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Unraveling the Complex Epigenetic Mechanisms that Regulate Gene Activity

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Book cover Plant Chromatin Dynamics

Part of the book series: Methods in Molecular Biology ((MIMB,volume 1675))

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.

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References

  1. 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

    Google Scholar 

  2. 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

    Google Scholar 

  3. 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

    Google Scholar 

  4. 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

    Google Scholar 

  5. 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

    Google Scholar 

  6. 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

    Google Scholar 

  7. 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

    Google Scholar 

  8. 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

    Google Scholar 

  9. 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

    Google Scholar 

  10. 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

    Google Scholar 

  11. 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

    Google Scholar 

  12. 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

    Google Scholar 

  13. 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

    Google Scholar 

  14. 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

    Google Scholar 

  15. 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

    Google Scholar 

  16. 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

    Article  CAS  PubMed  Google Scholar 

  17. 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

    Google Scholar 

  18. 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

    Google Scholar 

  19. 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

  20. 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

    PubMed  PubMed Central  Google Scholar 

  21. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. 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

    Article  CAS  PubMed  Google Scholar 

  23. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. 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

  25. 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

    CAS  PubMed  PubMed Central  Google Scholar 

  26. 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

    Article  CAS  PubMed  Google Scholar 

  27. 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

    Article  PubMed  PubMed Central  Google Scholar 

  28. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. 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

    Article  CAS  PubMed  Google Scholar 

  30. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. 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

    Google Scholar 

  37. Merini W, Calonje M (2015) PRC1 is taking the lead in PcG repression. Plant J 83(1):110–120. doi:10.1111/tpj.12818

    Article  CAS  PubMed  Google Scholar 

  38. 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

    Article  CAS  PubMed  Google Scholar 

  39. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. 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

    Article  CAS  PubMed  Google Scholar 

  42. 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

    Article  CAS  PubMed  Google Scholar 

  43. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. 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

    CAS  PubMed  PubMed Central  Google Scholar 

  45. 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

    Google Scholar 

  46. 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

    Article  CAS  PubMed  Google Scholar 

  47. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. To TK, Saze H, Kakutani T (2015) DNA methylation within transcribed regions. Plant Physiol 168(4):1219–1225. doi:10.1104/pp.15.00543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. 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

    Article  CAS  PubMed  Google Scholar 

  50. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. 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

    Article  CAS  PubMed  Google Scholar 

  57. 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

    Google Scholar 

  58. 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

    Google Scholar 

  59. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. 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

    Article  CAS  PubMed  Google Scholar 

  61. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. 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

    Article  CAS  PubMed  Google Scholar 

  66. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. 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

    Article  CAS  PubMed  Google Scholar 

  70. 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

  71. 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

    Article  CAS  PubMed  Google Scholar 

  72. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. 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

    Article  CAS  PubMed  Google Scholar 

  75. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. 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

    Article  CAS  PubMed  Google Scholar 

  77. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. 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

    Article  PubMed  CAS  Google Scholar 

  81. 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

    Article  PubMed  CAS  Google Scholar 

  82. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. 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

    Article  CAS  PubMed Central  Google Scholar 

  84. 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

  85. 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

    CAS  PubMed  Google Scholar 

  86. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. 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

    Article  CAS  PubMed  Google Scholar 

  88. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. 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

    Article  PubMed  CAS  Google Scholar 

  90. 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

  91. 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

    Article  CAS  PubMed  Google Scholar 

  92. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. 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

    CAS  PubMed  PubMed Central  Google Scholar 

  94. 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

    Article  PubMed  PubMed Central  Google Scholar 

  95. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. 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

    Article  CAS  PubMed  Google Scholar 

  97. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. 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

    CAS  PubMed  Google Scholar 

  99. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  102. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  103. Hehenberger E, Kradolfer D, Köhler C (2012) Endosperm cellularization defines an important developmental transition for embryo development. Development 139(11):2031

    Article  CAS  PubMed  Google Scholar 

  104. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. 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

    Article  CAS  PubMed  Google Scholar 

  107. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. 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

    Article  PubMed  PubMed Central  Google Scholar 

  112. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  113. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. 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

    Article  CAS  PubMed  Google Scholar 

  116. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. 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

    Article  CAS  PubMed  Google Scholar 

  119. 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

    Article  PubMed  CAS  Google Scholar 

  120. 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

    Article  PubMed  PubMed Central  Google Scholar 

  121. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. 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

    Article  CAS  PubMed  Google Scholar 

  123. 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

    Article  PubMed Central  CAS  Google Scholar 

  124. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  125. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  126. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  127. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  128. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  129. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. 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

    Article  CAS  PubMed  Google Scholar 

  135. 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

    Article  CAS  PubMed  Google Scholar 

  136. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. 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

    Google Scholar 

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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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