Pereira, C.F., Brookes, E., Walker, K., Bell, G.W., et al. (2010). Short RNAs are transcribed from repressed polycomb target genes and interact with polycomb repressive complex-2. Mol. Cell 38, 675-688. https://doi.org/10.1016/j.molcel.2010.03.019
  47. Khalil, A.M., Guttman, M., Huarte, M., Garber, M., Raj, A., Rivea Morales, D., Thomas, K., Presser, A., Bernstein, B.E., van Oudenaarden, A., et al. (2009). Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc. Natl. Acad. Sci. USA 106, 11667-11672. https://doi.org/10.1073/pnas.0904715106
  48. Kim, S.Y., He, Y., Jacob, Y., Noh, Y.S., Michaels, S., and Amasino, R. (2005). Establishment of the vernalization-responsive, winter-annual habit in Arabidopsis requires a putative histone H3 methyl transferase. Plant Cell 17, 3301-3310. https://doi.org/10.1105/tpc.105.034645
  49. Kim, S.Y., Lee, J., Eshed-Williams, L., Zilberman, D., and Sung, Z.R. (2012). EMF1 and PRC2 cooperate to repress key regulators of Arabidopsis development. PLoS Genet. 8, e1002512. https://doi.org/10.1371/journal.pgen.1002512
  50. Ko, J.H., Mitina, I., Tamada, Y., Hyun, Y., Choi, Y., Amasino, R.M., Noh, B., and Noh, Y.S. (2010). Growth habit determination by the balance of histone methylation activities in Arabidopsis. EMBO J. 29, 3208-3215. https://doi.org/10.1038/emboj.2010.198
  51. Kohler, C., Hennig, L., Spillane, C., Pien, S., Gruissem, W., and Grossniklaus, U. (2003). The Polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1. Genes Dev. 17, 1540-1553. https://doi.org/10.1101/gad.257403
  52. Ku, M., Koche, R.P., Rheinbay, E., Mendenhall, E.M., Endoh, M., Mikkelsen, T.S., Presser, A., Nusbaum, C., Xie, X., Chi, A.S., et al. (2008). Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet. 4, e1000242. https://doi.org/10.1371/journal.pgen.1000242
  53. Lafos, M., Kroll, P., Hohenstatt, M.L., Thorpe, F.L., Clarenz, O., and Schubert, D. (2011). Dynamic regulation of H3K27 trimethylation during Arabidopsis differentiation. PLoS Genet. 7, e1002040. https://doi.org/10.1371/journal.pgen.1002040
  54. Lanctot, C., Kaspar, C., and Cremer, T. (2007). Positioning of the mouse Hox gene clusters in the nuclei of developing embryos and differentiating embryoid bodies. Exp. Cell Res. 313, 1449-1459. https://doi.org/10.1016/j.yexcr.2007.01.027
  55. Lanzuolo, C., Roure, V., Dekker, J., Bantignies, F., and Orlando, V. (2007). Polycomb response elements mediate the formation of chromosome higher-order structures in the bithorax complex. Nat. Cell Biol. 9, 1167-1174. https://doi.org/10.1038/ncb1637
  56. Latrasse, D., Germann, S., Houba-Herin, N., Dubois, E., Bui- Prodhomme, D., Hourcade, D., Juul-Jensen, T., Le Roux, C., Majira, A., Simoncello, N., et al. (2011). Control of flowering and cell fate by LIF2, an RNA binding partner of the polycomb complex component LHP1. PLoS One 6, e16592. https://doi.org/10.1371/journal.pone.0016592
  57. Lee, J.S., Shukla, A., Schneider, J., Swanson, S.K., Washburn, M.P., Florens, L., Bhaumik, S.R., and Shilatifard, A. (2007a). Histone crosstalk between H2B monoubiquitination and H3 methylation mediated by COMPASS. Cell 131, 1084-1096. https://doi.org/10.1016/j.cell.2007.09.046
  58. Lee, M.G., Villa, R., Trojer, P., Norman, J., Yan, K.P., Reinberg, D., Di Croce, L., and Shiekhattar, R. (2007b). Demethylation of H3K27 regulates polycomb recruitment and H2A ubiquitination. Science 318, 447-450. https://doi.org/10.1126/science.1149042
  59. Levy, Y.Y., Mesnage, S., Mylne, J.S., Gendall, A.R., and Dean, C. (2002). Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control. Science 297, 243-246. https://doi.org/10.1126/science.1072147
  60. Lewis, E.B. (1978). A gene complex controlling segmentation in Drosophila. Nature 276, 565-570. https://doi.org/10.1038/276565a0
  61. Li, H., and Luan, S. (2011). The cyclophilin AtCYP71 interacts with CAF-1 and LHP1 and functions in multiple chromatin remodeling processes. Mol. Plant 4, 748-758. https://doi.org/10.1093/mp/ssr036
  62. Liu, X., Kim, Y.J., Muller, R., Yumul, R.E., Liu, C., Pan, Y., Cao, X., Goodrich, J., and Chen, X. (2011). AGAMOUS terminates floral stem cell maintenance in Arabidopsis by directly repressing WUSCHEL through recruitment of Polycomb Group proteins. Plant Cell 23, 3654-3670. https://doi.org/10.1105/tpc.111.091538
  63. Li, W., Wang, Z., Li, J., Yang, H., Cui, S., Wang, X., and Ma, L. (2011). Overexpression of AtBMI1C, a polycomb group protein gene, accelerates flowering in Arabidopsis. PLoS One 6, e21364. https://doi.org/10.1371/journal.pone.0021364
  64. Lin, W.C., Shuai, B., and Springer, P.S. (2003). The Arabidopsis LATERAL ORGAN BOUNDARIES-domain gene ASYMMETRIC LEAVES2 functions in the repression of KNOX gene expression and in adaxial-abaxial patterning. Plant Cell 15, 2241-2252. https://doi.org/10.1105/tpc.014969
  65. Liu, F., Marquardt, S., Lister, C., Swiezewski, S., and Dean, C. (2010). Targeted 3' processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science 327, 94-97. https://doi.org/10.1126/science.1180278
  66. Liu, J., Jung, C., Xu, J., Wang, H., Deng, S., Bernad, L., Arenas-Huertero, C., and Chua, N.H. (2012). Genome-wide analysis uncovers regulation of long intergenic noncoding RNAs in Arabidopsis. Plant Cell 24, 4333-4345. https://doi.org/10.1105/tpc.112.102855
  67. Lodha, M., Marco, C.F., and Timmermans, M.C. (2013). The ASYMMETRIC LEAVES complex maintains repression of KNOX homeobox genes via direct recruitment of Polycomb-repressive complex2. Genes Dev. 27, 596-601. https://doi.org/10.1101/gad.211425.112
  68. Lohmann, J.U., Hong, R.L., Hobe, M., Busch, M.A., Parcy, F., Simon, R., and Weigel, D. (2001). A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105, 793-803. https://doi.org/10.1016/S0092-8674(01)00384-1
  69. Makarevich, G., Leroy, O., Akinci, U., Schubert, D., Clarenz, O., Goodrich, J., Grossniklaus, U., and Kohler, C. (2006). Different Polycomb group complexes regulate common target genes in Arabidopsis. EMBO Rep. 7, 947-952. https://doi.org/10.1038/sj.embor.7400760
  70. Margueron, R., and Reinberg, D. (2011). The Polycomb complex PRC2 and its mark in life. Nature 469, 343-349. https://doi.org/10.1038/nature09784
  71. Margueron, R., Justin, N., Ohno, K., Sharpe, M.L., Son, J., Drury, W.J., 3rd, Voigt, P., Martin, S.R., Taylor, W.R., De Marco, V., et al. (2009). Role of the polycomb protein EED in the propagation of repressive histone marks. Nature 461, 762-767. https://doi.org/10.1038/nature08398
  72. Marquardt, S., Raitskin, O., Wu, Z., Liu, F., Sun, Q., and Dean, C. (2014). Functional consequences of splicing of the antisense transcript COOLAIR on FLC transcription. Mol. Cell 54, 156-165. https://doi.org/10.1016/j.molcel.2014.03.026
  73. Mercer, T.R., and Mattick, J.S. (2013). Understanding the regulatory and transcriptional complexity of the genome through structure. Genome Res. 23, 1081-1088. https://doi.org/10.1101/gr.156612.113
  74. Messmer, S., Franke, A., and Paro, R. (1992). Analysis of the functional role of the Polycomb chromo domain in Drosophila melanogaster. Genes Dev. 6, 1241-1254. https://doi.org/10.1101/gad.6.7.1241
  75. Min, J., Zhang, Y., and Xu, R.M. (2003). Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27. Genes Dev. 17, 1823-1828. https://doi.org/10.1101/gad.269603
  76. Mohan, M., Herz, H.M., Smith, E.R., Zhang, Y., Jackson, J., Washburn, M.P., Florens, L., Eissenberg, J.C., and Shilatifard, A. (2011). The COMPASS family of H3K4 methylases in Drosophila. Mol. Cell. Biol. 31, 4310-4318. https://doi.org/10.1128/MCB.06092-11
  77. Molitor, A., and Shen, W.H. (2013). The polycomb complex PRC1: composition and function in plants. J. Genet. Genomics 40, 231-238. https://doi.org/10.1016/j.jgg.2012.12.005
  78. Moon, Y.H., Chen, L., Pan, R.L., Chang, H.S., Zhu, T., Maffeo, D.M., and Sung, Z.R. (2003). EMF genes maintain vegetative development by repressing the flower program in Arabidopsis. Plant Cell 15, 681-693. https://doi.org/10.1105/tpc.007831
  79. Muller, R., and Goodrich, J. (2011). Sweet memories: epigenetic control in flowering. F1000 Biol. Rep. 3, 13.
  80. Papp, B., and Muller, J. (2006). Histone trimethylation and the maintenance of transcriptional ON and OFF states by trxG and PcG proteins. Genes Dev. 20, 2041-2054. https://doi.org/10.1101/gad.388706
  81. Muller, J., Hart, C.M., Francis, N.J., Vargas, M.L., Sengupta, A., Wild, B., Miller, E.L., O'Connor, M.B., Kingston, R.E., and Simon, J.A. (2002). Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111, 197-208. https://doi.org/10.1016/S0092-8674(02)00976-5
  82. Mylne, J.S., Barrett, L., Tessadori, F., Mesnage, S., Johnson, L., Bernatavichute, Y.V., Jacobsen, S.E., Fransz, P., and Dean, C. (2006). LHP1, the Arabidopsis homologue of HETEROCHROMATIN PROTEIN1, is required for epigenetic silencing of FLC. Proc. Natl. Acad. Sci. USA 103, 5012-5017. https://doi.org/10.1073/pnas.0507427103
  83. Oh, S., Park, S., and van Nocker, S. (2008). Genic and global functions for Paf1C in chromatin modification and gene expression in Arabidopsis. PLoS Genet. 4, e1000077. https://doi.org/10.1371/journal.pgen.1000077
  84. Pasini, D., Malatesta, M., Jung, H.R., Walfridsson, J., Willer, A., Olsson, L., Skotte, J., Wutz, A., Porse, B., Jensen, O.N., et al. (2010). Characterization of an antagonistic switch between histone H3 lysine 27 methylation and acetylation in the transcriptional regulation of Polycomb group target genes. Nucleic Acids Res. 38, 4958-4969. https://doi.org/10.1093/nar/gkq244
  85. Pien, S., and Grossniklaus, U. (2007). Polycomb group and trithorax group proteins in Arabidopsis. Biochim. Biophys. Acta 1769, 375-382. https://doi.org/10.1016/j.bbaexp.2007.01.010
  86. Pien, S., Fleury, D., Mylne, J.S., Crevillen, P., Inze, D., Avramova, Z., Dean, C., and Grossniklaus, U. (2008). ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation. Plant Cell 20, 580-588. https://doi.org/10.1105/tpc.108.058172
  87. Pirrotta, V. (1997). Chromatin-silencing mechanisms in Drosophila maintain patterns of gene expression. Trends Genet. 13, 314-318. https://doi.org/10.1016/S0168-9525(97)01178-5
  88. Rosa, S., De Lucia, F., Mylne, J.S., Zhu, D., Ohmido, N., Pendle, A., Kato, N., Shaw, P., and Dean, C. (2013). Physical clustering of FLC alleles during Polycomb-mediated epigenetic silencing in vernalization. Genes Dev. 27, 1845-1850. https://doi.org/10.1101/gad.221713.113
  89. Ringrose, L., and Paro, R. (2004). Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins. Ann. Rev. Genet. 38, 413-443. https://doi.org/10.1146/annurev.genet.38.072902.091907
  90. Rinn, J.L., and Chang, H.Y. (2012). Genome regulation by long noncoding RNAs. Ann. Rev. Biochem. 81, 145-166. https://doi.org/10.1146/annurev-biochem-051410-092902
  91. Rinn, J.L., Kertesz, M., Wang, J.K., Squazzo, S.L., Xu, X., Brugmann, S.A., Goodnough, L.H., Helms, J.A., Farnham, P.J., Segal, E., et al. (2007). Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129, 1311-1323. https://doi.org/10.1016/j.cell.2007.05.022
  92. Roudier, F., Ahmed, I., Berard, C., Sarazin, A., Mary-Huard, T., Cortijo, S., Bouyer, D., Caillieux, E., Duvernois-Berthet, E., Al-Shikhley, L., et al. (2011). Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J. 30, 1928-1938. https://doi.org/10.1038/emboj.2011.103
  93. Saleh, A., Alvarez-Venegas, R., Yilmaz, M., Le, O., Hou, G., Sadder, M., Al-Abdallat, A., Xia, Y., Lu, G., Ladunga, I., et al. (2008). The highly similar Arabidopsis homologs of trithorax ATX1 and ATX2 encode proteins with divergent biochemical functions. Plant Cell 20, 568-579. https://doi.org/10.1105/tpc.107.056614
  94. Sanchez-Pulido, L., Devos, D., Sung, Z.R., and Calonje, M. (2008). RAWUL: a new ubiquitin-like domain in PRC1 ring finger proteins that unveils putative plant and worm PRC1 orthologs. BMC Genomics 9, 308. https://doi.org/10.1186/1471-2164-9-308
  95. Schatlowski, N., Creasey, K., Goodrich, J., and Schubert, D. (2008). Keeping plants in shape: polycomb-group genes and histone methylation. Semin. Cell Dev. Biol. 19, 547-553. https://doi.org/10.1016/j.semcdb.2008.07.019
  96. Schuettengruber, B., Ganapathi, M., Leblanc, B., Portoso, M., Jaschek, R., Tolhuis, B., van Lohuizen, M., Tanay, A., and Cavalli, G. (2009). Functional anatomy of polycomb and trithorax chromatin landscapes in Drosophila embryos. PLoS Biol. 7, e13. https://doi.org/10.1371/journal.pbio.1000013
  97. Schmitges, F.W., Prusty, A.B., Faty, M., Stutzer, A., Lingaraju, G.M., Aiwazian, J., Sack, R., Hess, D., Li, L., Zhou, S., et al. (2011). Histone methylation by PRC2 is inhibited by active chromatin marks. Mol. Cell 42, 330-341. https://doi.org/10.1016/j.molcel.2011.03.025
  98. Schubert, D., Clarenz, O., and Goodrich, J. (2005). Epigenetic control of plant development by Polycomb-group proteins. Curr. Opin. Plant Biol. 8, 553-561. https://doi.org/10.1016/j.pbi.2005.07.005
  99. Schuettengruber, B., Chourrout, D., Vervoort, M., Leblanc, B., and Cavalli, G. (2007). Genome regulation by polycomb and trithorax proteins. Cell 128, 735-745. https://doi.org/10.1016/j.cell.2007.02.009
  100. Schwartz, Y.B., and Pirrotta, V. (2007). Polycomb silencing mechanisms and the management of genomic programmes. Nat. Rev. Genet. 8, 9-22.
  101. Schwartz, Y.B., and Pirrotta, V. (2008). Polycomb complexes and epigenetic states. Curr. Opin. Plant Biol. 20, 266-273. https://doi.org/10.1016/j.ceb.2008.03.002
  102. Schwartz, Y.B., Kahn, T.G., Nix, D.A., Li, X.Y., Bourgon, R., Biggin, M., and Pirrotta, V. (2006). Genome-wide analysis of polycomb targets in Drosophila melanogaster. Nat. Genet. 38, 700-705. https://doi.org/10.1038/ng1817
  103. Schwartz, Y.B., Kahn, T.G., Stenberg, P., Ohno, K., Bourgon, R., and Pirrotta, V. (2010). Alternative epigenetic chromatin states of polycomb target genes. PLoS Genet. 6, e1000805. https://doi.org/10.1371/journal.pgen.1000805
  104. Semiarti, E., Ueno, Y., Tsukaya, H., Iwakawa, H., Machida, C., and Machida, Y. (2001). The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana regulates formation of a symmetric lamina, establishment of venation and repression of meristem-related homeobox genes in leaves. Development 128, 1771-1783.
  105. Simon, J., Chiang, A., and Bender, W. (1992). Ten different Polycomb group genes are required for spatial control of the abdA and AbdB homeotic products. Development 114, 493-505.
  106. Sexton, T., Yaffe, E., Kenigsberg, E., Bantignies, F., Leblanc, B., Hoichman, M., Parrinello, H., Tanay, A., and Cavalli, G. (2012). Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 148, 458-472. https://doi.org/10.1016/j.cell.2012.01.010
  107. Simon, J.A., and Kingston, R.E. (2009). Mechanisms of polycomb gene silencing: knowns and unknowns. Nat. Rev. Mol. Cell Biol. 10, 697-708. https://doi.org/10.1038/nrn2731
  108. Simon, J.A., and Kingston, R.E. (2013). Occupying chromatin: Polycomb mechanisms for getting to genomic targets, stopping transcriptional traffic, and staying put. Mol. Cell 49, 808-824. https://doi.org/10.1016/j.molcel.2013.02.013
  109. Sing, A., Pannell, D., Karaiskakis, A., Sturgeon, K., Djabali, M., Ellis, J., Lipshitz, H.D., and Cordes, S.P. (2009). A vertebrate Polycomb response element governs segmentation of the posterior hindbrain. Cell 138, 885-897. https://doi.org/10.1016/j.cell.2009.08.020
  110. Smalle, J., and Vierstra, R.D. (2004). The ubiquitin 26S proteasome proteolytic pathway. Ann. Rev. Plant Biol. 55, 555-590. https://doi.org/10.1146/annurev.arplant.55.031903.141801
  111. Soppe, W.J., Bentsink, L., and Koornneef, M. (1999). The early-flowering mutant efs is involved in the autonomous promotion pathway of Arabidopsis thaliana. Development 126, 4763-4770.
  112. Soto, M.C., Chou, T.B., and Bender, W. (1995). Comparison of germline mosaics of genes in the Polycomb group of Drosophila melanogaster. Genetics 140, 231-243.
  113. Steffen, P.A., and Ringrose, L. (2014). What are memories made of? How Polycomb and Trithorax proteins mediate epigenetic memory. Nat. Rev. Mol. Cell Biol. 15, 340-356. https://doi.org/10.1038/nrm3789
  114. Stone, S.L., Kwong, L.W., Yee, K.M., Pelletier, J., Lepiniec, L., Fischer, R.L., Goldberg, R.B., and Harada, J.J. (2001). LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development. Proc. Natl. Acad. Sci. USA 98, 11806-11811. https://doi.org/10.1073/pnas.201413498
  115. Struhl, G., and Akam, M. (1985). Altered distributions of Ultrabithorax transcripts in extra sex combs mutant embryos of Drosophila. EMBO J. 4, 3259-3264.
  116. Sun, B., Xu, Y., Ng, K.H., and Ito, T. (2009). A timing mechanism for stem cell maintenance and differentiation in the Arabidopsis floral meristem. Genes Dev. 23, 1791-1804. https://doi.org/10.1101/gad.1800409
  117. Sun, B., Looi, L.S., Guo, S., He, Z., Gan, E.S., Huang, J., Xu, Y., Wee, W.Y., and Ito, T. (2014). Timing mechanism dependent on cell division is invoked by Polycomb eviction in plant stem cells. Science 343, 1248559. https://doi.org/10.1126/science.1248559
  118. Sung, S., and Amasino, R.M. (2004). Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427, 159-164. https://doi.org/10.1038/nature02195
  119. Sung, S., He, Y., Eshoo, T.W., Tamada, Y., Johnson, L., Nakahigashi, K., Goto, K., Jacobsen, S.E., and Amasino, R.M. (2006). Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1. Nat. Genet. 38, 706-710. https://doi.org/10.1038/ng1795
  120. Suzuki, M., Wang, H.H., and McCarty, D.R. (2007). Repression of the LEAFY COTYLEDON 1/B3 regulatory network in plant embryo development by VP1/ABSCISIC ACID INSENSITIVE 3-LIKE B3 genes. Plant Physiol. 143, 902-911.
  121. Swiezewski, S., Liu, F., Magusin, A., and Dean, C. (2009). Coldinduced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462, 799-802. https://doi.org/10.1038/nature08618
  122. Tamada, Y., Yun, J.Y., Woo, S.C., and Amasino, R.M. (2009). ARABIDOPSIS TRITHORAX-RELATED7 is required for methylation of lysine 4 of histone H3 and for transcriptional activation of FLOWERING LOCUS C. Plant Cell 21, 3257-3269. https://doi.org/10.1105/tpc.109.070060
  123. Tripoulas, N.A., Hersperger, E., La Jeunesse, D., and Shearn, A. (1994). Molecular genetic analysis of the Drosophila melanogaster gene absent, small or homeotic discs1 (ash1). Genetics 137, 1027-1038.
  124. Tang, X., Lim, M.H., Pelletier, J., Tang, M., Nguyen, V., Keller, W.A., Tsang, E.W., Wang, A., Rothstein, S.J., Harada, J.J., et al. (2012). Synergistic repression of the embryonic programme by SET DOMAIN GROUP 8 and EMBRYONIC FLOWER 2 in Arabidopsis seedlings. J. Exp. Bot. 63, 1391-1404. https://doi.org/10.1093/jxb/err383
  125. Tie, F., Banerjee, R., Stratton, C.A., Prasad-Sinha, J., Stepanik, V., Zlobin, A., Diaz, M.O., Scacheri, P.C., and Harte, P.J. (2009). CBP-mediated acetylation of histone H3 lysine 27 antagonizes Drosophila Polycomb silencing. Development 136, 3131-3141. https://doi.org/10.1242/dev.037127
  126. Tie, F., Banerjee, R., Saiakhova, A.R., Howard, B., Monteith, K.E., Scacheri, P.C., Cosgrove, M.S., and Harte, P.J. (2014). Trithorax monomethylates histone H3K4 and interacts directly with CBP to promote H3K27 acetylation and antagonize Polycomb silencing. Development 141, 1129-1139. https://doi.org/10.1242/dev.102392
  127. Turck, F., Roudier, F., Farrona, S., Martin-Magniette, M.L., Guillaume, E., Buisine, N., Gagnot, S., Martienssen, R.A., Coupland, G., and Colot, V. (2007). Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet. 3, e86. https://doi.org/10.1371/journal.pgen.0030086
  128. Wang, H., Wang, L., Erdjument-Bromage, H., Vidal, M., Tempst, P., Jones, R.S., and Zhang, Y. (2004). Role of histone H2A ubiquitination in Polycomb silencing. Nature 431, 873-878. https://doi.org/10.1038/nature02985
  129. Wang, K.C., and Chang, H.Y. (2011). Molecular mechanisms of long noncoding RNAs. Mol. Cell 43, 904-914. https://doi.org/10.1016/j.molcel.2011.08.018
  130. Wang, H., Chung, P.J., Liu, J., Jang, I.C., Kean, M.J., Xu, J., and Chua, N.H. (2014a). Genome-wide identification of long noncoding natural antisense transcripts and their responses to light in Arabidopsis. Genome Res. 24, 444-453. https://doi.org/10.1101/gr.165555.113
  131. Wang, Y., Fan, X., Lin, F., He, G., Terzaghi, W., Zhu, D., and Deng, X.W. (2014b). Arabidopsis noncoding RNA mediates control of photomorphogenesis by red light. Proc. Natl. Acad. Sci. USA 111, 10359-10364. https://doi.org/10.1073/pnas.1409457111
  132. Wang, Z.W., Wu, Z., Raitskin, O., Sun, Q., and Dean, C. (2014c). Antisense-mediated FLC transcriptional repression requires the P-TEFb transcription elongation factor. Proc. Natl. Acad. Sci. USA 111, 7468-7473. https://doi.org/10.1073/pnas.1406635111
  133. Weake, V.M., and Workman, J.L. (2008). Histone ubiquitination: triggering gene activity. Mol. Cell 29, 653-663. https://doi.org/10.1016/j.molcel.2008.02.014
  134. Weinhofer, I., Hehenberger, E., Roszak, P., Hennig, L., and Kohler, C. (2010). H3K27me3 profiling of the endosperm implies exclusion of polycomb group protein targeting by DNA methylation. PLoS Genet. 6.
  135. Woo, C.J., Kharchenko, P.V., Daheron, L., Park, P.J., and Kingston, R.E. (2010). A region of the human HOXD cluster that confers polycomb-group responsiveness. Cell 140, 99-110. https://doi.org/10.1016/j.cell.2009.12.022
  136. Xu, L., and Shen, W.H. (2008). Polycomb silencing of KNOX genes confines shoot stem cell niches in Arabidopsis. Curr. Biol. 18, 1966-1971. https://doi.org/10.1016/j.cub.2008.11.019
  137. Yang, C., Bratzel, F., Hohmann, N., Koch, M., Turck, F., and Calonje, M. (2013). VAL- and AtBMI1-mediated H2Aub initiate the switch from embryonic to postgerminative growth in Arabidopsis. Curr. Biol. 23, 1324-1329. https://doi.org/10.1016/j.cub.2013.05.050
  138. Yang, H., Howard, M., and Dean, C. (2014a). Antagonistic roles for H3K36me3 and H3K27me3 in the cold-induced epigenetic switch at Arabidopsis FLC. Curr. Biol. 24, 1793-1797. https://doi.org/10.1016/j.cub.2014.06.047
  139. Yang, Y.W., Flynn, R.A., Chen, Y., Qu, K., Wan, B., Wang, K.C., Lei, M., and Chang, H.Y. (2014b). Essential role of lncRNA binding for WDR5 maintenance of active chromatin and embryonic stem cell pluripotency. eLife 3, e02046.
  140. Zhang, X., Bernatavichute, Y.V., Cokus, S., Pellegrini, M., and Jacobsen, S.E. (2009). Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol. 10, R62. https://doi.org/10.1186/gb-2009-10-6-r62
  141. Yuan, W., Xu, M., Huang, C., Liu, N., Chen, S., and Zhu, B. (2011). H3K36 methylation antagonizes PRC2-mediated H3K27 methylation. J. Biol. Chem. 286, 7983-7989. https://doi.org/10.1074/jbc.M110.194027
  142. Yun, J.Y., Tamada, Y., Kang, Y.E., and Amasino, R.M. (2012). ARABIDOPSIS TRITHORAX-RELATED3/SET DOMAIN GROUP2 is required for the winter-annual habit of Arabidopsis thaliana. Plant Cell Physiol. 53, 834-846. https://doi.org/10.1093/pcp/pcs021
  143. Zhang, X., Germann, S., Blus, B.J., Khorasanizadeh, S., Gaudin, V., and Jacobsen, S.E. (2007). The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trimethylation. Nat. Struct. Mol. Biol. 14, 869-871. https://doi.org/10.1038/nsmb1283
  144. Zhao, Z., Yu, Y., Meyer, D., Wu, C., and Shen, W.H. (2005). Prevention of early flowering by expression of FLOWERING LOCUS C requires methylation of histone H3 K36. Nat. Cell Biol. 7, 1256-1260. https://doi.org/10.1038/ncb1329
  145. Zhao, J., Sun, B.K., Erwin, J.A., Song, J.J., and Lee, J.T. (2008). Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322, 750-756. https://doi.org/10.1126/science.1163045
  146. Zhao, J., Ohsumi, T.K., Kung, J.T., Ogawa, Y., Grau, D.J., Sarma, K., Song, J.J., Kingston, R.E., Borowsky, M., and Lee, J.T. (2010). Genome-wide identification of polycomb-associated RNAs by RIP-seq. Mol. Cell 40, 939-953. https://doi.org/10.1016/j.molcel.2010.12.011

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