Abstract
Our understanding of the epigenetic mechanisms that regulate gene expression has been largely increased in recent years by the development and refinement of different techniques. This has revealed that gene transcription is highly influenced by epigenetic mechanisms, i.e., those that do not involve changes in the genome sequence, but rather in nuclear architecture, chromosome conformation and histone and DNA modifications. Our understanding of how these different levels of epigenetic regulation interact with each other and with classical transcription-factor based gene regulation to influence gene transcription has just started to emerge. This review discusses the latest advances in unraveling the complex interactions between different types of epigenetic regulation and transcription factor activity, with special attention to the approaches that can be used to study these interactions.
References
Pajoro A, Muiño JM, Angenent GC, Kaufmann K (2017) Profiling nucleosome occupancy by MNase-seq: experimental protocol and computational analysis. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols. Springer, New York, NY. doi:10.1007/978-1-4939-7318-7_11
Bajic M, Maher KA, Deal RB (2017) Identification of open chromatin regions in plant genomes using ATAC-Seq. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols. Springer, New York, NY. doi:10.1007/978-1-4939-7318-7_12
Chen Y-R, Yu S, Zhong S (2017) Profiling DNA methylation using bisulfite sequencing (BS-Seq). In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols. Springer, New York, NY. doi:10.1007/978-1-4939-7318-7_2
Edelmann S, Scholten S (2017) Bisulphite sequencing using small DNA amounts. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols. Springer, New York, NY. doi:10.1007/978-1-4939-7318-7_3
Kishore K, Pelizzola M (2017) Identification of differentially methylated regions in the genome of Arabidopsis thaliana. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols. Springer, New York, NY. doi:10.1007/978-1-4939-7318-7_4
Desvoyes B, Vergara Z, Sequeira-Mendes J, Madeira S, Gutierrez C (2017) A rapid and efficient ChIP protocol to profile chromatin binding proteins and epigenetic modifications in Arabidopsis. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols. Springer, New York, NY. doi:10.1007/978-1-4939-7318-7_5
Desvoyes B, Sequeira-Mendes J, Vergara Z, Madeira S, Gutierrez C (2017) Sequential ChIP protocol for profiling bivalent epigenetic modifications (ReChIP). In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols. Springer, New York, NY. doi:10.1007/978-1-4939-7318-7_6
Morao AK, Caillieux E, Colot V, Roudier F (2017) Cell type-specific profiling of chromatin modifications and associated proteins. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols. Springer, New York, NY. doi:10.1007/978-1-4939-7318-7_8
Engelhorn J, Wellmer F, Carles CC (2017) Profiling histone modifications in synchronised floral tissues for quantitative resolution of chromatin and transcriptome dynamics. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols. Springer, New York, NY. doi:10.1007/978-1-4939-7318-7_16
Grob S, Cavalli G (2017) A Hitchhiker’s guide to chromosome conformation capture. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols. Springer, New York, NY. doi:10.1007/978-1-4939-7318-7_14
Weber B, Jamge S, Stam ME (2017) 3C in maize and Arabidopsis. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols. Springer, New York, NY. doi:10.1007/978-1-4939-7318-7_15
Jamge S, Angenent GC, Bemer M (2017) Identification of in planta protein-protein interactions using IP-MS. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols. Springer, New York, NY. doi:10.1007/978-1-4939-7318-7_18
Lunardon A, Forestan C, Farinati S, Varotto S (2017) De novo identification of sRNA loci and non-coding RNAs by high-throughput sequencing. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols. Springer, New York, NY. doi:10.1007/978-1-4939-7318-7_17
Mermaz B, Liu F, Song J (2017) RNA ImmunoPrecipitation protocol to profile RNA-binding proteins in Arabidopsis thaliana. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols. Springer, New York, NY. doi:10.1007/978-1-4939-7318-7_19
Jacob Y, Voigt P (2017) In vitro assays to measure histone methyltransferase activity using different chromatin substrates. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols. Springer, New York, NY. doi:10.1007/978-1-4939-7318-7_20
Over RS, Michaels SD (2014) Open and closed: the roles of linker histones in plants and animals. Mol Plant 7(3):481–491. doi:10.1093/mp/sst164
Probst AV (2017) A compendium of methods to analyze the spatial organization of plant chromatin. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols. Springer, New York, NY. doi:10.1007/978-1-4939-7318-7_23
She W, Baroux C, Grossniklaus U (2017) Cell-type specific chromatin analysis in whole-mount plant tissues by immunostaining. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols. Springer, New York, NY. doi:10.1007/978-1-4939-7318-7_25
Rodriguez-Granados NY, Ramirez-Prado JS, Veluchamy A, Latrasse D, Raynaud C, Crespi M, Ariel F, Benhamed M (2016) Put your 3D glasses on: plant chromatin is on show. J Exp Bot. doi:10.1093/jxb/erw168
Feng C-M, Qiu Y, Van Buskirk EK, Yang EJ, Chen M (2014) Light-regulated gene repositioning in Arabidopsis. Nat Commun 5:3027–3027. doi:10.1038/ncomms4027
Bourbousse C, Mestiri I, Zabulon G, Bourge M, Formiggini F, Koini MA, Brown SC, Fransz P, Bowler C, Barneche F (2015) Light signaling controls nuclear architecture reorganization during seedling establishment. Proc Natl Acad Sci U S A 112(21):E2836–E2844. doi:10.1073/pnas.1503512112
Han S-K, Wu M-F, Cui S, Wagner D (2015) Roles and activities of chromatin remodeling ATPases in plants. Plant J 83(1):62–77. doi:10.1111/tpj.12877
Liang SC, Hartwig B, Perera P, Mora-García S, de Leau E, Thornton H, de Alves FL, Rapsilber J, Yang S, James GV, Schneeberger K, Finnegan EJ, Turck F, Goodrich J (2015) Kicking against the PRCs – a domesticated transposase antagonises silencing mediated by Polycomb group proteins and is an accessory component of Polycomb repressive complex 2. PLoS Genet 11(12):e1005660
Sura W, Kabza M, Karlowski WM, Bieluszewski T, Kuś-Slowinska M, Pawełoszek Ł, Sadowski J, Ziolkowski PA (2017) Dual role of the histone variant H2A.Z in transcriptional regulation of stress-response genes. Plant Cell. doi:10.1105/tpc.16.00573
Rutowicz K, Puzio M, Halibart-Puzio J, Lirski M, Kotliński M, Kroteń MA, Knizewski L, Lange B, Muszewska A, Śniegowska-Świerk K, Kościelniak J, Iwanicka-Nowicka R, Buza K, Janowiak F, Żmuda K, Jõesaar I, Laskowska-Kaszub K, Fogtman A, Kollist H, Zielenkiewicz P, Tiuryn J, Siedlecki P, Swiezewski S, Ginalski K, Koblowska M, Archacki R, Wilczynski B, Rapacz M, Jerzmanowski A (2015) A specialized histone H1 variant is required for adaptive responses to complex abiotic stress and related DNA methylation in Arabidopsis. Plant Physiol 169(3):2080–2101. doi:10.1104/pp.15.00493
She W, Grimanelli D, Rutowicz K, Whitehead MWJ, Puzio M, Kotliński M, Jerzmanowski A, Baroux C (2013) Chromatin reprogramming during the somatic-to-reproductive cell fate transition in plants. Development 140(19):4008
She W, Baroux C (2015) Chromatin dynamics in pollen mother cells underpin a common scenario at the somatic-to-reproductive fate transition of both the male and female lineages in Arabidopsis. Front Plant Sci 6:294. doi:10.3389/fpls.2015.00294
Wu M-F, Sang Y, Bezhani S, Yamaguchi N, Han S-K, Li Z, Su Y, Slewinski TL, Wagner D (2012) SWI2/SNF2 chromatin remodeling ATPases overcome Polycomb repression and control floral organ identity with the LEAFY and SEPALLATA3 transcription factors. Proc Natl Acad Sci U S A 109(9):3576–3581. doi:10.1073/pnas.1113409109
Bemer M, Grossniklaus U (2012) Dynamic regulation of Polycomb group activity during plant development. Curr Opin Plant Biol 15(5):523–529. doi:10.1016/j.pbi.2012.09.006
Kotliński M, Rutowicz K, Kniżewski Ł, Palusiński A, Olędzki J, Fogtman A, Rubel T, Koblowska M, Dadlez M, Ginalski K, Jerzmanowski A (2016) Histone H1 variants in Arabidopsis are subject to numerous post-translational modifications, both conserved and previously unknown in histones, suggesting complex functions of H1 in plants. PLoS One 11(1):e0147908. doi:10.1371/journal.pone.0147908
Roudier F, Ahmed I, Bérard C, Sarazin A, Mary-Huard T, Cortijo S, Bouyer D, Caillieux E, Duvernois-Berthet E, Al-Shikhley L, Giraut L, Després B, Drevensek S, Barneche F, Dèrozier S, Brunaud V, Aubourg S, Schnittger A, Bowler C, Martin-Magniette M-L, Robin S, Caboche M, Colot V (2011) Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J 30(10):1928–1938. doi:10.1038/emboj.2011.103
Sequeira-Mendes J, Aragüez I, Peiró R, Mendez-Giraldez R, Zhang X, Jacobsen SE, Bastolla U, Gutierrez C (2014) The functional topography of the Arabidopsis genome is organized in a reduced number of linear motifs of chromatin states. Plant Cell 26(6):2351–2366. doi:10.1105/tpc.114.124578
Müller-Xing R, Clarenz O, Pokorny L, Goodrich J, Schubert D (2014) Polycomb-group proteins and FLOWERING LOCUS T maintain commitment to flowering in Arabidopsis thaliana. Plant Cell 26(6):2457–2471. doi:10.1105/tpc.114.123323
Pajoro A, Madrigal P, Muiño JM, Matus JT, Jin J, Mecchia MA, Debernardi JM, Palatnik JF, Balazadeh S, Arif M, Ó’Maoiléidigh DS, Wellmer F, Krajewski P, Riechmann J-L, Angenent GC, Kaufmann K (2014) Dynamics of chromatin accessibility and gene regulation by MADS-domain transcription factors in flower development. Genome Biol 15(3):R41–R41. doi:10.1186/gb-2014-15-3-r41
Veluchamy A, Jégu T, Ariel F, Latrasse D, Mariappan KG, Kim S-K, Crespi M, Hirt H, Bergounioux C, Raynaud C, Benhamed M (2016) LHP1 regulates H3K27me3 spreading and shapes the three-dimensional conformation of the Arabidopsis genome. PLoS One 11(7):e0158936. doi:10.1371/journal.pone.0158936
Zhang W, Jiang J (2015) Genome-wide mapping of DNase I hypersensitive sites in plants. In: Alonso JM, Stepanova AN (eds) Plant functional genomics: methods and protocols. Springer, New York, pp 71–89. doi:10.1007/978-1-4939-2444-8_4
Merini W, Calonje M (2015) PRC1 is taking the lead in PcG repression. Plant J 83(1):110–120. doi:10.1111/tpj.12818
Yang C, Bratzel F, Hohmann N, Koch M, Turck F, Calonje M (2013) VAL- and AtBMI1-mediated H2Aub initiate the switch from embryonic to postgerminative growth in Arabidopsis. Curr Biol 23(14):1324–1329. doi:10.1016/j.cub.2013.05.050
Ng DWK, Wang T, Chandrasekharan MB, Aramayo R, Kertbundit S, Hall TC (2007) Plant SET domain-containing proteins: structure, function and regulation. Biochim Biophys Acta 1769(5–6):316–329. doi:10.1016/j.bbaexp.2007.04.003
Jiang D, Kong NC, Gu X, Li Z, He Y (2011) Arabidopsis COMPASS-like complexes mediate histone H3 lysine-4 trimethylation to control floral transition and plant development. PLoS Genet 7(3):e1001330. doi:10.1371/journal.pgen.1001330
Chen X, Hu Y, Zhou D-X (2011) Epigenetic gene regulation by plant Jumonji group of histone demethylase. Biochim Biophys Acta 1809(8):421–426. doi:10.1016/j.bbagrm.2011.03.004
Xiao J, Lee U-S, Wagner D (2016) Tug of war: adding and removing histone lysine methylation in Arabidopsis. Curr Opin Plant Biol 34:41–53. doi:10.1016/j.pbi.2016.08.002
Pandey R, Müller A, Napoli CA, Selinger DA, Pikaard CS, Richards EJ, Bender J, Mount DW, Jorgensen RA (2002) Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic Acids Res 30(23):5036–5055
Mahrez W, Arellano MST, Moreno-Romero J, Nakamura M, Shu H, Nanni P, Köhler C, Gruissem W, Hennig L (2016) H3K36ac is an evolutionary conserved plant histone modification that marks active genes. Plant Physiol 170(3):1566–1577. doi:10.1104/pp.15.01744
Mahrez W, Hennig L (2017) Mapping of histone modifications in plants by tandem mass spectrometry. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols. Springer, New York, NY. doi:10.1007/978-1-4939-7318-7_9
Berr A, Shafiq S, Shen W-H (2011) Histone modifications in transcriptional activation during plant development. Biochim Biophys Acta 1809(10):567–576. doi:10.1016/j.bbagrm.2011.07.001
Du J, Johnson LM, Jacobsen SE, Patel DJ (2015) DNA methylation pathways and their crosstalk with histone methylation. Nat Rev Mol Cell Biol 16(9):519–532. doi:10.1038/nrm4043
To TK, Saze H, Kakutani T (2015) DNA methylation within transcribed regions. Plant Physiol 168(4):1219–1225. doi:10.1104/pp.15.00543
Stroud H, Do T, Du J, Zhong X, Feng S, Johnson L, Patel DJ, Jacobsen SE (2014) Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat Struct Mol Biol 21(1):64–72. doi:10.1038/nsmb.2735
Soppe WJJ, Jasencakova Z, Houben A, Kakutani T, Meister A, Huang MS, Jacobsen SE, Schubert I, Fransz PF (2002) DNA methylation controls histone H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis. EMBO J 21(23):6549–6559. doi:10.1093/emboj/cdf657
Tran RK, Zilberman D, de Bustos C, Ditt RF, Henikoff JG, Lindroth AM, Delrow J, Boyle T, Kwong S, Bryson TD, Jacobsen SE, Henikoff S (2005) Chromatin and siRNA pathways cooperate to maintain DNA methylation of small transposable elements in Arabidopsis. Genome Biol 6(11):R90–R90. doi:10.1186/gb-2005-6-11-r90
Greenberg MVC, Deleris A, Hale CJ, Liu A, Feng S, Jacobsen SE (2013) Interplay between active chromatin marks and RNA-directed DNA methylation in Arabidopsis thaliana. PLoS Genet 9(11):e1003946. doi:10.1371/journal.pgen.1003946
Aufsatz W, Mette M, van der Winden J, Matzke M, Matzke AJM (2002) HDA6, a putative histone deacetylase needed to enhance DNA methylation induced by double-stranded RNA. EMBO J 21(24):6832–6841. doi:10.1093/emboj/cdf663
Tang K, Lang Z, Zhang H, Zhu J-K (2016) The DNA demethylase ROS1 targets genomic regions with distinct chromatin modifications. Nat Plants 2:16169. doi:10.1038/nplants.2016.169
Dowen RH, Pelizzola M, Schmitz RJ, Lister R, Dowen JM, Nery JR, Dixon JE, Ecker JR (2012) Widespread dynamic DNA methylation in response to biotic stress. Proc Natl Acad Sci U S A 109(32):E2183–E2191. doi:10.1073/pnas.1209329109
Zhang Y-Y, Fischer M, Colot V, Bossdorf O (2013) Epigenetic variation creates potential for evolution of plant phenotypic plasticity. New Phytol 197(1):314–322. doi:10.1111/nph.12010
Lauss K, Keurentjes JJB (2017) epiQTL mapping in Arabidopsis thaliana. In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols. Springer, New York, NY. doi:10.1007/978-1-4939-7318-7_22
Pires ND, Grossniklaus U (2017) Identification of parent-of-origin-dependent QTLs using bulk-segregant sequencing (Bulk-Seq). In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols. Springer, New York, NY. doi:10.1007/978-1-4939-7318-7_21
Feng S, Cokus SJ, Schubert V, Zhai J, Pellegrini M, Jacobsen SE (2014) Genome-wide Hi-C analyses in wild type and mutants reveal high-resolution chromatin interactions in Arabidopsis. Mol Cell 55(5):694–707. doi:10.1016/j.molcel.2014.07.008
Grob S, Schmid Marc W, Grossniklaus U (2014) Hi-C analysis in Arabidopsis identifies the KNOT, a structure with similarities to the flamenco locus of Drosophila. Mol Cell 55(5):678–693. doi:10.1016/j.molcel.2014.07.009
Liu C, Wang C, Wang G, Becker C, Zaidem M, Weigel D (2016) Genome-wide analysis of chromatin packing in Arabidopsis thaliana at single-gene resolution. Genome Res 26(8):1057–1068. doi:10.1101/gr.204032.116
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(3):832–842. doi:10.1105/tpc.108.064329
Cao S, Kumimoto RW, Gnesutta N, Calogero AM, Mantovani R, Holt BF (2014) A distal CCAAT/NUCLEAR FACTOR Y complex promotes chromatin looping at the FLOWERING LOCUS T promoter and regulates the timing of flowering in Arabidopsis. Plant Cell 26(3):1009–1017. doi:10.1105/tpc.113.120352
Jégu T, Latrasse D, Delarue M, Hirt H, Domenichini S, Ariel F, Crespi M, Bergounioux C, Raynaud C, 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(2):538–551. doi:10.1105/tpc.113.114454
Ariel F, Jegu T, Latrasse D, Romero-Barrios N, Christ A, Benhamed M, Crespi M (2014) Noncoding transcription by alternative RNA polymerases dynamically regulates an auxin-driven chromatin loop. Mol Cell 55(3):383–396. doi:10.1016/j.molcel.2014.06.011
Wang C, Liu C, Roqueiro D, Grimm D, Schwab R, Becker C, Lanz C, Weigel D (2015) Genome-wide analysis of local chromatin packing in Arabidopsis thaliana. Genome Res 25(2):246–256. doi:10.1101/gr.170332.113
Musselman CA, Lalonde M-E, Côté J, Kutateladze TG (2012) Perceiving the epigenetic landscape through histone readers. Nat Struct Mol Biol 19(12):1218–1227. doi:10.1038/nsmb.2436
Zhang T, Cooper S, Brockdorff N (2015) The interplay of histone modifications – writers that read. EMBO Rep 16(11):1467–1481. doi:10.15252/embr.201540945
Li Z, Jiang D, Fu X, Luo X, Liu R, He Y (2016) Coupling of histone methylation and RNA processing by the nuclear mRNA cap-binding complex. Nat Plants 2:16015. doi:10.1038/nplants.2016.15
Hecker A, Brand LH, Peter S, Simoncello N, Kilian J, Harter K, Gaudin V, Wanke D (2015) The Arabidopsis GAGA-binding factor BPC6 recruits PRC1 component LHP1 to GAGA DNA-motifs. Plant Physiol. doi:10.1104/pp.15.00409
Smaczniak C, Li N, Boeren S, America T, van Dongen W, Goerdayal SS, de Vries S, Angenent GC, Kaufmann K (2012) Proteomics-based identification of low-abundance signaling and regulatory protein complexes in native plant tissues. Nat Protoc 7(12):2144–2158
Davidovich C, Cech TR (2015) The recruitment of chromatin modifiers by long noncoding RNAs: lessons from PRC2. RNA 21(12):2007–2022. doi:10.1261/rna.053918.115
Zhu Y, Rowley MJ, Böhmdorfer G, Wierzbicki Andrzej T (2013) A SWI/SNF chromatin-remodeling complex acts in noncoding RNA-mediated transcriptional silencing. Mol Cell 49(2):298–309. doi:10.1016/j.molcel.2012.11.011
Bratzel F, López-Torrejón G, Koch M, Del Pozo JC, Calonje M (2010) Keeping cell identity in Arabidopsis requires PRC1 RING-finger homologs that catalyze H2A monoubiquitination. Curr Biol 20(20):1853–1859. doi:10.1016/j.cub.2010.09.046
Wang H, Liu C, Cheng J, Liu J, Zhang L, He C, Shen W-H, Jin H, Xu L, Zhang Y (2016) Arabidopsis flower and embryo developmental genes are repressed in seedlings by different combinations of Polycomb group proteins in association with distinct sets of Cis-regulatory elements. PLoS Genet 12(1):e1005771. doi:10.1371/journal.pgen.1005771
Wang Y, Gu X, Yuan W, Schmitz Robert J, He Y (2014) Photoperiodic control of the floral transition through a distinct Polycomb repressive complex. Dev Cell 28(6):727–736. doi:10.1016/j.devcel.2014.01.029
Calonje M, Sanchez R, Chen L, Sung ZR (2008) EMBRYONIC FLOWER1 participates in Polycomb group-mediated AG gene silencing in Arabidopsis. Plant Cell 20(2):277–291. doi:10.1105/tpc.106.049957
Kim SY, Lee J, Eshed-Williams L, Zilberman D, Sung ZR (2012) EMF1 and PRC2 cooperate to repress key regulators of Arabidopsis development. PLoS Genet 8(3):e1002512. doi:10.1371/journal.pgen.1002512
Derkacheva M, Steinbach Y, Wildhaber T, Mozgová I, Mahrez W, Nanni P, Bischof S, Gruissem W, Hennig L (2013) Arabidopsis MSI1 connects LHP1 to PRC2 complexes. EMBO J 32(14):2073–2085. doi:10.1038/emboj.2013.145
Del Olmo I, López-González L, Martín-Trillo MM, Martínez-Zapater JM, Piñeiro M, Jarillo JA (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(4):623–636. doi:10.1111/j.1365-313X.2009.04093.x
Hyun Y, Yun H, Park K, Ohr H, Lee O, Kim D-H, Sung S, Choi Y (2012) The catalytic subunit of Arabidopsis DNA polymerase α ensures stable maintenance of histone modification. Development 140(1):156
Latrasse D, Germann S, Houba-Hérin N, Dubois E, Bui-Prodhomme D, Hourcade D, Juul-Jensen T, Le Roux C, Majira A, Simoncello N, Granier F, Taconnat L, Renou J-P, Gaudin V (2011) Control of flowering and cell fate by LIF2, an RNA binding partner of the Polycomb complex component LHP1. PLoS One 6(1):e16592. doi:10.1371/journal.pone.0016592
Molitor AM, Latrasse D, Zytnicki M, Andrey P, Houba-Hérin N, Hachet M, Battail C, Del Prete S, Alberti A, Quesneville H, Gaudin V (2016) The Arabidopsis hnRNP-Q protein LIF2 and the PRC1 subunit LHP1 function in concert to regulate the transcription of stress-responsive genes. Plant Cell 28(9):2197–2211. doi:10.1105/tpc.16.00244
Merini W, Romero-Campero FJ, Gomez-Zambrano A, Zhou Y, Turck F, Calonje M (2016) The Arabidopsis Polycomb Repressive Complex 1 (PRC1) components AtBMI1A, B and C impact gene networks throughout all stages of plant development. Plant Physiol. doi:10.1104/pp.16.01259
Zhou Y, Hartwig B, James GV, Schneeberger K, Turck F (2016) Complementary activities of TELOMERE REPEAT BINDING proteins and Polycomb group complexes in transcriptional regulation of target genes. Plant Cell 28(1):87–101. doi:10.1105/tpc.15.00787
Zhou Y, Tan B, Luo M, Li Y, Liu C, Chen C, Yu C-W, Yang S, Dong S, Ruan J, Yuan L, Zhang Z, Zhao L, Li C, Chen H, Cui Y, Wu K, Huang S (2013) HISTONE DEACETYLASE19 interacts with HSL1 and participates in the repression of seed maturation genes in Arabidopsis seedlings. Plant Cell 25(1):134–148. doi:10.1105/tpc.112.096313
Chhun T, Chong SY, Park BS, Wong ECC, Yin J-L, Kim M, Chua N-H (2016) HSI2 repressor recruits MED13 and HDA6 to down-regulate seed maturation gene expression directly during Arabidopsis early seedling growth. Plant Cell Physiol 57(8):1689–1706. doi:10.1093/pcp/pcw095
Suzuki M, Wang HHY, McCarty DR (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(2):902–911. doi:10.1104/pp.106.092320
Qüesta JI, Song J, Geraldo N, An H, Dean C (2016) Arabidopsis transcriptional repressor VAL1 triggers Polycomb silencing at FLC during vernalization. Science 353(6298):485
Yuan W, Luo X, Li Z, Yang W, Wang Y, Liu R, Du J, He Y (2016) A cis cold memory element and a trans epigenome reader mediate Polycomb silencing of FLC by vernalization in Arabidopsis. Nat Genet, advance online publication. doi:10.1038/ng.3712
Yang Y, Li L, Qu L-J (2016) Plant Mediator complex and its critical functions in transcription regulation. J Integr Plant Biol 58(2):106–118. doi:10.1111/jipb.12377
Gillmor CS, Silva-Ortega CO, Willmann MR, Buendía-Monreal M, Poethig RS (2014) The Arabidopsis Mediator CDK8 module genes CCT (MED12) and GCT (MED13) are global regulators of developmental phase transitions. Development 141(23):4580–4589. doi:10.1242/dev.111229
Liao C-J, Lai Z, Lee S, Yun D-J, Mengiste T (2016) Arabidopsis HOOKLESS1 regulates responses to pathogens and abscisic acid through interaction with MED18 and acetylation of WRKY33 and ABI5 chromatin. Plant Cell 28(7):1662–1681. doi:10.1105/tpc.16.00105
Ding Y, Ndamukong I, Xu Z, Lapko H, Fromm M, Avramova Z (2012) ATX1-generated H3K4me3 is required for efficient elongation of transcription, not initiation, at ATX1-regulated genes. PLoS Genet 8(12):e1003111. doi:10.1371/journal.pgen.1003111
Gonzalez D, Bowen AJ, Carroll TS, Conlan RS (2007) The transcription corepressor LEUNIG interacts with the histone deacetylase HDA19 and mediator components MED14 (SWP) and CDK8 (HEN3) to repress transcription. Mol Cell Biol 27(15):5306–5315. doi:10.1128/mcb.01912-06
Causier B, Ashworth M, Guo W, Davies B (2012) The TOPLESS interactome: a framework for gene repression in Arabidopsis. Plant Physiol 158(1):423–438. doi:10.1104/pp.111.186999
Krogan NT, Hogan K, Long JA (2012) APETALA2 negatively regulates multiple floral organ identity genes in Arabidopsis by recruiting the co-repressor TOPLESS and the histone deacetylase HDA19. Development 139(22):4180–4190. doi:10.1242/dev.085407
Ryu H, Cho H, Bae W, Hwang I (2014) Control of early seedling development by BES1/TPL/HDA19-mediated epigenetic regulation of ABI3. Nat Commun 5:4138. doi:10.1038/ncomms5138
Vercruyssen L, Verkest A, Gonzalez N, Heyndrickx KS, Eeckhout D, Han S-K, Jégu T, Archacki R, Van Leene J, Andriankaja M, De Bodt S, Abeel T, Coppens F, Dhondt S, De Milde L, Vermeersch M, Maleux K, Gevaert K, Jerzmanowski A, Benhamed M, Wagner D, Vandepoele K, De Jaeger G, Inzé D (2014) ANGUSTIFOLIA3 binds to SWI/SNF chromatin remodeling complexes to regulate transcription during Arabidopsis leaf development. Plant Cell 26(1):210–229. doi:10.1105/tpc.113.115907
Park K, Kim MY, Vickers M, Park J-S, Hyun Y, Okamoto T, Zilberman D, Fischer RL, Feng X, Choi Y, Scholten S (2016) DNA demethylation is initiated in the central cells of Arabidopsis and rice. Proc Natl Acad Sci U S A 113(52):15138–15143. doi:10.1073/pnas.1619047114
Raissig MT, Bemer M, Baroux C, Grossniklaus U (2013) Genomic imprinting in the Arabidopsis embryo is partly regulated by PRC2. PLoS Genet 9(12):e1003862. doi:10.1371/journal.pgen.1003862
Pires ND, Bemer M, Müller LM, Baroux C, Spillane C, Grossniklaus U (2016) Quantitative genetics identifies cryptic genetic variation involved in the paternal regulation of seed development. PLoS Genet 12(1):e1005806. doi:10.1371/journal.pgen.1005806
Hehenberger E, Kradolfer D, Köhler C (2012) Endosperm cellularization defines an important developmental transition for embryo development. Development 139(11):2031
Roszak P, Köhler C (2011) Polycomb group proteins are required to couple seed coat initiation to fertilization. Proc Natl Acad Sci U S A 108(51):20826–20831. doi:10.1073/pnas.1117111108
Carter B, Henderson JT, Svedin E, Fiers M, McCarthy K, Smith A, Guo C, Bishop B, Zhang H, Riksen T, Shockley A, Dilkes BP, Boutilier K, Ogas J (2016) Cross-talk between sporophyte and gametophyte generations is promoted by CHD3 chromatin remodelers in Arabidopsis thaliana. Genetics 203(2):817
Derkacheva M, Liu S, Figueiredo DD, Gentry M, Mozgova I, Nanni P, Tang M, Mannervik M, Köhler C, Hennig L (2016) H2A deubiquitinases UBP12/13 are part of the Arabidopsis polycomb group protein system. Nat Plants 2:16126. doi:10.1038/nplants.2016.126
Luo M, Luo M-Z, Buzas D, Finnegan J, Helliwell C, Dennis ES, Peacock WJ, Chaudhury A (2008) UBIQUITIN-SPECIFIC PROTEASE 26 is required for seed development and the repression of PHERES1 in Arabidopsis. Genetics 180(1):229–236. doi:10.1534/genetics.108.091736
Dumbliauskas E, Lechner E, Jaciubek M, Berr A, Pazhouhandeh M, Alioua M, Cognat V, Brukhin V, Koncz C, Grossniklaus U, Molinier J, Genschik P (2011) The Arabidopsis CUL4–DDB1 complex interacts with MSI1 and is required to maintain MEDEA parental imprinting. EMBO J 30(4):731–743. doi:10.1038/emboj.2010.359
Pazhouhandeh M, Molinier J, Berr A, Genschik P (2011) MSI4/FVE interacts with CUL4–DDB1 and a PRC2-like complex to control epigenetic regulation of flowering time in Arabidopsis. Proc Natl Acad Sci U S A 108(8):3430–3435. doi:10.1073/pnas.1018242108
Gao M-J, Lydiate DJ, Li X, Lui H, Gjetvaj B, Hegedus DD, Rozwadowski K (2009) Repression of seed maturation genes by a trihelix transcriptional repressor in Arabidopsis seedlings. Plant Cell 21(1):54–71. doi:10.1105/tpc.108.061309
Gao M-J, Li X, Huang J, Gropp GM, Gjetvaj B, Lindsay DL, Wei S, Coutu C, Chen Z, Wan X-C, Hannoufa A, Lydiate DJ, Gruber MY, Chen ZJ, Hegedus DD (2015) SCARECROW-LIKE15 interacts with HISTONE DEACETYLASE19 and is essential for repressing the seed maturation programme. Nat Commun 6:7243. doi:10.1038/ncomms8243
Molitor AM, Bu Z, Yu Y, Shen W-H (2014) Arabidopsis AL PHD-PRC1 complexes promote seed germination through H3K4me3-to-H3K27me3 chromatin state switch in repression of seed developmental genes. PLoS Genet 10(1):e1004091. doi:10.1371/journal.pgen.1004091
Yang H, Howard M, Dean C (2016) Physical coupling of activation and derepression activities to maintain an active transcriptional state at FLC. Proc Natl Acad Sci U S A 113(33):9369–9374. doi:10.1073/pnas.1605733113
Choi K, Kim J, Hwang H-J, Kim S, Park C, Kim SY, Lee I (2011) The FRIGIDA complex activates transcription of FLC, a strong flowering repressor in Arabidopsis, by recruiting chromatin modification factors. Plant Cell 23(1):289–303. doi:10.1105/tpc.110.075911
Zhang C, Cao L, Rong L, An Z, Zhou W, Ma J, Shen W-H, Zhu Y, Dong A (2015) The chromatin-remodeling factor AtINO80 plays crucial roles in genome stability maintenance and in plant development. Plant J 82(4):655–668. doi:10.1111/tpj.12840
Kim SY, He Y, Jacob Y, Noh Y-S, Michaels S, Amasino R (2005) Establishment of the vernalization-responsive, winter-annual habit in Arabidopsis requires a putative histone H3 methyl transferase. Plant Cell 17(12):3301–3310. doi:10.1105/tpc.105.034645
He Y, Doyle MR, Amasino RM (2004) PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis. Genes Dev 18(22):2774–2784. doi:10.1101/gad.1244504
Wu Z, Ietswaart R, Liu F, Yang H, Howard M, Dean C (2016) Quantitative regulation of FLC via coordinated transcriptional initiation and elongation. Proc Natl Acad Sci U S A 113(1):218–223. doi:10.1073/pnas.1518369112
Crevillén P, Sonmez C, Wu Z, Dean C (2013) A gene loop containing the floral repressor FLC is disrupted in the early phase of vernalization. EMBO J 32(1):140–148. doi:10.1038/emboj.2012.324
De Lucia F, Crevillen P, Jones AME, Greb T, Dean C (2008) A PHD-Polycomb Repressive Complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc Natl Acad Sci U S A 105(44):16831–16836. doi:10.1073/pnas.0808687105
Angel A, Song J, Yang H, Questa JI, Dean C, Howard M (2015) Vernalizing cold is registered digitally at FLC. Proc Natl Acad Sci U S A 112(13):4146–4151. doi:10.1073/pnas.1503100112
Luo M, Tai R, Yu C-W, Yang S, Chen C-Y, Lin W-D, Schmidt W, Wu K (2015) Regulation of flowering time by the histone deacetylase HDA5 in Arabidopsis. Plant J 82(6):925–936. doi:10.1111/tpj.12868
Berry S, Hartley M, Olsson TSG, Dean C, Howard M (2015) Local chromatin environment of a Polycomb target gene instructs its own epigenetic inheritance. Elife 4:e07205. doi:10.7554/eLife.07205
Jiang D, Wang Y, Wang Y, He Y (2008) Repression of FLOWERING LOCUS C and FLOWERING LOCUS T by the Arabidopsis Polycomb Repressive Complex 2 components. PLoS One 3(10):e3404. doi:10.1371/journal.pone.0003404
López-González L, Mouriz A, Narro-Diego L, Bustos R, Martínez-Zapater JM, Jarillo JA, Piñeiro M (2014) Chromatin-dependent repression of the Arabidopsis floral integrator genes involves plant specific PHD-containing proteins. Plant Cell 26(10):3922–3938. doi:10.1105/tpc.114.130781
Olmo ID, López JA, Vázquez J, Raynaud C, Piñeiro M, Jarillo JA (2016) Arabidopsis DNA polymerase ε recruits components of Polycomb repressor complex to mediate epigenetic gene silencing. Nucleic Acids Res 44(12):5597–5614. doi:10.1093/nar/gkw156
Liu C, Weigel D (2015) Chromatin in 3D: progress and prospects for plants. Genome Biol 16(1):170. doi:10.1186/s13059-015-0738-6
Bu Z, Yu Y, Li Z, Liu Y, Jiang W, Huang Y, Dong A-W (2014) Regulation of Arabidopsis flowering by the histone mark readers MRG1/2 via interaction with CONSTANS to modulate FT expression. PLoS Genet 10(9):e1004617. doi:10.1371/journal.pgen.1004617
Xu Y, Gan E-S, Zhou J, Wee W-Y, Zhang X, Ito T (2014) Arabidopsis MRG domain proteins bridge two histone modifications to elevate expression of flowering genes. Nucleic Acids Res 42(17):10960–10974. doi:10.1093/nar/gku781
Liu X, Kim YJ, Müller R, Yumul RE, Liu C, Pan Y, Cao X, Goodrich J, Chen X (2011) AGAMOUS terminates floral stem cell maintenance in Arabidopsis by directly repressing WUSCHEL through recruitment of Polycomb group proteins. Plant Cell 23(10):3654–3670. doi:10.1105/tpc.111.091538
Liu X, Gao L, Dinh TT, Shi T, Li D, Wang R, Guo L, Xiao L, Chen X (2014) DNA topoisomerase I affects Polycomb group protein-mediated epigenetic regulation and plant development by altering nucleosome distribution in Arabidopsis. Plant Cell 26(7):2803–2817. doi:10.1105/tpc.114.124941
Smaczniak C, Immink RGH, Muiño JM, Blanvillain R, Busscher M, Busscher-Lange J, Dinh QD, Liu S, Westphal AH, Boeren S, Parcy F, Xu L, Carles CC, Angenent GC, Kaufmann K (2012) Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development. Proc Natl Acad Sci U S A 109(5):1560–1565. doi:10.1073/pnas.1112871109
Li C, Gu L, Gao L, Chen C, Wei C-Q, Qiu Q, Chien C-W, Wang S, Jiang L, Ai L-F, Chen C-Y, Yang S, Nguyen V, Qi Y, Snyder MP, Burlingame AL, Kohalmi SE, Huang S, Cao X, Wang Z-Y, Wu K, Chen X, Cui Y (2016) Concerted genomic targeting of H3K27 demethylase REF6 and chromatin-remodeling ATPase BRM in Arabidopsis. Nat Genet 48(6):687–693. doi:10.1038/ng.3555
Smaczniak C, Immink RGH, Angenent GC, Kaufmann K (2012) Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies. Development 139(17):3081
Monfared MM, Carles CC, Rossignol P, Pires HR, Fletcher JC (2013) The ULT1 and ULT2 trxG genes play overlapping roles in Arabidopsis development and gene regulation. Mol Plant 6(5):1564–1579. doi:10.1093/mp/sst041
Sacharowski SP, Gratkowska DM, Sarnowska EA, Kondrak P, Jancewicz I, Porri A, Bucior E, Rolicka AT, Franzen R, Kowalczyk J, Pawlikowska K, Huettel B, Torti S, Schmelzer E, Coupland G, Jerzmanowski A, Koncz C, Sarnowski TJ (2015) SWP73 subunits of Arabidopsis SWI/SNF chromatin remodeling complexes play distinct roles in leaf and flower development. Plant Cell 27(7):1889–1906. doi:10.1105/tpc.15.00233
Carpentier M-C, Picart-Picolo A, Pontvianne F (2017) A method to identify nucleolus-associated chromatin domains (NADs). In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols. Springer, New York, NY. doi:10.1007/978-1-4939-7318-7_7
Acknowledgments
The author is very grateful to Kim Boutilier (WUR, Wageningen, the Netherlands) and Fredy Barneche (IBENS, Paris, France) for their critical reading of the manuscript and their helpful suggestions. This work was supported by a Dutch NWO-Veni grant.
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Bemer, M. (2018). Unraveling the Complex Epigenetic Mechanisms that Regulate Gene Activity. In: Bemer, M., Baroux, C. (eds) Plant Chromatin Dynamics. Methods in Molecular Biology, vol 1675. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-7318-7_13
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