Profiling Developmentally and Environmentally Controlled Chromatin Reprogramming

  • Clara Bourbousse
  • Moussa Benhamed
  • Fredy BarnecheEmail author
Part of the Methods in Molecular Biology book series (MIMB, volume 1675)


Dynamic reshuffling of the chromatin landscape is a recurrent theme orchestrated in many, if not all, plant developmental transitions and adaptive responses. Spatiotemporal variations of the chromatin properties on regulatory genes and on structural genomic elements trigger the establishment of distinct transcriptional contexts, which in some instances can epigenetically be inherited. Studies on plant cell plasticity during the differentiation of stem cells, including gametogenesis, or the specialization of vegetative cells in various organs, as well as the investigation of allele-specific gene regulation have long been impaired by technical challenges in generating specific chromatin profiles in complex or hardly accessible cell populations. Recent advances in increasing the sensitivity of genome-enabled technologies and in the isolation of specific cell types have allowed for overcoming such limitations. These developments hint at multilevel regulatory events ranging from nucleosome accessibility and composition to higher order chromatin organization and genome topology. Uncovering the large extent to which chromatin dynamics and epigenetic processes influence gene expression is therefore not surprisingly revolutionizing current views on plant molecular genetics and (epi)genomics as well as their perspectives in eco-evolutionary biology. Here, we introduce current methodologies to probe genome-wide chromatin variations for which protocols are detailed in this book chapter, with an emphasis on the plant model species Arabidopsis.

Key words

Chromatin Histone DNA methylation Epigenome Methodology 



The authors thank Chris Bowler for constant support, Vincent Colot (IBENS, Paris France) and François Roudier (ENS, Lyon France) for helpful discussions and sharing unpublished data. They are also grateful to Damarys Loew (Curie Institute, Paris France) and Julie Law (Salk Institute for Biological Studies, San Diego USA) for helpful discussions. Work by the authors is supported by the CNRS, ANR-11-JSV2-003-01, Investissements d’Avenir Labex MEMOLIFE ANR-10-LABX-54 to FB, by PSL Research University to FB and CB, and by Université Paris-Saclay to MB.


  1. 1.
    Berger SL (2007) The complex language of chromatin regulation during transcription. Nature 447:407–412. doi: 10.1038/nature05915 PubMedCrossRefGoogle Scholar
  2. 2.
    Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693–705. doi: 10.1016/j.cell.2007.02.005 PubMedCrossRefGoogle Scholar
  3. 3.
    Li G, Zhu P (2015) Structure and organization of chromatin fiber in the nucleus. FEBS Lett 589:2893–2904. doi: 10.1016/j.febslet.2015.04.023 PubMedCrossRefGoogle Scholar
  4. 4.
    Richards EJ (2006) Inherited epigenetic variation—revisiting soft inheritance. Nat Rev Genet 7:395–401PubMedCrossRefGoogle Scholar
  5. 5.
    Richmond TJ, Finch JT, Rushton B, Rhodes D, Klug A (1984) Structure of the nucleosome core particle at 7 [angst] resolution. Nature 311:532–537. doi: 10.1038/311532a0 PubMedCrossRefGoogle Scholar
  6. 6.
    Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389:251–260. doi: 10.1038/38444 PubMedCrossRefGoogle Scholar
  7. 7.
    Jiang J, Zhang T, Zhang W (2015) Genome-wide nucleosome occupancy and positioning and their impact on gene expression and evolution in plants. Plant Physiol 168(4):1406. doi: 10.1104/pp.15.00125 PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Cutter AR, Hayes JJ (2015) A brief review of nucleosome structure. FEBS Lett 589:2914–2922. doi: 10.1016/j.febslet.2015.05.016 PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Jiang C, Pugh BF (2009) Nucleosome positioning and gene regulation: advances through genomics. Nat Rev Genet 10:161–172. doi: 10.1038/nrg2522 PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Fransz P, Soppe W, Schubert I (2003) Heterochromatin in interphase nuclei of Arabidopsis thaliana. Chromosome Res 11:227–240PubMedCrossRefGoogle Scholar
  11. 11.
    Fransz P, de Jong H (2011) From nucleosome to chromosome: a dynamic organization of genetic information. Plant J Cell Mol Biol 66:4–17. doi: 10.1111/j.1365-313X.2011.04526.x CrossRefGoogle Scholar
  12. 12.
    Struhl K, Segal E (2013) Determinants of nucleosome positioning. Nat Struct Mol Biol 20:267–273. doi: 10.1038/nsmb.2506 PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Liu M-J, Seddon AE, Tsai ZT-Y, Major IT, Floer M, Howe GA, Shiu S-H (2015) Determinants of nucleosome positioning and their influence on plant gene expression. Genome Res 25(8):1182. doi: 10.1101/gr.188680.114 PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Zaret KS, Carroll JS (2011) Pioneer transcription factors: establishing competence for gene expression. Genes Dev 25:2227–2241. doi: 10.1101/gad.176826.111 PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Zentner GE, Henikoff S (2012) Surveying the epigenomic landscape, one base at a time. Genome Biol 13:250. doi: 10.1186/gb-2012-13-10-250 PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Jiang D, Berger F (2016) Histone variants in plant transcriptional regulation. Biochim Biophys Acta. doi: 10.1016/j.bbagrm.2016.07.002
  17. 17.
    Huang H, Sabari BR, Garcia BA, Allis CD, Zhao Y (2014) SnapShot: histone modifications. Cell 159:458–458.e1. doi: 10.1016/j.cell.2014.09.037 PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Kornberg RD, Lorch Y (1999) Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98:285–294. doi: 10.1016/S0092-8674(00)81958-3 PubMedCrossRefGoogle Scholar
  19. 19.
    Feng J, Shen WH (2014) Dynamic regulation and function of histone monoubiquitination in plants. Front Plant Sci 5:83. doi: 10.3389/fpls.2014.00083 PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Shogren-Knaak M, Ishii H, Sun J-M, Pazin MJ, Davie JR, Peterson CL (2006) Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311:844–847. doi: 10.1126/science.1124000 PubMedCrossRefGoogle Scholar
  21. 21.
    Robinson PJ, An W, Routh A, Martino F, Chapman L, Roeder RG, Rhodes D (2008) 30 nm chromatin fibre decompaction requires both H4-K16 acetylation and linker histone eviction. J Mol Biol 381:816–825PubMedCrossRefGoogle Scholar
  22. 22.
    Fierz B, Chatterjee C, McGinty RK, Bar-Dagan M, Raleigh DP, Muir TW (2011) Histone H2B ubiquitylation disrupts local and higher-order chromatin compaction. Nat Chem Biol 7:113–119PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Smith E, Shilatifard A (2010) The chromatin signaling pathway: diverse mechanisms of recruitment of histone-modifying enzymes and varied biological outcomes. Mol Cell 40:689–701PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Krueger F, Kreck B, Franke A, Andrews SR (2012) DNA methylome analysis using short bisulfite sequencing data. Nat Methods 9:145–151. doi: 10.1038/nmeth.1828 PubMedCrossRefGoogle Scholar
  25. 25.
    Chen Y-R, Sheng Y, 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
  26. 26.
    Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204–220PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Feng S, Jacobsen SE (2011) Epigenetic modifications in plants: an evolutionary perspective. Curr Opin Plant Biol 14:179–186PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Baroux C, Raissig MT, Grossniklaus U (2011) Epigenetic regulation and reprogramming during gamete formation in plants. Curr Opin Genet Dev 21:124–133. doi: 10.1016/j.gde.2011.01.017 PubMedCrossRefGoogle Scholar
  29. 29.
    Jullien PE, Susaki D, Yelagandula R, Higashiyama T, Berger F (2012) DNA methylation dynamics during sexual reproduction in Arabidopsis thaliana. Curr Biol 22:1825–1830. doi: 10.1016/j.cub.2012.07.061 PubMedCrossRefGoogle Scholar
  30. 30.
    Bourc’his D, Voinnet O (2010) A small-RNA perspective on gametogenesis, fertilization, and early zygotic development. Science 330:617–622. doi: 10.1126/science.1194776 PubMedCrossRefGoogle Scholar
  31. 31.
    Berger F, Gaudin V (2003) Chromatin dynamics and Arabidopsis development. Chromosome Res 11:277–304PubMedCrossRefGoogle Scholar
  32. 32.
    Crevillen P, Dean C (2010) Regulation of the floral repressor gene FLC: the complexity of transcription in a chromatin context. Curr Opin Plant Biol 14:38–44PubMedCrossRefGoogle Scholar
  33. 33.
    Berr A, Shafiq S, Shen W-H (2011) Histone modifications in transcriptional activation during plant development. Biochim Biophys Acta 1809:567–576PubMedCrossRefGoogle Scholar
  34. 34.
    He G, Elling AA, Deng XW (2011) The epigenome and plant development. Annu Rev Plant Biol 62:411–435PubMedCrossRefGoogle Scholar
  35. 35.
    Grimanelli D, Roudier F (2013) Epigenetics and development in plants: green light to convergent innovations. Curr Top Dev Biol 104:189–222. doi: 10.1016/B978-0-12-416027-9.00006-1 PubMedCrossRefGoogle Scholar
  36. 36.
    Patel DJ, Wang Z (2013) Readout of epigenetic modifications. Annu Rev Biochem 82:81–118. doi: 10.1146/annurev-biochem-072711-165700 PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Liu C, Weigel D (2015) Chromatin in 3D: progress and prospects for plants. Genome Biol 16:170. doi: 10.1186/s13059-015-0738-6 PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Barneche F, Malapeira J, Mas P (2014) The impact of chromatin dynamics on plant light responses and circadian clock function. J Exp Bot 65:2895–2913. doi: 10.1093/jxb/eru011 PubMedCrossRefGoogle Scholar
  39. 39.
    Perrella G, Kaiserli E (2016) Light behind the curtain: photoregulation of nuclear architecture and chromatin dynamics in plants. New Phytol 212:908–919. doi: 10.1111/nph.14269 PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Sullivan AM, Arsovski AA, Lempe J, Bubb KL, Weirauch MT, Sabo PJ, Sandstrom R, Thurman RE, Neph S, Reynolds AP, Stergachis AB, Vernot B, Johnson AK, Haugen E, Sullivan ST, Thompson A, Neri FV 3rd, Weaver M, Diegel M, Mnaimneh S, Yang A, Hughes TR, Nemhauser JL, Queitsch C, Stamatoyannopoulos JA (2014) Mapping and dynamics of regulatory DNA and transcription factor networks in A. thaliana. Cell Rep 8:2015–2030. doi: 10.1016/j.celrep.2014.08.019 PubMedCrossRefGoogle Scholar
  41. 41.
    Charron J-BF, He H, Elling AA, Deng XW (2009) Dynamic landscapes of four histone modifications during deetiolation in Arabidopsis. Plant Cell 21:3732–3748PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Bourbousse C, Ahmed I, Roudier F, Zabulon G, Blondet E, Balzergue S, Colot V, Bowler C, Barneche F (2012) Histone H2B monoubiquitination facilitates the rapid modulation of gene expression during Arabidopsis photomorphogenesis. PLoS Genet 8:e1002825. doi: 10.1371/journal.pgen.1002825 PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Benhamed M, Bertrand C, Servet C, Zhou DX (2006) Arabidopsis GCN5, HD1, and TAF1/HAF2 interact to regulate histone acetylation required for light-responsive gene expression. Plant Cell 18:2893–2903PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Quint M, Delker C, Franklin KA, Wigge PA, Halliday KJ, van Zanten M (2016) Molecular and genetic control of plant thermomorphogenesis. Nat Plants 2:15190. doi: 10.1038/nplants.2015.190 PubMedCrossRefGoogle Scholar
  45. 45.
    March-Díaz R, Reyes JC (2009) The beauty of being a variant: H2A.Z and the SWR1 complex in plants. Mol Plant 2(7):565–577. doi: 10.1093/mp/ssp019 PubMedCrossRefGoogle Scholar
  46. 46.
    Kumar SV, Wigge PA (2010) H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140:136–147PubMedCrossRefGoogle Scholar
  47. 47.
    Kumar SV, Lucyshyn D, Jaeger KE, Alos E, Alvey E, Harberd NP, Wigge PA (2012) Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484:242–245. doi: 10.1038/nature10928 PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Coleman-Derr D, Zilberman D (2012) Deposition of histone variant H2A.Z within gene bodies regulates responsive genes. PLoS Genet 8:e1002988. doi: 10.1371/journal.pgen.1002988 PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Koike N, Yoo SH, Huang HC, Kumar V, Lee C, Kim TK, Takahashi JS (2012) Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science 338:349–354. doi: 10.1126/science.1226339 PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Baerenfaller K, Shu H, Hirsch-Hoffmann M, Fütterer J, Opitz L, Rehrauer H, Hennig L, Gruissem W (2016) Diurnal changes in the histone H3 signature H3K9ac|H3K27ac|H3S28p are associated with diurnal gene expression in Arabidopsis. Plant Cell Environ 39:2557–2569. doi: 10.1111/pce.12811 PubMedCrossRefGoogle Scholar
  51. 51.
    Seo PJ, Mas P (2015) STRESSing the role of the plant circadian clock. Trends Plant Sci 20:230–237. doi: 10.1016/j.tplants.2015.01.001 PubMedCrossRefGoogle Scholar
  52. 52.
    Filion GJ, van Bemmel JG, Braunschweig U, Talhout W, Kind J, Ward LD, Brugman W, de Castro IJ, Kerkhoven RM, Bussemaker HJ (2010) Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 143:212–224PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Roudier F, Ahmed I, Bérard C, Sarazin A, Mary-Huard T, Cortijo S, Bouyer D, Caillieux E, Duvernois-Berthet E, Al-Shikhley L (2011) Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J 30:1928–1938PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Sequeira-Mendes J, Araguez I, Peiro 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 26:2351–2366. doi: 10.1105/tpc.114.124578 PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Baker K, Dhillon T, Colas I, Cook N, Milne I, Milne L, Bayer M, Flavell AJ (2015) Chromatin state analysis of the barley epigenome reveals a higher-order structure defined by H3K27me1 and H3K27me3 abundance. Plant J 84:111–124. doi: 10.1111/tpj.12963 PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Bonev B, Cavalli G (2016) Organization and function of the 3D genome. Nat Rev Genet 17:661–678. doi: 10.1038/nrg.2016.112 PubMedCrossRefGoogle Scholar
  57. 57.
    Grob S, Schmid MW, Grossniklaus U (2014) Hi-C analysis in Arabidopsis identifies the KNOT, a structure with similarities to the flamenco locus of Drosophila. Mol Cell 55:678–693. doi: 10.1016/j.molcel.2014.07.009 PubMedCrossRefGoogle Scholar
  58. 58.
    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 55:694–707. doi: 10.1016/j.molcel.2014.07.008 PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    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:e0158936. doi: 10.1371/journal.pone.0158936 PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    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. doi: 10.1101/gr.204032.116 PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Wang C, Liu C, Roqueiro D, Grimm D, Schwab R, Becker C, Lanz C, Weigel D (2014) Genome-wide analysis of local chromatin packing in Arabidopsis thaliana. Genome Res 25(2):246. doi: 10.1101/gr.170332.113 PubMedCrossRefGoogle Scholar
  62. 62.
    Zhang Y, Wong C-H, Birnbaum RY, Li G, Favaro R, Ngan CY, Lim J, Tai E, Poh HM, Wong E, Mulawadi FH, Sung W-K, Nicolis S, Ahituv N, Ruan Y, Wei C-L (2013) Chromatin connectivity maps reveal dynamic promoter-enhancer long-range associations. Nature 504:306–310. doi: 10.1038/nature12716 PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    van Koningsbruggen S, Gierliński M, Schofield P, Martin D, Barton GJ, Ariyurek Y, den Dunnen JT, Lamond AI (2010) High-resolution whole-genome sequencing reveals that specific chromatin domains from most human chromosomes associate with nucleoli. Mol Biol Cell 21:3735–3748. doi: 10.1091/mbc.E10-06-0508 PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Németh A, Conesa A, Santoyo-Lopez J, Medina I, Montaner D, Péterfia B, Solovei I, Cremer T, Dopazo J, Längst G (2010) Initial genomics of the human nucleolus. PLoS Genet 6:e1000889. doi: 10.1371/journal.pgen.1000889 PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Pontvianne F, Carpentier M-C, Durut N, Pavlištová V, Jaške K, Schořová Š, Parrinello H, Rohmer M, Pikaard CS, Fojtová M, Fajkus J, Sáez-Vásquez J (2016) Identification of nucleolus-associated chromatin domains reveals a role for the nucleolus in 3D organization of the A. thaliana genome. Cell Rep 16:1574–1587. doi: 10.1016/j.celrep.2016.07.016 PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Pickersgill H, Kalverda B, de Wit E, Talhout W, Fornerod M, van Steensel B (2006) Characterization of the Drosophila melanogaster genome at the nuclear lamina. Nat Genet 38:1005–1014. doi: 10.1038/ng1852 PubMedCrossRefGoogle Scholar
  67. 67.
    Malapeira J, Khaitova LC, Mas P (2012) Ordered changes in histone modifications at the core of the Arabidopsis circadian clock. Proc Natl Acad Sci U S A 109:21540–21545. doi: 10.1073/pnas.1217022110 PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Takahashi N, Hirata Y, Aihara K, Mas P (2015) A hierarchical multi-oscillator network orchestrates the arabidopsis circadian system. Cell 163(1):148–159. doi: 10.1016/j.cell.2015.08.062 PubMedCrossRefGoogle Scholar
  69. 69.
    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
  70. 70.
    Deal RB, Henikoff S (2011) The INTACT method for cell type-specific gene expression and chromatin profiling in Arabidopsis thaliana. Nat Protoc 6:56–68. doi: 10.1038/nprot.2010.175 PubMedCrossRefGoogle Scholar
  71. 71.
    Deal RB, Henikoff S (2010) A simple method for gene expression and chromatin profiling of individual cell types within a tissue. Dev Cell 18(6):1030. doi: 10.1016/j.devcel.2010.05.013 PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Morao K, 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
  73. 73.
    Erhard KF, Talbot J-ERB, Deans NC, McClish AE, Hollick JB (2015) Nascent transcription affected by RNA polymerase IV in Zea mays. Genetics 199:1107–1125. doi: 10.1534/genetics.115.174714 PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Hetzel J, Duttke SH, Benner C, Chory J (2016) Nascent RNA sequencing reveals distinct features in plant transcription. Proc Natl Acad Sci 113:12316–12321. doi: 10.1073/pnas.1603217113 PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Bourbousse C, Mestiri I, Zabulon G, Bourge M, Formiggini F, Koinig M, Spencer CB, Fransz P, Bowler C, Barneche F (2015) Heterochromatin reorganization during photomorphogenic reprogramming of plant development. Proc Natl Acad Sci U S A 112:E2836–E2844. doi: 10.1073/pnas.1503512112 PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Huang H, Lin S, Garcia BA, Zhao Y (2015) Quantitative proteomic analysis of histone modifications. Chem Rev 115:2376–2418. doi: 10.1021/cr500491u PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Sidoli S, Cheng L, Jensen ON (2012) Proteomics in chromatin biology and epigenetics: elucidation of post-translational modifications of histone proteins by mass spectrometry. J Proteomics 75(6):3419–3433. doi: 10.1016/j.jprot.2011.12.029 PubMedCrossRefGoogle Scholar
  78. 78.
    Zheng Y, Huang X, Kelleher NL (2016) Epiproteomics: quantitative analysis of histone marks and codes by mass spectrometry. Curr Opin Chem Biol 33:142–150. doi: 10.1016/j.cbpa.2016.06.007 PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    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
  80. 80.
    Kotliński M, Jerzmanowski A (2017) Histone H1 purification and PTM profiling by high-sensitive MS approaches (Orbitrap). In: Bemer M, Baroux C (eds) Plant chromatin dynamics: methods and protocols. Springer, New York, NY. doi: 10.1007/978-1-4939-7318-7_10 Google Scholar
  81. 81.
    Bergmuller E, Gehrig PM, Gruissem W (2007) Characterization of post-translational modifications of histone H2B-variants isolated from Arabidopsis thaliana. J Proteome Res 6:3655–3668PubMedCrossRefGoogle Scholar
  82. 82.
    Zhang K, Sridhar VV, Zhu J, Kapoor A, Zhu J-K (2007) Distinctive core histone post-translational modification patterns in arabidopsis thaliana. PLoS One 2:e1210PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Shanower GA, Muller M, Blanton JL, Honti V, Gyurkovics H, Schedl P (2005) Characterization of the grappa gene, the Drosophila histone H3 lysine 79 methyltransferase. Genetics 169:173–184. doi: 10.1534/genetics.104.033191 PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Feng Q, Wang H, Ng HH, Erdjument-Bromage H, Tempst P, Struhl K, Zhang Y (2002) Methylation of H3-lysine 79 is mediated by a new family of HMTases without a SET domain. Curr Biol 12:1052–1058. doi: 10.1016/S0960-9822(02)00901-6 PubMedCrossRefGoogle Scholar
  85. 85.
    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:e0147908. doi: 10.1371/journal.pone.0147908 PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Zemach A, Kim MY, Hsieh PH, Coleman-Derr D, Eshed-Williams L, Thao K, Harmer SL, Zilberman D (2013) The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153:193–205. doi: 10.1016/j.cell.2013.02.033 PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Rutowicz K, Puzio M, Halibart-Puzio J, Lirski M, Kroten MA, Kotlinski M, Knizewski L, Lange B, Muszewska A, Sniegowska-Swierk K, Koscielniak J, Iwanicka-Nowicka R, Zmuda K, Buza K, Janowiak F, Joesaar I, Laskowska-Kaszub K, Fogtman A, Zielenkiewicz P, Tiuryn J, Kollist H, Siedlecki P, Ginalski K, Swiezewski S, 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. doi: 10.1104/pp.15.00493 PubMedPubMedCentralGoogle Scholar
  88. 88.
    Jacob Y, Bergamin E, Donoghue MT, Mongeon V, LeBlanc C, Voigt P, Underwood CJ, Brunzelle JS, Michaels SD, Reinberg D, Couture JF, Martienssen RA (2014) Selective methylation of histone H3 variant H3.1 regulates heterochromatin replication. Science 343:1249–1253. doi: 10.1126/science.1248357 PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Johnson L, Mollah S, Garcia BA, Muratore TL, Shabanowitz J, Hunt DF, Jacobsen SE (2004) Mass spectrometry analysis of Arabidopsis histone H3 reveals distinct combinations of post-translational modifications. Nucleic Acids Res 32:6511–6518. doi: 10.1093/nar/gkh992 PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Luo C, Sidote DJ, Zhang Y, Kerstetter RA, Michael TP, Lam E (2013) Integrative analysis of chromatin states in Arabidopsis identified potential regulatory mechanisms for natural antisense transcript production. Plant J 73:77–90. doi: 10.1111/tpj.12017 PubMedCrossRefGoogle Scholar
  91. 91.
    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
  92. 92.
    Pasini D, Malatesta M, Jung HR, Walfridsson J, Willer A, Olsson L, Skotte J, Wutz A, Porse B, Jensen ON, Helin K (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: 10.1093/nar/gkq244 PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Gendrel A-V, Lippman Z, Martienssen R, Colot V (2005) Profiling histone modification patterns in plants using genomic tiling microarrays. Nat Methods 2:213–218. doi: 10.1038/nmeth0305-213 PubMedCrossRefGoogle Scholar
  94. 94.
    Desvoyes B, Vergara Z, Sequeira-Mendes JO, Madeira S, Gutierrez C (2017) A rapid and efficient ChIP protocol to profile chromatin binding proteins and epigenetic modifications in bulk Arabidopsis tissue. 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
  95. 95.
    Landt SG, Marinov GK, Kundaje A, Kheradpour P, Pauli F, Batzoglou S, Bernstein BE, Bickel P, Brown JB, Cayting P, Chen Y, DeSalvo G, Epstein C, Fisher-Aylor KI, Euskirchen G, Gerstein M, Gertz J, Hartemink AJ, Hoffman MM, Iyer VR, Jung YL, Karmakar S, Kellis M, Kharchenko PV, Li Q, Liu T, Liu XS, Ma L, Milosavljevic A, Myers RM, Park PJ, Pazin MJ, Perry MD, Raha D, Reddy TE, Rozowsky J, Shoresh N, Sidow A, Slattery M, Stamatoyannopoulos JA, Tolstorukov MY, White KP, Xi S, Farnham PJ, Lieb JD, Wold BJ, Snyder M (2012) ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia. Genome Res 22:1813–1831. doi: 10.1101/gr.136184.111 PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Egelhofer TA, Minoda A, Klugman S, Lee K, Kolasinska-Zwierz P, Alekseyenko AA, Cheung M-S, Day DS, Gadel S, Gorchakov AA, Gu T, Kharchenko PV, Kuan S, Latorre I, Linder-Basso D, Luu Y, Ngo Q, Perry M, Rechtsteiner A, Riddle NC, Schwartz YB, Shanower GA, Vielle A, Ahringer J, Elgin SCR, Kuroda MI, Pirrotta V, Ren B, Strome S, Park PJ, Karpen GH, Hawkins RD, Lieb JD (2011) An assessment of histone-modification antibody quality. Nat Struct Mol Biol 18:91–93. doi: 10.1038/nsmb.1972 PubMedCrossRefGoogle Scholar
  97. 97.
    Bernatavichute YV, Zhang X, Cokus S, Pellegrini M, Jacobsen SE (2008) Genome-wide association of histone H3 lysine nine methylation with CHG DNA methylation in Arabidopsis thaliana. PLoS One 3:e3156. doi: 10.1371/journal.pone.0003156 PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Bonhoure N, Bounova G, Bernasconi D, Praz V, Lammers F, Canella D, Willis IM, Herr W, Hernandez N, Delorenzi M, The CycliX Consortium (2014) Quantifying ChIP-seq data: a spiking method providing an internal reference for sample-to-sample normalization. Genome Res 24:1157–1168. doi: 10.1101/gr.168260.113 CrossRefGoogle Scholar
  99. 99.
    Orlando DA, Chen MW, Brown VE, Solanki S, Choi YJ, Olson ER, Fritz CC, Bradner JE, Guenther MG (2014) Quantitative ChIP-Seq normalization reveals global modulation of the epigenome. Cell Rep 9:1163–1170. doi: 10.1016/j.celrep.2014.10.018 PubMedCrossRefGoogle Scholar
  100. 100.
    Egan B, Yuan C-C, Craske ML, Labhart P, Guler GD, Arnott D, Maile TM, Busby J, Henry C, Kelly TK, Tindell CA, Jhunjhunwala S, Zhao F, Hatton C, Bryant BM, Classon M, Trojer P (2016) An alternative approach to ChIP-Seq normalization enables detection of genome-wide changes in histone H3 lysine 27 trimethylation upon EZH2 inhibition. PLoS One 11:e0166438. doi: 10.1371/journal.pone.0166438 PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Grzybowski AT, Chen Z, Ruthenburg AJ (2015) Calibrating ChIP-Seq with nucleosomal internal standards to measure histone modification density genome wide. Mol Cell 58:886–899. doi: 10.1016/j.molcel.2015.04.022 PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Stroud H, Otero S, Desvoyes B, Ramírez-Parra E, Jacobsen SE, Gutierrez C (2012) Genome-wide analysis of histone H3.1 and H3.3 variants in Arabidopsis thaliana. Proc Natl Acad Sci 109:5370–5375. doi: 10.1073/pnas.1203145109 PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Wollmann H, Holec S, Alden K, Clarke ND, Jacques P-É, Berger F (2012) Dynamic deposition of histone variant H3.3 accompanies developmental remodeling of the arabidopsis transcriptome. PLoS Genet 8:e1002658. doi: 10.1371/journal.pgen.1002658 PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Pajoro A, Muiňo J, Angenent G, 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
  105. 105.
    Gent JI, Madzima TF, Bader R, Kent MR, Zhang X, Stam M, McGinnis KM, Dawe RK (2014) Accessible DNA and relative depletion of H3K9me2 at maize loci undergoing RNA-directed DNA methylation. Plant Cell 26(12):4903. doi: 10.1105/tpc.114.130427 PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Chodavarapu R, Feng S, Bernatavichute Y, Chen P, Stroud H, Yu Y, Hetzel J, Kuo F, Kim J, Cokus S, Casero D, Bernal M, Huijser P, Clark A, Kramer U, Merchant S, Zhang X, Jacobsen S, Pellegrini M (2010) Relationship between nucleosome positioning and DNA methylation. Nature 466:388–392PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Li G, Liu S, Wang J, He J, Huang H, Zhang Y, Xu L (2014) ISWI proteins participate in the genome-wide nucleosome distribution in Arabidopsis. Plant J 78:706–714. doi: 10.1111/tpj.12499 PubMedCrossRefGoogle Scholar
  108. 108.
    Wu Y, Zhang W, Jiang J (2014) Genome-wide nucleosome positioning is orchestrated by genomic regions associated with DNase I hypersensitivity in rice. PLoS Genet 10:e1004378. doi: 10.1371/journal.pgen.1004378 PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Fincher JA, Vera DL, Hughes DD, McGinnis KM, Dennis JH, Bass HW (2013) Genome-wide prediction of nucleosome occupancy in maize reveals plant chromatin structural features at genes and other elements at multiple scales. Plant Physiol 162:1127–1141. doi: 10.1104/pp.113.216432 PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Vera DL, Madzima TF, Labonne JD, Alam MP, Hoffman GG, Girimurugan SB, Zhang J, McGinnis KM, Dennis JH, Bass HW (2014) Differential nuclease sensitivity profiling of chromatin reveals biochemical footprints coupled to gene expression and functional DNA elements in maize. Plant Cell 26:3883–3893. doi: 10.1105/tpc.114.130609 PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Pecinka A, Dinh HQ, Baubec T, Rosa M, Lettner N, Mittelsten Scheid O (2010) Epigenetic regulation of repetitive elements is attenuated by prolonged heat stress in Arabidopsis. Plant Cell 22:3118–3129. doi: 10.1105/tpc.110.078493 PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    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 27:1889–1906. doi: 10.1105/tpc.15.00233 PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Jegu T, Latrasse D, Delarue M, Hirt H, Domenichini S, Ariel F (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. doi: 10.1105/tpc.113.114454 PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Simon JM, Giresi PG, Davis IJ, Lieb JD (2012) Using formaldehyde-assisted isolation of regulatory elements (FAIRE) to isolate active regulatory DNA. Nat Protoc 7:256–267. doi: 10.1038/nprot.2011.444 PubMedPubMedCentralCrossRefGoogle Scholar
  115. 115.
    Gangadharan S, Mularoni L, Fain-Thornton J, Wheelan SJ, Craig NL (2010) DNA transposon Hermes inserts into DNA in nucleosome-free regions in vivo. Proc Natl Acad Sci 107:21966–21972. doi: 10.1073/pnas.1016382107 PubMedPubMedCentralCrossRefGoogle Scholar
  116. 116.
    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
  117. 117.
    Buenrostro JD, Giresi PG, Zaba LC, Chang HY, Greenleaf WJ (2013) Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat Methods 10:1213–1218. doi: 10.1038/nmeth.2688 PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Buenrostro JD, Wu B, Litzenburger UM, Ruff D, Gonzales ML, Snyder MP, Chang HY, Greenleaf WJ (2015) Single-cell chromatin accessibility reveals principles of regulatory variation. Nature 523:486–490. doi: 10.1038/nature14590 PubMedPubMedCentralCrossRefGoogle Scholar
  119. 119.
    Lu Z, Hofmeister BT, Vollmers C, RM DB, Schmitz RJ (2017) Combining ATAC-seq with nuclei sorting for discovery of cis-regulatory regions in plant genomes. Nucleic Acids Res 45(6):e41. doi: 10.1093/nar/gkw1179. gkw1179PubMedCrossRefGoogle Scholar
  120. 120.
    Piper J, Elze MC, Cauchy P, Cockerill PN, Bonifer C, Ott S (2013) Wellington: a novel method for the accurate identification of digital genomic footprints from DNase-seq data. Nucleic Acids Res 41:e201–e201. doi: 10.1093/nar/gkt850 PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Frommer M, McDonald LE, Millar DS, Collis CM, Watt F, Grigg GW, Molloy PL, Paul CL (1992) A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc Natl Acad Sci 89:1827–1831. doi: 10.1073/pnas.89.5.1827 PubMedPubMedCentralCrossRefGoogle Scholar
  122. 122.
    Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, Pradhan S, Nelson SF, Pellegrini M, Jacobsen SE (2008) Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452:215–219. doi: 10.1038/nature06745 PubMedPubMedCentralCrossRefGoogle Scholar
  123. 123.
    Lister R, O’Malley RC, Tonti-Filippini J, Gregory BD, Berry CC, Millar AH, Ecker JR (2008) Highly integrated single-base resolution maps of the epigenome in arabidopsis. Cell 133:523–536PubMedPubMedCentralCrossRefGoogle Scholar
  124. 124.
    Stroud H, Greenberg MV, Feng S, Bernatavichute YV, Jacobsen SE (2013) Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152:352–364PubMedPubMedCentralCrossRefGoogle Scholar
  125. 125.
    Heard E, Martienssen RA (2014) Transgenerational epigenetic inheritance: myths and mechanisms. Cell 157(3):95–109. doi: 10.1016/j.cell.2014.02.045 PubMedPubMedCentralCrossRefGoogle Scholar
  126. 126.
    Becker C, Weigel D (2012) Epigenetic variation: origin and transgenerational inheritance. Curr Opin Plant Biol 15(5):562. doi: 10.1016/j.pbi.2012.08.004 PubMedCrossRefGoogle Scholar
  127. 127.
    Slotkin RK, Vaughn M, Borges F, Tanurdzic M, Becker JD, Feijó JA, Martienssen RA (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:461–472. doi: 10.1016/j.cell.2008.12.038 PubMedPubMedCentralCrossRefGoogle Scholar
  128. 128.
    Calarco JP, Borges F, Donoghue MT, Van Ex F, Jullien PE, Lopes T, Gardner R, Berger F, Feijo JA, Becker JD, Martienssen RA (2012) Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151:194–205. doi: 10.1016/j.cell.2012.09.001 PubMedPubMedCentralCrossRefGoogle Scholar
  129. 129.
    Ibarra CA, Feng X, Schoft VK, Hsieh TF, Uzawa R, Rodrigues JA, Zemach A, Chumak N, Machlicova A, Nishimura T, Rojas D, Fischer RL, Tamaru H, Zilberman D (2012) Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science 337:1360–1364. doi: 10.1126/science.1224839 PubMedPubMedCentralCrossRefGoogle Scholar
  130. 130.
    Martínez G, Panda K, Köhler C, Slotkin RK (2016) Silencing in sperm cells is directed by RNA movement from the surrounding nurse cell. Nat Plants 2:16030. doi: 10.1038/nplants.2016.30 PubMedCrossRefGoogle Scholar
  131. 131.
    Schmitz RJ, Schultz MD, Urich MA, Nery JR, Pelizzola M, Libiger O, Alix A, McCosh RB, Chen H, Schork NJ, Ecker JR (2013) Patterns of population epigenomic diversity. Nature 495:193–198. doi: 10.1038/nature11968 PubMedPubMedCentralCrossRefGoogle Scholar
  132. 132.
    Dubin MJ, Zhang P, Meng D, Remigereau M-S, Osborne EJ, Paolo Casale F, Drewe P, Kahles A, Jean G, Vilhjálmsson B, Jagoda J, Irez S, Voronin V, Song Q, Long Q, Rätsch G, Stegle O, Clark RM, Nordborg M (2015) DNA methylation in Arabidopsis has a genetic basis and shows evidence of local adaptation. Elife 4:e05255. doi: 10.7554/eLife.05255 PubMedPubMedCentralCrossRefGoogle Scholar
  133. 133.
    Willing E-M, Rawat V, Mandáková T, Maumus F, James GV, Nordström KJV, Becker C, Warthmann N, Chica C, Szarzynska B, Zytnicki M, Albani MC, Kiefer C, Bergonzi S, Castaings L, Mateos JL, Berns MC, Bujdoso N, Piofczyk T, de Lorenzo L, Barrero-Sicilia C, Mateos I, Piednoël M, Hagmann J, Chen-Min-Tao R, Iglesias-Fernández R, Schuster SC, Alonso-Blanco C, Roudier F, Carbonero P, Paz-Ares J, Davis SJ, Pecinka A, Quesneville H, Colot V, Lysak MA, Weigel D, Coupland G, Schneeberger K (2015) Genome expansion of Arabis alpina linked with retrotransposition and reduced symmetric DNA methylation. Nat Plants 1:14023. doi: 10.1038/nplants.2014.23 PubMedCrossRefGoogle Scholar
  134. 134.
    Quadrana L, Bortolini Silveira A, Mayhew GF, LeBlanc C, Martienssen RA, Jeddeloh JA, Colot V (2016) The Arabidopsis thaliana mobilome and its impact at the species level. Elife 5:e15716. doi: 10.7554/eLife.15716 PubMedPubMedCentralCrossRefGoogle Scholar
  135. 135.
    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
  136. 136.
    Suzuki MM, Bird A (2008) DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 9:465–476. doi: 10.1038/nrg2341 PubMedCrossRefGoogle Scholar
  137. 137.
    Becker C, Hagmann J, Muller J, Koenig D, Stegle O, Borgwardt K, Weigel D (2011) Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 480:245–249. doi: 10.1038/nature10555 PubMedCrossRefGoogle Scholar
  138. 138.
    Schmitz RJ, Schultz MD, Lewsey MG, O’Malley RC, Urich MA, Libiger O, Schork NJ, Ecker JR (2011) Transgenerational epigenetic instability is a source of novel methylation variants. Science 334(6054):369. doi: 10.1126/science.1212959 PubMedPubMedCentralCrossRefGoogle Scholar
  139. 139.
    Kishore K, Pelizzola M (2017) Identification of differentially methylated regions in the Arabidopsis thaliana genome. 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
  140. 140.
    Lieberman-Aiden E, Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A (2009) Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326(5950):289. doi: 10.1126/science.1181369 PubMedPubMedCentralCrossRefGoogle Scholar
  141. 141.
    Baccarini J (1908) Sulle cinesi vegitative de Cynomorium coccineum L. Nuovo Giorn Botan Ital 15:189–203Google Scholar
  142. 142.
    Heitz E (1928) Das Heterochromatin der Moose. Jahrb Wiss Bot 69:762–818Google Scholar
  143. 143.
    Fransz P, De Jong JH, Lysak M, Castiglione MR, Schubert I (2002) Interphase chromosomes in Arabidopsis are organized as well defined chromocenters from which euchromatin loops emanate. Proc Natl Acad Sci U S A 99:14584–14589PubMedPubMedCentralCrossRefGoogle Scholar
  144. 144.
    Pecinka A, Schubert V, Meister A, Kreth G, Klatte M, Lysak M, Fuchs J, Schubert I (2004) Chromosome territory arrangement and homologous pairing in nuclei of Arabidopsis thaliana are predominantly random except for NOR-bearing chromosomes. Chromosoma 113:258–269PubMedCrossRefGoogle Scholar
  145. 145.
    Chandrasekhara C, Mohannath G, Blevins T, Pontvianne F, Pikaard CS (2016) Chromosome-specific NOR inactivation explains selective rRNA gene silencing and dosage control in Arabidopsis. Genes Dev 30(2):177. doi: 10.1101/gad.273755.115 PubMedPubMedCentralGoogle Scholar
  146. 146.
    Grob S, Schmid MW, Luedtke NW, Wicker T, Grossniklaus U (2013) Characterization of chromosomal architecture in Arabidopsis by chromosome conformation capture. Genome Biol 14:R129PubMedPubMedCentralCrossRefGoogle Scholar
  147. 147.
    Guenatri M, Bailly D, Maison C, Almouzni G (2004) Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J Cell Biol 166:493–505PubMedPubMedCentralCrossRefGoogle Scholar
  148. 148.
    Mitchell JA, Fraser P (2008) Transcription factories are nuclear subcompartments that remain in the absence of transcription. Genes Dev 22:20–25PubMedPubMedCentralCrossRefGoogle Scholar
  149. 149.
    Tessadori F, van Zanten M, Pavlova P, Clifton R, Pontvianne F, Snoek LB, Millenaar FF, Schulkes RK, van Driel R, Voesenek LA (2009) Phytochrome B and histone deacetylase 6 control light-induced chromatin compaction in Arabidopsis thaliana. PLoS Genet 5:e1000638PubMedPubMedCentralCrossRefGoogle Scholar
  150. 150.
    Del Prete S, Arpon J, Sakai K, Andrey P, Gaudin V (2014) Nuclear architecture and chromatin dynamics in interphase nuclei of Arabidopsis thaliana. Cytogenet Genome Res 143:28–50. doi: 10.1159/000363724 PubMedCrossRefGoogle Scholar
  151. 151.
    Probst AV, Mittelsten Scheid O (2015) Stress-induced structural changes in plant chromatin. Curr Opin Plant Biol 27:8–16. doi: 10.1016/j.pbi.2015.05.011 PubMedCrossRefGoogle Scholar
  152. 152.
    van Zanten M, Tessadori F, McLoughlin F, Smith R, Millenaar FF, van Driel R, Voesenek LACJ, Peeters A, Fransz PF (2010) Photoreceptors CRYTOCHROME 2 and Phytochrome B control chromatin compaction in Arabidopsis thaliana. Plant Physiol 154(4):1686PubMedPubMedCentralCrossRefGoogle Scholar
  153. 153.
    Grob S, Cavalli G (2017) Technical review: 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
  154. 154.
    Schubert V (2014) RNA polymerase II forms transcription networks in rye and Arabidopsis nuclei and its amount increases with endopolyploidy. Cytogenet Genome Res 143:69–77. doi: 10.1159/000365233 PubMedCrossRefGoogle Scholar
  155. 155.
    Roudier F, Teixeira FK, Colot V (2009) Chromatin indexing in Arabidopsis: an epigenomic tale of tails and more. Trends Genet 25:511–517. doi: 10.1016/j.tig.2009.09.013 PubMedCrossRefGoogle Scholar
  156. 156.
    Rosa S, De Lucia F, Mylne JS, Zhu D, Ohmido N, Pendle A, Kato N, Shaw P, Dean C (2013) Physical clustering of FLC alleles during Polycomb-mediated epigenetic silencing in vernalization. Genes Dev 27:1845–1850. doi: 10.1101/gad.221713.113 PubMedPubMedCentralCrossRefGoogle Scholar
  157. 157.
    Crevillen 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. doi: 10.1038/emboj.2012.324 PubMedCrossRefGoogle Scholar
  158. 158.
    Feng CM, Qiu Y, Van Buskirk EK, Yang EJ, Chen M (2014) Light-regulated gene repositioning in Arabidopsis. Nat Commun 5:3027. doi: 10.1038/ncomms4027 PubMedPubMedCentralGoogle Scholar
  159. 159.
    Smith S, Galinha C, Desset S, Tolmie F, Evans D, Tatout C, Graumann K (2015) Marker gene tethering by nucleoporins affects gene expression in plants. Nucleus 6:471–478. doi: 10.1080/19491034.2015.1126028 PubMedPubMedCentralCrossRefGoogle Scholar
  160. 160.
    Amendola M, van Steensel B (2014) Mechanisms and dynamics of nuclear lamina–genome interactions. Curr Opin Cell Biol 28(6):61–68. doi: 10.1016/ PubMedCrossRefGoogle Scholar
  161. 161.
    Poulet A, Probst AV, Graumann K, Tatout C, Evans D (2017) Exploring the evolution of the proteins of the plant nuclear envelope. Nucleus 28:1–46. doi: 10.1080/19491034.2016.1236166 Google Scholar
  162. 162.
    Andersen JS, Lam YW, Leung AKL, Ong S-E, Lyon CE, Lamond AI, Mann M (2005) Nucleolar proteome dynamics. Nature 433:77–83. doi: 10.1038/nature03207 PubMedCrossRefGoogle Scholar
  163. 163.
    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
  164. 164.
    Ding Y, Fromm M, Avramova Z (2012) Multiple exposures to drought “train” transcriptional responses in Arabidopsis. Nat Commun 3:740. doi: 10.1038/ncomms1732 PubMedCrossRefGoogle Scholar
  165. 165.
    Sani E, Herzyk P, Perrella G, Colot V, Amtmann A (2013) Hyperosmotic priming of Arabidopsis seedlings establishes a long-term somatic memory accompanied by specific changes of the epigenome. Genome Biol 14:R59. doi: 10.1186/gb-2013-14-6-r59 PubMedPubMedCentralCrossRefGoogle Scholar
  166. 166.
    Sequeira-Mendes J, Gutierrez C (2016) Genome architecture: from linear organisation of chromatin to the 3D assembly in the nucleus. Chromosoma 125:455–469. doi: 10.1007/s00412-015-0538-5 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media LLC 2018

Authors and Affiliations

  • Clara Bourbousse
    • 1
  • Moussa Benhamed
    • 2
  • Fredy Barneche
    • 1
    Email author
  1. 1.Département de Biologie, IBENS, Ecole Normale Supérieure, CNRS, INSERMPSL Research UniversityParisFrance
  2. 2.Institute of Plant Sciences Paris-Saclay (IPS2), UMR 9213/UMR1403, CNRS, INRA, Université Paris-Sud, Université d’Evry, Université Paris-DiderotSorbonne Paris-CitéOrsayFrance

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