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http://dx.doi.org/10.14348/molcells.2014.0249

Polycomb-Mediated Gene Silencing in Arabidopsis thaliana  

Kim, Dong-Hwan (Department of Molecular Biosciences, Institute for Cellular and Molecular Biology, The University of Texas at Austin)
Sung, Sibum (Department of Molecular Biosciences, Institute for Cellular and Molecular Biology, The University of Texas at Austin)
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;
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1 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.   DOI   ScienceOn
2 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.   DOI   ScienceOn
3 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.   DOI   ScienceOn
4 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.   DOI   ScienceOn
5 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.   DOI   ScienceOn
6 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.   DOI   ScienceOn
7 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.   DOI   ScienceOn
8 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.   DOI   ScienceOn
9 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.   DOI   ScienceOn
10 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.   DOI   ScienceOn
11 Lewis, E.B. (1978). A gene complex controlling segmentation in Drosophila. Nature 276, 565-570.   DOI   ScienceOn
12 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.   DOI   ScienceOn
13 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.   DOI   ScienceOn
14 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.   DOI   ScienceOn
15 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.   DOI   ScienceOn
16 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.   DOI   ScienceOn
17 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.   DOI   ScienceOn
18 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.   DOI
19 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.   DOI   ScienceOn
20 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.   DOI   ScienceOn
21 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.   DOI   ScienceOn
22 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.   DOI   ScienceOn
23 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.   DOI   ScienceOn
24 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.   DOI   ScienceOn
25 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.   DOI
26 Heo, J.B., and Sung, S. (2011). Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331, 76-79.   DOI   ScienceOn
27 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.   DOI   ScienceOn
28 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.   DOI   ScienceOn
29 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.   DOI   ScienceOn
30 Dekker, J., Rippe, K., Dekker, M., and Kleckner, N. (2002). Capturing chromosome conformation. Science 295, 1306-1311.   DOI   ScienceOn
31 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.   DOI
32 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.   DOI   ScienceOn
33 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.   DOI   ScienceOn
34 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.   DOI   ScienceOn
35 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.   DOI   ScienceOn
36 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.   DOI   ScienceOn
37 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.
38 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.   DOI   ScienceOn
39 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.   DOI   ScienceOn
40 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.   DOI   ScienceOn
41 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.   DOI   ScienceOn
42 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.   DOI   ScienceOn
43 Cheutin, T., and Cavalli, G. (2014). Polycomb silencing: from linear chromatin domains to 3D chromosome folding. Curr. Opin. Genet. Dev. 25, 30-37.   DOI   ScienceOn
44 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.   DOI   ScienceOn
45 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.
46 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.   DOI   ScienceOn
47 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.   DOI   ScienceOn
48 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.
49 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.   DOI   ScienceOn
50 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.   DOI   ScienceOn
51 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.   DOI   ScienceOn
52 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.   DOI   ScienceOn
53 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.   DOI
54 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.   DOI   ScienceOn
55 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.   DOI   ScienceOn
56 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.   DOI   ScienceOn
57 Bowman, J.L., Smyth, D.R., and Meyerowitz, E.M. (1989). Genes directing flower development in Arabidopsis. Plant Cell 1, 37-52.   DOI   ScienceOn
58 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.   DOI   ScienceOn
59 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.   DOI   ScienceOn
60 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.   DOI   ScienceOn
61 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.   DOI   ScienceOn
62 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.   DOI   ScienceOn
63 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.   DOI   ScienceOn
64 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.   DOI   ScienceOn
65 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.   DOI   ScienceOn
66 Wang, K.C., and Chang, H.Y. (2011). Molecular mechanisms of long noncoding RNAs. Mol. Cell 43, 904-914.   DOI   ScienceOn
67 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.   DOI   ScienceOn
68 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.   DOI   ScienceOn
69 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.
70 Bantignies, F., and Cavalli, G. (2011). Polycomb group proteins: repression in 3D. Trends Genet. 27, 454-464.   DOI   ScienceOn
71 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.   DOI   ScienceOn
72 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.   DOI   ScienceOn
73 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.
74 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.   DOI   ScienceOn
75 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.   DOI   ScienceOn
76 Weake, V.M., and Workman, J.L. (2008). Histone ubiquitination: triggering gene activity. Mol. Cell 29, 653-663.   DOI   ScienceOn
77 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.   DOI   ScienceOn
78 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.   DOI   ScienceOn
79 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.
80 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.   DOI   ScienceOn
81 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.   DOI   ScienceOn
82 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.   DOI   ScienceOn
83 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.   DOI   ScienceOn
84 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.
85 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.   DOI
86 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.   DOI   ScienceOn
87 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.   DOI   ScienceOn
88 Smalle, J., and Vierstra, R.D. (2004). The ubiquitin 26S proteasome proteolytic pathway. Ann. Rev. Plant Biol. 55, 555-590.   DOI   ScienceOn
89 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.
90 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.
91 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.   DOI   ScienceOn
92 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.   DOI   ScienceOn
93 Struhl, G., and Akam, M. (1985). Altered distributions of Ultrabithorax transcripts in extra sex combs mutant embryos of Drosophila. EMBO J. 4, 3259-3264.
94 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.   DOI   ScienceOn
95 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.   DOI   ScienceOn
96 Sung, S., and Amasino, R.M. (2004). Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427, 159-164.   DOI   ScienceOn
97 Schuettengruber, B., Chourrout, D., Vervoort, M., Leblanc, B., and Cavalli, G. (2007). Genome regulation by polycomb and trithorax proteins. Cell 128, 735-745.   DOI   ScienceOn
98 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.   DOI   ScienceOn
99 Schwartz, Y.B., and Pirrotta, V. (2007). Polycomb silencing mechanisms and the management of genomic programmes. Nat. Rev. Genet. 8, 9-22.
100 Schwartz, Y.B., and Pirrotta, V. (2008). Polycomb complexes and epigenetic states. Curr. Opin. Plant Biol. 20, 266-273.   DOI   ScienceOn
101 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.   DOI   ScienceOn
102 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.
103 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.
104 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.   DOI   ScienceOn
105 Simon, J.A., and Kingston, R.E. (2009). Mechanisms of polycomb gene silencing: knowns and unknowns. Nat. Rev. Mol. Cell Biol. 10, 697-708.   DOI
106 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.   DOI   ScienceOn
107 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.   DOI   ScienceOn
108 Rinn, J.L., and Chang, H.Y. (2012). Genome regulation by long noncoding RNAs. Ann. Rev. Biochem. 81, 145-166.   DOI   ScienceOn
109 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.   DOI   ScienceOn
110 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.   DOI   ScienceOn
111 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.   DOI   ScienceOn
112 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.   DOI   ScienceOn
113 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.   DOI   ScienceOn
114 Schubert, D., Clarenz, O., and Goodrich, J. (2005). Epigenetic control of plant development by Polycomb-group proteins. Curr. Opin. Plant Biol. 8, 553-561.   DOI   ScienceOn
115 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.   DOI
116 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.   DOI   ScienceOn
117 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.   DOI   ScienceOn
118 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.   DOI   ScienceOn
119 Pien, S., and Grossniklaus, U. (2007). Polycomb group and trithorax group proteins in Arabidopsis. Biochim. Biophys. Acta 1769, 375-382.   DOI   ScienceOn
120 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.   DOI   ScienceOn
121 Pirrotta, V. (1997). Chromatin-silencing mechanisms in Drosophila maintain patterns of gene expression. Trends Genet. 13, 314-318.   DOI   ScienceOn
122 Ringrose, L., and Paro, R. (2004). Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins. Ann. Rev. Genet. 38, 413-443.   DOI   ScienceOn
123 Mercer, T.R., and Mattick, J.S. (2013). Understanding the regulatory and transcriptional complexity of the genome through structure. Genome Res. 23, 1081-1088.   DOI   ScienceOn
124 Margueron, R., and Reinberg, D. (2011). The Polycomb complex PRC2 and its mark in life. Nature 469, 343-349.   DOI   ScienceOn
125 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.   DOI   ScienceOn
126 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.   DOI   ScienceOn
127 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.   DOI
128 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.   DOI   ScienceOn
129 Molitor, A., and Shen, W.H. (2013). The polycomb complex PRC1: composition and function in plants. J. Genet. Genomics 40, 231-238.   DOI   ScienceOn
130 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.   DOI
131 Muller, R., and Goodrich, J. (2011). Sweet memories: epigenetic control in flowering. F1000 Biol. Rep. 3, 13.
132 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.   DOI
133 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.   DOI   ScienceOn
134 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.   DOI   ScienceOn
135 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.   DOI   ScienceOn
136 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.   DOI   ScienceOn
137 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.   DOI   ScienceOn
138 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.   DOI   ScienceOn
139 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.   DOI   ScienceOn
140 Xu, L., and Shen, W.H. (2008). Polycomb silencing of KNOX genes confines shoot stem cell niches in Arabidopsis. Curr. Biol. 18, 1966-1971.   DOI   ScienceOn
141 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.   DOI   ScienceOn
142 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.   DOI   ScienceOn
143 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.   DOI   ScienceOn
144 He, C., Huang, H., and Xu, L. (2013). Mechanisms guiding Polycomb activities during gene silencing in Arabidopsis thaliana. Front. Plant Sci. 4, 454.
145 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.   DOI   ScienceOn
146 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.   DOI