Understanding how the packaging of chromatin in the nucleus is regulated and organized to guide complex cellular and developmental programmes, as well as responses to environmental cues is a major question in biology. Technological advances have allowed remarkable progress within this field over the last years. However, we still know very little about how the 3D genome organization within the cell nucleus contributes to the regulation of gene expression. The nuclear space is compartmentalized in several domains such as the nucleolus, chromocentres, telomeres, protein bodies, and the nuclear periphery without the presence of a membrane around these domains. The role of these domains and their possible impact on nuclear activities is currently under intense investigation. In this review, we discuss new data from research in plants that clarify functional links between the organization of different nuclear domains and plant genome function with an emphasis on the potential of this organization for gene regulation.

Agricultural Genetic Engineering Department Niğde Ömer Halisdemir University Niğde Turkey

Biology Centre of the Czech Academy of Sciences České Budějovice Czech Republic

CEITEC Masaryk University Brno Czech Republic

Center for Plant Molecular Biology University of Tübingen Tübingen Germany

CNRS Laboratoire Génome et Développement des Plantes Université de Perpignan Via Domitia Perpignan France

Faculty of Science University of South Bohemia České Budějovice Czech Republic

Institut Jean Pierre Bourgin INRAE AgroParisTech Université Paris Saclay Versailles France

Institute for Biology Freie Universität Berlin Berlin Germany

Institute of Biology University of Hohenheim Stuttgart Germany

Instituto de Tecnologia Química e Biológica António Xavier Universidade Nova de Lisboa Oeiras Portugal

Plant and AgriBiosciences Centre Ryan Institute NUI Galway Galway Ireland

Swedish University of Agricultural Sciences Uppsala Sweden

University of Amsterdam Amsterdam The Netherlands

Erratum v

J Exp Bot. 2021 Jul 28;72(15):5782. doi: 10.1093/jxb/erab134. PubMed

Zobrazit více v PubMed

Adamusova K, Khosravi S, Fujimoto S, Matsunaga S, Fajkus J, Fojtová M. 2020. Two combinatorial patterns of telomere histone marks in plants with canonical and non-canonical telomere repeats. The Plant Journal 102, 678–687. PubMed

Adriaens C, Serebryannyy LA, Feric M, et al. . 2018. Blank spots on the map: some current questions on nuclear organization and genome architecture. Histochemistry and Cell Biology 150, 579–592. PubMed PMC

Albert PS, Zhang T, Semrau K, Rouillard JM, Kao YH, Wang CR, Danilova TV, Jiang J, Birchler JA. 2019. Whole-chromosome paints in maize reveal rearrangements, nuclear domains, and chromosomal relationships. Proceedings of the National Academy of Sciences, USA 116, 1679–1685. PubMed PMC

Alberti S. 2017. Phase separation in biology. Current Biology 27, R1097–R1102. PubMed

Andrey G, Montavon T, Mascrez B, Gonzalez F, Noordermeer D, Leleu M, Trono D, Spitz F, Duboule D. 2013. A switch between topological domains underlies HoxD genes collinearity in mouse limbs. Science 340, 1234167. PubMed

Anton T, Bultmann S, Leonhardt H, Markaki Y. 2014. Visualization of specific DNA sequences in living mouse embryonic stem cells with a programmable fluorescent CRISPR/Cas system. Nucleus 5, 163–172. PubMed PMC

Aparicio OM, Billington BL, Gottschling DE. 1991. Modifiers of position effect are shared between telomeric and silent mating-type loci in S. cerevisiae. Cell 66, 1279–1287. PubMed

Aragon-Alcaide L, Reader S, Beven A, Shaw P, Miller T, Moore G. 1997. Association of homologous chromosomes during floral development. Current Biology 7, 905–908. PubMed

Audas TE, Jacob MD, Lee S. 2012. Immobilization of proteins in the nucleolus by ribosomal intergenic spacer noncoding RNA. Molecular Cell 45, 147–157. PubMed

Audas TE, Lee S. 2016. Stressing out over long noncoding RNA. Biochimica et Biophysica Acta 1859, 184–191. PubMed PMC

Azzalin CM, Reichenbach P, Khoriauli L, Giulotto E, Lingner J. 2007. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 318, 798–801. PubMed

Baroux C, Pecinka A, Fuchs J, Kreth G, Schubert I, Grossniklaus U. 2017. Non-random chromosome arrangement in triploid endosperm nuclei. Chromosoma 126, 115–124. PubMed

Bass HW, Riera-Lizarazu O, Ananiev EV, Bordoli SJ, Rines HW, Phillips RL, Sedat JW, Agard DA, Cande WZ. 2000. Evidence for the coincident initiation of homolog pairing and synapsis during the telomere-clustering (bouquet) stage of meiotic prophase. Journal of Cell Science 113, 1033–1042. PubMed

Bassett CL. 2012. Cajal bodies and plant RNA metabolism. Critical Reviews in Plant Sciences 31, 258–270.

Baudement MO, Cournac A, Court F, et al. . 2018. High-salt-recovered sequences are associated with the active chromosomal compartment and with large ribonucleoprotein complexes including nuclear bodies. Genome Research 28, 1733–1746. PubMed PMC

Bauer D, Viczián A, Kircher S, et al. . 2004. Constitutive photomorphogenesis 1 and multiple photoreceptors control degradation of phytochrome interacting factor 3, a transcription factor required for light signaling in Arabidopsis. The Plant Cell 16, 1433–1445. PubMed PMC

Benoit M, Simon L, Desset S, Duc C, Cotterell S, Poulet A, Le Goff S, Tatout C, Probst AV. 2019. Replication-coupled histone H3.1 deposition determines nucleosome composition and heterochromatin dynamics during Arabidopsis seedling development. New Phytologist 221, 385–398. PubMed

Bi X, Cheng YJ, Hu B, Ma X, Wu R, Wang JW, Liu C. 2017. Nonrandom domain organization of the Arabidopsis genome at the nuclear periphery. Genome Research 27, 1162–1173. PubMed PMC

Bintu B, Mateo LJ, Su JH, Sinnott-Armstrong NA, Parker M, Kinrot S, Yamaya K, Boettiger AN, Zhuang X. 2018. Super-resolution chromatin tracing reveals domains and cooperative interactions in single cells. Science 362, eaau1783. PubMed PMC

Boeynaems S, Holehouse AS, Weinhardt V, et al. . 2019. Spontaneous driving forces give rise to protein–RNA condensates with coexisting phases and complex material properties. Proceedings of the National Academy of Sciences, USA 116, 7889–7898. PubMed PMC

Boisvert FM, van Koningsbruggen S, Navascués J, Lamond AI. 2007. The multifunctional nucleolus. Nature Reviews. Molecular Cell Biology 8, 574–585. PubMed

Boudonck K, Dolan L, Shaw PJ. 1998. Coiled body numbers in the Arabidopsis root epidermis are regulated by cell type, developmental stage and cell cycle parameters. Journal of Cell Science 111, 3687–3694. PubMed

Boudonck K, Dolan L, Shaw PJ. 1999. The movement of coiled bodies visualized in living plant cells by the green fluorescent protein. Molecular Biology of the Cell 10, 2297–2307. PubMed PMC

Boulon S, Westman BJ, Hutten S, Boisvert FM, Lamond AI. 2010. The nucleolus under stress. Molecular Cell 40, 216–227. PubMed PMC

Brangwynne CP, Eckmann CR, Courson DS, Rybarska A, Hoege C, Gharakhani J, Jülicher F, Hyman AA. 2009. Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science 324, 1729–1732. PubMed

Brown DD, Gurdon JB. 1964. Absence of ribosomal RNA synthesis in the anucleolate mutant of Xenopus. Proceedings of the National Academy of Sciences, USA 51, 139–146. PubMed PMC

Buckley MS, Lis JT. 2014. Imaging RNA polymerase II transcription sites in living cells. Current Opinion in Genetics & Development 25, 126–130. PubMed PMC

Calil IP, Quadros IPS, Araújo TC, et al. . 2018. A WW domain-containing protein forms immune nuclear bodies against Begomoviruses. Molecular Plant 11, 1449–1465. PubMed

Calonje M, Sanchez R, Chen L, Sung ZR. 2008. EMBRYONIC FLOWER1 participates in polycomb group-mediated AG gene silencing in Arabidopsis. The Plant Cell 20, 277–291. PubMed PMC

Carpentier MC, Picart-Picolo A, Pontvianne F. 2018. A method to identify nucleolus-associated chromatin domains (NADs). Methods in Molecular Biology 1675, 99–109. PubMed

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 & Development 30, 177–190. PubMed PMC

Chen M, Chory J. 2011. Phytochrome signaling mechanisms and the control of plant development. Trends in Cell Biology 21, 664–671. PubMed PMC

Cheutin T, Cavalli G. 2014. Polycomb silencing: from linear chromatin domains to 3D chromosome folding. Current Opinion in Genetics & Development 25, 30–37. PubMed

Choi J, Strickler SR, Richards EJ. 2019. Loss of CRWN nuclear proteins induces cell death and salicylic acid defense signaling. Plant Physiology 179, 1315–1329. PubMed PMC

Chu HP, Cifuentes-Rojas C, Kesner B, Aeby E, Lee HG, Wei C, Oh HJ, Boukhali M, Haas W, Lee JT. 2017. TERRA RNA antagonizes ATRX and protects telomeres. Cell 170, 86–101.e16. PubMed PMC

Ciabrelli F, Cavalli G. 2015. Chromatin-driven behavior of topologically associating domains. Journal of Molecular Biology 427, 608–625. PubMed

Colas I, Shaw P, Prieto P, Wanous M, Spielmeyer W, Mago R, Moore G. 2008. Effective chromosome pairing requires chromatin remodeling at the onset of meiosis. Proceedings of the National Academy of Sciences, USA 105, 6075–6080. PubMed PMC

Collier S, Pendle A, Boudonck K, van Rij T, Dolan L, Shaw P. 2006. A distant coilin homologue is required for the formation of cajal bodies in Arabidopsis. Molecular Biology of the Cell 17, 2942–2951. PubMed PMC

Concia L, Veluchamy A, Ramirez-Prado JS, et al. . 2020. Wheat chromatin architecture is organized in genome territories and transcription factories. Genome Biology 21, 104. PubMed PMC

Cremer T, Cremer C. 2001. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nature Reviews. Genetics 2, 292–301. PubMed

Cremer T, Cremer M. 2010. Chromosome territories. Cold Spring Harbor Perspectives in Biology 2, a003889. PubMed PMC

Del Prete S, Arpón J, Sakai K, Andrey P, Gaudin V. 2014. Nuclear architecture and chromatin dynamics in interphase nuclei of Arabidopsis thaliana. Cytogenetic and Genome Research 143, 28–50. PubMed

Del Prete S, Mikulski P, Schubert D, Gaudin V. 2015. One, two, three: polycomb proteins hit all dimensions of gene regulation. Genes 6, 520–542. PubMed PMC

Deng Z, Norseen J, Wiedmer A, Riethman H, Lieberman PM. 2009. TERRA RNA binding to TRF2 facilitates heterochromatin formation and ORC recruitment at telomeres. Molecular Cell 35, 403–413. PubMed PMC

De Storme N, Keçeli BN, Zamariola L, Angenon G, Geelen D. 2016. CENH3–GFP: a visual marker for gametophytic and somatic ploidy determination in Arabidopsis thaliana. BMC Plant Biology 16, 1. PubMed PMC

Digby L. 1919. On the archesporial and meiotic mitoses of Osmunda. Annals of Botany 2, 135–172.

Dittmer TA, Stacey NJ, Sugimoto-Shirasu K, Richards EJ. 2007. LITTLE NUCLEI genes affecting nuclear morphology in Arabidopsis thaliana. The Plant Cell 19, 2793–2803. PubMed PMC

Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, Hu M, Liu JS, Ren B. 2012. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485, 376–380. PubMed PMC

Dixon JR, Xu J, Dileep V, et al. . 2018. Integrative detection and analysis of structural variation in cancer genomes. Nature Genetics 50, 1388–1398. PubMed PMC

Docquier S, Tillemans V, Deltour R, Motte P. 2004. Nuclear bodies and compartmentalization of pre-mRNA splicing factors in higher plants. Chromosoma 112, 255–266. PubMed

Doğan ES, Liu C. 2018. Three-dimensional chromatin packing and positioning of plant genomes. Nature Plants 4, 521–529. PubMed

Dolata J, Taube M, Bajczyk M, Jarmolowski A, Szweykowska-Kulinska Z, Bielewicz D. 2018. Regulation of plant microprocessor function in shaping microRNA landscape. Frontiers in Plant Science 9, 753. PubMed PMC

Dong F, Jiang J. 1998. Non-Rabl patterns of centromere and telomere distribution in the interphase nuclei of plant cells. Chromosome Research 6, 551–558. PubMed

Dong P, Tu X, Chu PY, Lü P, Zhu N, Grierson D, Du B, Li P, Zhong S. 2017. 3D Chromatin architecture of large plant genomes determined by local A/B compartments. Molecular Plant 10, 1497–1509. PubMed

Dong P, Tu X, Li H, Zhang J, Grierson D, Li P, Zhong S. 2020. Tissue-specific Hi-C analyses of rice, foxtail millet and maize suggest non-canonical function of plant chromatin domains. Journal of Integrative Plant Biology 62, 201–217. PubMed

Dreissig S, Schiml S, Schindele P, Weiss O, Rutten T, Schubert V, Gladilin E, Mette MF, Puchta H, Houben A. 2017. Live-cell CRISPR imaging in plants reveals dynamic telomere movements. The Plant Journal 91, 565–573. PubMed PMC

Duncan S, Olsson TSG, Hartley M, Dean C, Rosa S. 2016. A method for detecting single mRNA molecules in Arabidopsis thaliana. Plant Methods 12, 13. PubMed PMC

Dundr M. 2012. Nuclear bodies: multifunctional companions of the genome. Current Opinion in Cell Biology 24, 415–422. PubMed PMC

Dvořáčková M, Fojtová M, Fajkus J. 2015. Chromatin dynamics of plant telomeres and ribosomal genes. The Plant Journal 83, 18–37. PubMed

Dvorácková M, Rossignol P, Shaw PJ, Koroleva OA, Doonan JH, Fajkus J. 2010. AtTRB1, a telomeric DNA-binding protein from Arabidopsis, is concentrated in the nucleolus and shows highly dynamic association with chromatin. The Plant Journal 61, 637–649. PubMed

Exner V, Aichinger E, Shu H, Wildhaber T, Alfarano P, Caflisch A, Gruissem W, Köhler C, Hennig L. 2009. The chromodomain of LIKE HETEROCHROMATIN PROTEIN 1 is essential for H3K27me3 binding and function during Arabidopsis development. PLoS One 4, e5335. PubMed PMC

Fajkus J, Kovarík A, Královics R. 1996. Telomerase activity in plant cells. FEBS Letters 391, 307–309. PubMed

Falk M, Feodorova Y, Naumova N, et al. . 2019. Heterochromatin drives compartmentalization of inverted and conventional nuclei. Nature 570, 395–399. PubMed PMC

Fang X, Wang L, Ishikawa R, et al. . 2019. Arabidopsis FLL2 promotes liquid–liquid phase separation of polyadenylation complexes. Nature 569, 265–269. PubMed PMC

Fang Y, Spector DL. 2007. Identification of nuclear dicing bodies containing proteins for microRNA biogenesis in living Arabidopsis plants. Current Biology 17, 818–823. PubMed PMC

Fei J, Jadaliha M, Harmon TS, et al. . 2017. Quantitative analysis of multilayer organization of proteins and RNA in nuclear speckles at super resolution. Journal of Cell Science 130, 4180–4192. PubMed PMC

Feng CM, Qiu Y, Van Buskirk EK, Yang EJ, Chen M. 2014. Light-regulated gene repositioning in Arabidopsis. Nature Communications 5, 3027. PubMed PMC

Feng S, Jacobsen SE. 2011. Epigenetic modifications in plants: an evolutionary perspective. Current Opinion in Plant Biology 14, 179–186. PubMed PMC

Feric M, Vaidya N, Harmon TS, Mitrea DM, Zhu L, Richardson TM, Kriwacki RW, Pappu RV, Brangwynne CP. 2016. Coexisting liquid phases underlie nucleolar subcompartments. Cell 165, 1686–1697. PubMed PMC

Fitzgerald MS, Shakirov EV, Hood EE, McKnight TD, Shippen DE. 2001. Different modes of de novo telomere formation by plant telomerases. The Plant Journal 26, 77–87. PubMed

Flavahan WA, Drier Y, Liau BB, Gillespie SM, Venteicher AS, Stemmer-Rachamimov AO, Suvà ML, Bernstein BE. 2016. Insulator dysfunction and oncogene activation in IDH mutant gliomas. Nature 529, 110–114. PubMed PMC

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. Proceedings of the National Academy of Sciences, USA 99, 14584–14589. PubMed PMC

Friesner JD, Liu B, Culligan K, Britt AB. 2005. Ionizing radiation-dependent gamma-H2AX focus formation requires ataxia telangiectasia mutated and ataxia telangiectasia mutated and Rad3-related. Molecular Biology of the Cell 16, 2566–2576. PubMed PMC

Fudenberg G, Imakaev M, Lu C, Goloborodko A, Abdennur N, Mirny LA. 2016. Formation of chromosomal domains by loop extrusion. Cell Reports 15, 2038–2049. PubMed PMC

Fujioka Y, Utsumi M, Ohba Y, Watanabe Y. 2007. Location of a possible miRNA processing site in SmD3/SmB nuclear bodies in Arabidopsis. Plant & Cell Physiology 48, 1243–1253. PubMed

Fujimoto S, Sugano SS, Kuwata K, Osakabe K, Matsunaga S. 2016. Visualization of specific repetitive genomic sequences with fluorescent TALEs in Arabidopsis thaliana. Journal of Experimental Botany 67, 6101–6110. PubMed PMC

Galganski L, Urbanek MO, Krzyzosiak WJ. 2017. Nuclear speckles: molecular organization, biological function and role in disease. Nucleic Acids Research 45, 10350–10368. PubMed PMC

Gall JG. 2000. Cajal bodies: the first 100 years. Annual Review of Cell and Developmental Biology 16, 273–300. PubMed

Galvão RM, Li M, Kothadia SM, Haskel JD, Decker PV, Van Buskirk EK, Chen M. 2012. Photoactivated phytochromes interact with HEMERA and promote its accumulation to establish photomorphogenesis in Arabidopsis. Genes & Development 26, 1851–1863. PubMed PMC

Gaudin V, Libault M, Pouteau S, Juul T, Zhao G, Lefebvre D, Grandjean O. 2001. Mutations in LIKE HETEROCHROMATIN PROTEIN 1 affect flowering time and plant architecture in Arabidopsis. Development 128, 4847–4858. PubMed

Gelato KA, Tauber M, Ong MS, et al. . 2014. Accessibility of different histone H3-binding domains of UHRF1 is allosterically regulated by phosphatidylinositol 5-phosphate. Molecular Cell 54, 905–919. PubMed

Gendall AR, Levy YY, Wilson A, Dean C. 2001. The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 107, 525–535. PubMed

Gent JI, Wang N, Dawe RK. 2017. Stable centromere positioning in diverse sequence contexts of complex and satellite centromeres of maize and wild relatives. Genome Biology 18, 121. PubMed PMC

Gerasimova TI, Corces VG. 1998. Polycomb and trithorax group proteins mediate the function of a chromatin insulator. Cell 92, 511–521. PubMed

Ghave-Helm Y, Jankoswki A, Meiers S, Viales RR, Korbel JO, Furlong EEM. 2019. Highly rearranged chromosomes reveal uncoupling between genome topology and gene expression. Nature Genetics 51, 1272–1282. PubMed PMC

Gibson BA, Doolittle LK, Schneider MWG, et al. . 2019. The role of 3D genome organization in development and cell differentiation. Cell 179, 470–484.e21. PubMed

Goto C, Tamura K, Fukao Y, Shimada T, Hara-Nishimura I. 2014. The novel nuclear envelope protein KAKU4 modulates nuclear morphology in Arabidopsis. The Plant Cell 26, 2143–2155. PubMed PMC

Gottschling DE, Aparicio OM, Billington BL, Zakian VA. 1990. Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription. Cell 63, 751–762. PubMed

Greider CW, Blackburn EH. 1985. Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43, 405–413. PubMed

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. Molecular Cell 55, 678–693. PubMed

Groves NR, Biel AM, Newman-Griffis AH, Meier I. 2018. Dynamic changes in plant nuclear organization in response to environmental and developmental signals. Plant Physiology 176, 230–241. PubMed PMC

Grummt I, Pikaard CS. 2003. Epigenetic silencing of RNA polymerase I transcription. Nature Reviews. Molecular Cell Biology 11, 2124–2136. PubMed

Gumber HH, Joseph FM, Estrada AL, Tolmie AF, Graumann K, Bass HW. 2019. Identification and characterization of genes encoding the nuclear envelope LINC complex in the monocot species Zea mays. Journal of Cell Science 132, jcs221390. PubMed

Guo T, Fang Y. 2014. Functional organization and dynamics of the cell nucleus. Frontiers in Plant Science 5, 378. PubMed PMC

Guo T, Mao X, Zhang H, Zhang Y, Fu M, Sun Z, Kuai P, Lou Y, Fang Y. 2017. Lamin-like proteins negatively regulate plant immunity through NAC WITH TRANSMEMBRANE MOTIF1-LIKE9 and NONEXPRESSOR OF PR GENES1 in Arabidopsis thaliana. Molecular Plant 10, 1334–1348. PubMed

Hall LL, Smith KP, Byron M, Lawrence JB. 2006. Molecular anatomy of a speckle. The Anatomical Record. Part A, Discoveries in Molecular, Cellular, and Evolutionary Biology 288, 664–675. PubMed PMC

Harris CJ, Husmann D, Liu W, et al. . 2016. Arabidopsis AtMORC4 and AtMORC7 form nuclear bodies and repress a large number of protein-coding genes. PLoS Genetics 12, e1005998. PubMed PMC

Hayflick L. 1982. Biological aspects of human ageing. British Journal of Hospital Medicine 27, 366, 368, passim. PubMed

Heacock M, Spangler E, Riha K, Puizina J, Shippen DE. 2004. Molecular analysis of telomere fusions in Arabidopsis: multiple pathways for chromosome end-joining. The EMBO Journal 23, 2304–2313. PubMed PMC

Heitz E. 1931. Nukleolen und Chromosomen in der Gattung Vicia. Planta 15, 494–505.

Hirakawa T, Matsunaga S. 2019. Characterization of DNA repair foci in root cells of arabidopsis in response to DNA damage. Frontiers in Plant Science 10, 990. PubMed PMC

Hnisz D, Weintraub AS, Day DS, et al. . 2016. Activation of proto-oncogenes by disruption of chromosome neighborhoods. Science 351, 1454–1458. PubMed PMC

Hohenstatt ML, Mikulski P, Komarynets O, Klose C, Kycia I, Jeltsch A, Farrona S, Schubert D. 2018. PWWP-DOMAIN INTERACTOR OF POLYCOMBS1 interacts with polycomb-group proteins and histones and regulates Arabidopsis flowering and development. The Plant Cell 30, 117–133. PubMed PMC

Holec S, Berger F. 2012. Polycomb group complexes mediate developmental transitions in plants. Plant Physiology 158, 35–43. PubMed PMC

Hu B, Wang N, Bi X, Karaaslan ES, Weber AL, Zhu W, Berendzen KW, Liu C. 2019. Plant lamin-like proteins mediate chromatin tethering at the nuclear periphery. Genome Biology 20, 87. PubMed PMC

Huang H, McLoughlin KE, Sorkin ML, Burgie ES, Bindbeutel RK, Vierstra RD, Nusinow DA. 2019. PCH1 regulates light, temperature, and circadian signaling as a structural component of phytochrome B-photobodies in Arabidopsis. Proceedings of the National Academy of Sciences, USA 116, 8603–8608. PubMed PMC

Huang Y, Jiang L, Liu B-Y, Tan C-F, Chen D-H, Shen W-H, Ruan Y. 2019. Evolution and conservation of polycomb repressive complex 1 core components and putative associated factors in the green lineage. BMC Genomics 20, 533. PubMed PMC

Jacob MD, Audas TE, Uniacke J, Trinkle-Mulcahy L, Lee S. 2013. Environmental cues induce a long noncoding RNA-dependent remodeling of the nucleolus. Molecular Biology of the Cell 24, 2943–2953. PubMed PMC

Jagannathan M, Cummings R, Yamashita YM. 2019. The modular mechanism of chromocenter formation in Drosophila. eLife 8, e43938. PubMed PMC

Jagannathan M, Yamashita YM. 2017. Function of junk: pericentromeric satellite DNA in chromosome maintenance. Cold Spring Harbor Symposia on Quantitative Biology 82, 319–327. PubMed

James TC, Elgin SC. 1986. Identification of a nonhistone chromosomal protein associated with heterochromatin in Drosophila melanogaster and its gene. Molecular and Cellular Biology 6, 3862–3872. PubMed PMC

Kaiserli E, Páldi K, O’Donnell L, Batalov O, Pedmale UV, Nusinow DA, Kay SA, Chory J. 2015. Integration of light and photoperiodic signaling in transcriptional nuclear foci. Developmental Cell 35, 311–321. PubMed PMC

Khan A, Garbelli A, Grossi S, et al. . 2014. The Arabidopsis STRESS RESPONSE SUPPRESSOR DEAD-box RNA helicases are nucleolar- and chromocenter-localized proteins that undergo stress-mediated relocalization and are involved in epigenetic gene silencing. The Plant Journal 79, 28–43. PubMed

Kim DH, Sung S. 2014. Polycomb-mediated gene silencing in Arabidopsis thaliana. Molecules and Cells 37, 841–850. PubMed PMC

Kim J, Han KY, Khanna N, Ha T, Belmont AS. 2019. Nuclear speckle fusion via long-range directional motion regulates speckle morphology after transcriptional inhibition. Journal of Cell Science 132, jcs226563. PubMed PMC

Kim W, Ludlow AT, Min J, Robin JD, Stadler G, Mender I, Lai TP, Zhang N, Wright WE, Shay JW. 2016. Regulation of the human telomerase gene TERT by telomere position effect-over long distances (TPE-OLD): implications for aging and cancer. PLoS Biology 14, e2000016. PubMed PMC

Kim W, Shay JW. 2018. Long-range telomere regulation of gene expression: telomere looping and telomere position effect over long distances (TPE-OLD). Differentiation 99, 1–9. PubMed PMC

Klose C, Viczián A, Kircher S, Schäfer E, Nagy F. 2015. Molecular mechanisms for mediating light-dependent nucleo/cytoplasmic partitioning of phytochrome photoreceptors. New Phytologist 206, 965–971. PubMed PMC

Koch A, Kang H-G, Steinbrenner J, Dempsey DA, Klessig DF, Kogel K-H. 2017. MORC proteins: novel players in plant and animal health. Frontiers in Plant Science 8, 1720. PubMed PMC

Köhler C, Springer N. 2017. Plant epigenomics—deciphering the mechanisms of epigenetic inheritance and plasticity in plants. Genome Biology 18, 132. PubMed PMC

Kotake T, Takada S, Nakahigashi K, Ohto M, Goto K. 2003. Arabidopsis TERMINAL FLOWER 2 gene encodes a heterochromatin protein 1 homolog and represses both FLOWERING LOCUS T to regulate flowering time and several floral homeotic genes. Plant & Cell Physiology 44, 555–564. PubMed

Kotova E, Jarnik M, Tulin AV. 2009. Poly (ADP-ribose) polymerase 1 is required for protein localization to Cajal body. PLoS Genetics 5, e1000387. PubMed PMC

Kovařik A, Fajkus J, Koukalová B, Bezděk M. 1996. Species-specific evolution of telomeric and rDNA repeats in the tobacco composite genome. Theoretical and Applied Genetics 92, 1108–1111. PubMed

Kuchar M, Fajkus J. 2004. Interactions of putative telomere-binding proteins in Arabidopsis thaliana: identification of functional TRF2 homolog in plants. FEBS Letters 578, 311–315. PubMed

Kumaran RI, Thakar R, Spector DL. 2008. Chromatin dynamics and gene positioning. Cell 132, 929–934. PubMed PMC

Kundu S, Ji F, Sunwoo H, Jain G, Lee JT, Sadreyev RI, Dekker J, Kingston RE. 2017. Polycomb repressive complex 1 generates discrete compacted domains that change during differentiation. Molecular Cell 65, 432–446.e5. PubMed PMC

Langdon EM, Gladfelter AS. 2018. A new lens for RNA localization: liquid–liquid phase separation. Annual Review of Microbiology 72, 255–271. PubMed

Langen G, von Einem S, Koch A, et al. . 2014. The compromised recognition of Turnip crinkle virus1 subfamily of microrchidia ATPases regulates disease resistance in barley to biotrophic and necrotrophic pathogens. Plant Physiology 164, 866–878. PubMed PMC

Larson AG, Elnatan D, Keenen MM, Trnka MJ, Johnston JB, Burlingame AL, Agard DA, Redding S, Narlikar GJ. 2017. Liquid droplet formation by HP1α suggests a role for phase separation in heterochromatin. Nature 547, 236–240. PubMed PMC

Lawrence RJ, Earley K, Pontes O, Silva M, Chen ZJ, Neves N, Viegas W, Pikaard CS. 2004. A concerted DNA methylation/histone methylation switch regulates rRNA gene dosage control and nucleolar dominance. Molecular Cell 13, 599–609. PubMed

Levy YY, Mesnage S, Mylne JS, Gendall AR, Dean C. 2002. Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control. Science 297, 243–246. PubMed

Lewis AE, Sommer L, Arntzen MØ, Strahm Y, Morrice NA, Divecha N, D’Santos CS. 2011. Identification of nuclear phosphatidylinositol 4,5-bisphosphate-interacting proteins by neomycin extraction. Molecular & Cellular Proteomics 10, M110.003376. PubMed PMC

Lewis PW, Elsaesser SJ, Noh KM, Stadler SC, Allis CD. 2010. Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. Proceedings of the National Academy of Sciences, USA 107, 14075–14080. PubMed PMC

Li HB, Müller M, Bahechar IA, Kyrchanova O, Ohno K, Georgiev P, Pirrotta V. 2011. Insulators, not Polycomb response elements, are required for long-range interactions between Polycomb targets in Drosophila melanogaster. Molecular and Cellular Biology 31, 616–625. PubMed PMC

Li HB, Ohno K, Gui H, Pirrotta V. 2013. Insulators target active genes to transcription factories and polycomb-repressed genes to polycomb bodies. PLoS Genetics 9, e1003436. PubMed PMC

Li P, Banjade S, Cheng HC, et al. . 2012. Phase transitions in the assembly of multivalent signalling proteins. Nature 483, 336–340. PubMed PMC

Libault M, Tessadori F, Germann S, Snijder B, Fransz P, Gaudin V. 2005. The Arabidopsis LHP1 protein is a component of euchromatin. Planta 222, 910–925. PubMed

Lieberman-Aiden E, van Berkum NL, Williams L, et al. . 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289–293. PubMed PMC

Lindhout BI, Fransz P, Tessadori F, Meckel T, Hooykaas PJ, van der Zaal BJ. 2007. Live cell imaging of repetitive DNA sequences via GFP-tagged polydactyl zinc finger proteins. Nucleic Acids Research 35, e107. PubMed PMC

Liti G, Louis EJ. 2003. NEJ1 prevents NHEJ-dependent telomere fusions in yeast without telomerase. Molecular Cell 11, 1373–1378. PubMed

Liu C, Cheng YJ, Wang JW, Weigel D. 2017. Prominent topologically associated domains differentiate global chromatin packing in rice from Arabidopsis. Nature Plants 3, 742–748. PubMed

Liu Q, Shi L, Fang Y. 2012. Dicing bodies. Plant Physiology 158, 61–66. PubMed PMC

Liu X, Wang C, Liu W, et al. . 2016. Distinct features of H3K4me3 and H3K27me3 chromatin domains in pre-implantation embryos. Nature 537, 558–562. PubMed

Liu Y, Liu Q, Yan Q, Shi L, Fang Y. 2014. Nucleolus-tethering system (NoTS) reveals that assembly of photobodies follows a self-organization model. Molecular Biology of the Cell 25, 1366–1373. PubMed PMC

Liu YG, Liu H, Chen L, et al. . 2002. Development of new transformation-competent artificial chromosome vectors and rice genomic libraries for efficient gene cloning. Gene 282, 247–255. PubMed

Liu YG, Shirano Y, Fukaki H, Yanai Y, Tasaka M, Tabata S, Shibata D. 1999. Complementation of plant mutants with large genomic DNA fragments by a transformation-competent artificial chromosome vector accelerates positional cloning. Proceedings of the National Academy of Sciences, USA 96, 6535–6540. PubMed PMC

Loubiere V, Martinez AM, Cavalli G. 2019. Cell fate and developmental regulation dynamics by polycomb proteins and 3D genome architecture. BioEssays 41, e1800222. PubMed

Love AJ, Yu C, Petukhova NV, Kalinina NO, Chen J, Taliansky ME. 2017. Cajal bodies and their role in plant stress and disease responses. RNA Biology 14, 779–790. PubMed PMC

Luke B, Lingner J. 2009. TERRA: telomeric repeat-containing RNA. The EMBO Journal 28, 2503–2510. PubMed PMC

Lundblad V, Wright WE. 1996. Telomeres and telomerase: a simple picture becomes complex. Cell 87, 369–375. PubMed

Lupiáñez DG, Kraft K, Heinrich V, et al. . 2015. Disruptions of topological chromatin domains cause pathogenic rewiring of gene–enhancer interactions. Cell 161, 1012–1025. PubMed PMC

Machyna M, Neugebauer KM, Staněk D. 2015. Coilin: the first 25 years. RNA Biology 12, 590–596. PubMed PMC

Maharana S, Wang J, Papadopoulos DK, et al. . 2018. RNA buffers the phase separation behavior of prion-like RNA binding proteins. Science 360, 918–921. PubMed PMC

Majerova E, Mandakova T, Vu GT, Fajkus J, Lysak MA, Fojtova M. 2014. Chromatin features of plant telomeric sequences at terminal vs. internal positions. Frontiers inPlant Science 5, 593. PubMed PMC

Malik HS, Henikoff S. 2009. Major evolutionary transitions in centromere complexity. Cell 138, 1067–1082. PubMed

Mao YS, Zhang B, Spector DL. 2011. Biogenesis and function of nuclear bodies. Trends in Genetics 27, 295–306. PubMed PMC

Marian CO, Bordoli SJ, Goltz M, Santarella RA, Jackson LP, Danilevskaya O, Beckstette M, Meeley R, Bass HW. 2003. The maize Single myb histone 1 gene, Smh1, belongs to a novel gene family and encodes a protein that binds telomere DNA repeats in vitro. Plant Physiology 133, 1336–1350. PubMed PMC

Masuda K, Xu ZJ, Takahashi S, Ito A, Ono M, Nomura K, Inoue M. 1997. Peripheral framework of carrot cell nucleus contains a novel protein predicted to exhibit a long alpha-helical domain. Experimental Cell Research 232, 173–181. PubMed

Mateo LJ, Murphy SE, Hafner A, Cinquini IS, Walker CA, Boettiger AN. 2019. Visualizing DNA folding and RNA in embryos at single-cell resolution. Nature 568, 49–54. PubMed PMC

Matera AG, Izaguire-Sierra M, Praveen K, Rajendra TK. 2009. Nuclear bodies: random aggregates of sticky proteins or crucibles of macromolecular assembly? Developmental Cell 17, 639–647. PubMed PMC

Matheson L, Elderkin S. 2018. Polycomb bodies .In: Lavelle C, Victor JM, eds. Nuclear architecture and dynamics, Vol. 2. Elsevier, 297–320.

McClintock B. 1934. The relation of a particular chromosomal element to the development of the nucleoli in Zea mays. Zeitschrift für Zellforschung und Mikroskopische Anatomie 21, 294–326.

McClintock B. 1941. The stability of broken ends of chromosomes in Zea mays. Genetics 26, 234–282. PubMed PMC

McClintock B. 1984. The significance of responses of the genome to challenge. Science 226, 792–801. PubMed

McKittrick E, Gafken PR, Ahmad K, Henikoff S. 2004. Histone H3.3 is enriched in covalent modifications associated with active chromatin. Proceedings of the National Academy of Sciences, USA 101, 1525–1530. PubMed PMC

Meier I, Richards EJ, Evans DE. 2017. Cell biology of the plant nucleus. Annual Review of Plant Biology 68, 139–172. PubMed

Melek M, Shippen DE. 1996. Chromosome healing: spontaneous and programmed de novo telomere formation by telomerase. Bioessays 18, 301–308. PubMed

Mikulski P, Hohenstatt ML, Farrona S, Smaczniak C, Stahl Y, Kalyanikrishna, Kaufmann K, Angenent G, Schubert D. 2019. The chromatin-associated protein PWO1 interacts with plant nuclear lamin-like components to regulate nuclear size. The Plant Cell 31, 1141–1154. PubMed PMC

Mintz PJ, Spector DL. 2000. Compartmentalization of RNA processing factors within nuclear speckles. Journal of Structural Biology 129, 241–251. PubMed

Moissiard G, Cokus SJ, Cary J, et al. . 2012. MORC family ATPases required for heterochromatin condensation and gene silencing. Science 336, 1448–1451. PubMed PMC

Molitor AM, Latrasse D, Zytnicki M, et al. . 2016. The Arabidopsis hnRNP-Q protein LIF2 and the PRC1 subunit LHP1 function in concert to regulate the transcription of stress-responsive genes. The Plant Cell 28, 2197–2211. PubMed PMC

Montacié C, Durut N, Opsomer A, et al. . 2017. Nucleolar proteome analysis and proteasomal activity assays reveal a link between nucleolus and 26S proteasome in A. thaliana. Frontiers in Plant Science 8, 1815. PubMed PMC

Montero JJ, López-Silanes I, Megías D, F Fraga M, Castells-García Á, Blasco MA. 2018. TERRA recruitment of polycomb to telomeres is essential for histone trimethylation marks at telomeric heterochromatin. Nature Communications 9, 1548. PubMed PMC

Moyzis RK, Buckingham JM, Cram LS, Dani M, Deaven LL, Jones MD, Meyne J, Ratliff RL, Wu JR. 1988. A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. Proceedings of the National Academy of Sciences, USA 85, 6622–6626. PubMed PMC

Mozgová I, Mikulski P, Pecinka A, Farrona S. 2019. Epigenetic mechanisms of abiotic stress response and memory in plants .In: Alvarez-Venegas R, De-la-Pena C, Cassas-Molano JA, eds. Epigenetics in plants of agronomic importance: fundamentals and applications. Cham: Springer International Publishing, 1–64.

Nagaki K, Talbert PB, Zhong CX, Dawe RK, Henikoff S, Jiang J. 2003. Chromatin immunoprecipitation reveals that the 180-bp satellite repeat is the key functional DNA element of Arabidopsis thaliana centromeres. Genetics 163, 1221–1225. PubMed PMC

Nakamura TM, Moser BA, Russell P. 2002. Telomere binding of checkpoint sensor and DNA repair proteins contributes to maintenance of functional fission yeast telomeres. Genetics 161, 1437–1452. PubMed PMC

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 Genetics 6, e1000889. PubMed PMC

Ng CK, Kinoshita T, Pandey S, Shimazaki K, Assmann SM. 2004. Abscisic acid induces rapid subnuclear reorganization in guard cells. Plant Physiology 134, 1327–1331. PubMed PMC

Nicodemi M, Pombo A. 2014. Models of chromosome structure. Current Opinion in Cell Biology 28, 90–95. PubMed

Ohtani M. 2017. Plant snRNP biogenesis: a perspective from the nucleolus and cajal bodies. Frontiers in Plant Science 8, 2184. PubMed PMC

Olovnikov AM. 1971. Principle of marginotomy in template synthesis of polynucleotides. Doklady Akademii Nauk SSSR 201, 1496–1499. PubMed

Ozer O, Hickson ID. 2018. Pathways for maintenance of telomeres and common fragile sites during DNA replication stress. Open Biology 8, 180018. PubMed PMC

Padeken J, Mendiburo MJ, Chlamydas S, Schwarz HJ, Kremmer E, Heun P. 2013. The nucleoplasmin homolog NLP mediates centromere clustering and anchoring to the nucleolus. Molecular Cell 50, 236–249. PubMed

Palm D, Simm S, Darm K, Weis BL, Ruprecht M, Schleiff E, Scharf C. 2016. Proteome distribution between nucleoplasm and nucleolus and its relation to ribosome biogenesis in Arabidopsis thaliana. RNA Biology 13, 441–454. PubMed PMC

Pawar V, Poulet A, Détourné G, Tatout C, Vanrobays E, Evans DE, Graumann K. 2016. A novel family of plant nuclear envelope-associated proteins. Journal of Experimental Botany 67, 5699–5710. PubMed

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. The Plant Cell 22, 3118–3129. PubMed PMC

Pecinka A, Schubert V, Meister A, Kreth G, Klatte M, Lysak MA, 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, 258–269. PubMed

Pederson T. 2011. The nucleolus. Cold Spring Harbor Perspectives in Biology 3, 1–15. PubMed PMC

Pendle AF, Clark GP, Boon R, Lewandowska D, Lam YW, Andersen J, Mann M, Lamond AI, Brown JW, Shaw PJ. 2005. Proteomic analysis of the Arabidopsis nucleolus suggests novel nucleolar functions. Molecular Biology of the Cell 16, 260–269. PubMed PMC

Picart C, Pontvianne F. 2017. Plant nucleolar DNA: green light shed on the role of nucleolin in genome organization. Nucleus 8, 11–16. PubMed PMC

Picart-Picolo A, Picart C, Picault N, Pontvianne F. 2020. Nucleolus-associated chromatin domains are maintained under heat stress, despite nucleolar reorganization in Arabidopsis thaliana. Journal of Plant Research doi: 10.1007/s10265-020-01201-3. PubMed DOI

Picart-Picolo A, Picault N, Pontvianne F. 2019. Ribosomal RNA genes shape chromatin domains associating with the nucleolus. Nucleus 10, 67–72. PubMed PMC

Pirrotta V, Li HB. 2012. A view of nuclear polycomb bodies. Current Opinion in Genetics & Development 22, 101–109. PubMed PMC

Pitchiaya S, Mourao MDA, Jalihal AP, Xiao L, Jiang X, Chinnaiyan AM, Schnell S, Walter NG. 2019. Dynamic recruitment of single RNAs to processing bodies depends on RNA functionality. Molecular Cell 74, 521–533.e6. PubMed PMC

Plys AJ, Davis CP, Kim J, Rizki G, Keenen MM, Marr SK, Kingston RE. 2019. Phase separation of Polycomb-repressive complex 1 is governed by a charged disordered region of CBX2. Genes & Development 33, 799–813. PubMed PMC

Pontes O, Pikaard CS. 2008. siRNA and miRNA processing: new functions for Cajal bodies. Current Opinion in Genetics & Development 18, 197–203. PubMed PMC

Pontes O, Vitins A, Ream TS, Hong E, Pikaard CS, Costa-Nunes P. 2013. Intersection of small RNA pathways in Arabidopsis thaliana sub-nuclear domains. PLoS One 8, e65652. PubMed PMC

Pontvianne F, Blevins T, Chandrasekhara C, Feng W, Stroud H, Jacobsen SE, Michaels SD, Pikaard CS. 2012. Histone methyltransferases regulating rRNA gene dose and dosage control in Arabidopsis. Genes & Development 26, 945–957. PubMed PMC

Pontvianne F, Blevins T, Chandrasekhara C, et al. . 2013. Subnuclear partitioning of rRNA genes between the nucleolus and nucleoplasm reflects alternative epiallelic states. Genes & Development 27, 1545–1550. PubMed PMC

Pontvianne F, Boyer-Clavel M, Sáez-Vásquez J. 2016a. Fluorescence-activated nucleolus sorting in Arabidopsis. Methods in Molecular Biology 1455, 203–211. PubMed

Pontvianne F, Carpentier MC, Durut N, et al. . 2016. b. Identification of nucleolus-associated chromatin domains reveals a role for the nucleolus in 3D organization of the A. thaliana genome. Cell Reports 16, 1574–1587. PubMed PMC

Pontvianne F, Grob S. 2020. Three-dimensional nuclear organization in Arabidopsis thaliana. Journal of Plant Research doi: 10.1007/s10265-020-01185-0. PubMed DOI

Pontvianne F, Liu C. 2019. Chromatin domains in space and their functional implications. Current Opinion in Plant Biology 54, 1–10. PubMed

Pontvianne F, Matía I, Douet J, Tourmente S, Medina FJ, Echeverria M, Sáez-Vásquez J. 2007. Characterization of AtNUC-L1 reveals a central role of nucleolin in nucleolus organization and silencing of AtNUC-L2 gene in Arabidopsis. Molecular Biology of the Cell 18, 369–379. PubMed PMC

Pott S, Lieb JD. 2015. What are super-enhancers? Nature Genetics 47, 8–12. PubMed

Poulet A, Duc C, Voisin M, Desset S, Tutois S, Vanrobays E, Benoit M, Evans DE, Probst AV, Tatout C. 2017a. The LINC complex contributes to heterochromatin organisation and transcriptional gene silencing in plants. Journal of Cell Science 130, 590–601. PubMed

Poulet A, Probst AV, Graumann K, Tatout C, Evans D. 2017b. Exploring the evolution of the proteins of the plant nuclear envelope. Nucleus 8, 46–59. PubMed PMC

Probst AV, Mittelsten Scheid O. 2015. Stress-induced structural changes in plant chromatin. Current Opinion in Plant Biology 27, 8–16. PubMed

Qiu Y, Pasoreck EK, Reddy AK, Nagatani A, Ma W, Chory J, Chen M. 2017. Mechanism of early light signaling by the carboxy-terminal output module of Arabidopsis phytochrome B. Nature Communications 8, 1905. PubMed PMC

Quinodoz SA, Ollikainen N, Tabak B, et al. . 2018. Higher-order inter-chromosomal hubs shape 3D genome organization in the nucleus. Cell 174, 744–757.e24. PubMed PMC

Reddy AS, Day IS, Göhring J, Barta A. 2012. Localization and dynamics of nuclear speckles in plants. Plant Physiology 158, 67–77. PubMed PMC

Ren X, Vincenz C, Kerppola TK. 2008. Changes in the distributions and dynamics of polycomb repressive complexes during embryonic stem cell differentiation. Molecular and Cellular Biology 28, 2884–2895. PubMed PMC

Riera M, Redko Y, Leung J. 2006. Arabidopsis RNA-binding protein UBA2a relocalizes into nuclear speckles in response to abscisic acid. FEBS Letters 580, 4160–4165. PubMed

Richards EJ, Ausubel FM. 1988. Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell 53, 127–136. PubMed

Ritossa FM, Spiegelman S. 1965. Localization of DNA complementary to ribosomal RNA in the nucleolus organizer region of Drosophila melanogaster. Proceedings of the National Academy of Sciences, USA 53, 737–745. PubMed PMC

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 & Development 27, 1845–1850. PubMed PMC

Rosa S, Shaw P. 2013. Insights into chromatin structure and dynamics in plants. Biology 2, 1378–1410. PubMed PMC

Sabari BR, Dall’Agnese A, Boija A, et al. . 2018. Coactivator condensation at super-enhancers links phase separation and gene control. Science 361, eaar3958. PubMed PMC

Sáez-Vásquez J, Delseny M. 2019. Ribosome biogenesis in plants: from functional 45S ribosomal DNA organization to ribosome assembly factors. The Plant Cell 31, 1945–1967. PubMed PMC

Sakamoto Y, Takagi S. 2013. LITTLE NUCLEI 1 and 4 regulate nuclear morphology in Arabidopsis thaliana. Plant & Cell Physiology 54, 622–633. PubMed

Sanborn AL, Rao SS, Huang SC, et al. . 2015. Chromatin extrusion explains key features of loop and domain formation in wild-type and engineered genomes. Proceedings of the National Academy of Sciences, USA 112, E6456–E6465. PubMed PMC

Santos AP, Abranches R, Oliveira M, Shaw P. 2015. Plasticity of chromatin organization in the plant interphase nucleus. In: Pontes O, Jin H, eds. Nuclear functions in plant transcription, signaling and development. New York: Springer New York, 57–79.

Santos AP, Abranches R, Stoger E, Beven A, Viegas W, Shaw PJ. 2002. The architecture of interphase chromosomes and gene positioning are altered by changes in DNA methylation and histone acetylation. Journal of Cell Science 115, 4597–4605. PubMed

Santos AP, Ferreira LJ, Oliveira MM. 2017. Concerted flexibility of chromatin structure, methylome, and histone modifications along with plant stress responses. Biology 6, 3. PubMed PMC

Santos AP, Shaw P. 2004. Interphase chromosomes and the Rabl configuration: does genome size matter? Journal of Microscopy 214, 201–206. PubMed

Sawyer IA, Sturgill D, Sung MH, Hager GL, Dundr M. 2016. Cajal body function in genome organization and transcriptome diversity. BioEssays 38, 1197–1208. PubMed PMC

Scarpin R, Sigaut L, Pietrasanta L, McCormick S, Zheng B, Muschietti J. 2013. Cajal bodies are developmentally regulated during pollen development and pollen tube growth in Arabidopsis thaliana. Molecular Plant 6, 1355–1357. PubMed

Schoeftner S, Blasco MA. 2008. Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nature Cell Biology 10, 228–236. PubMed

Schořová Š, Fajkus J, Záveská Drábková L, Honys D, Schrumpfová PP. 2019. The plant Pontin and Reptin homologues, RuvBL1 and RuvBL2a, colocalize with TERT and TRB proteins in vivo, and participate in telomerase biogenesis. The Plant Journal 98, 195–212. PubMed

Schrumpfová PP, Vychodilová I, Dvořáčková M, Majerská J, Dokládal L, Schořová S, Fajkus J. 2014. Telomere repeat binding proteins are functional components of Arabidopsis telomeres and interact with telomerase. The Plant Journal 77, 770–781. PubMed PMC

Schubert V, Weisshart K. 2015. Abundance and distribution of RNA polymerase II in Arabidopsis interphase nuclei. Journal of Experimental Botany 66, 1687–1698. PubMed PMC

Schwarzacher T, Anamthawat-Jónsson K, Harrison GE, et al. . 1992. Genomic in situ hybridization to identify alien chromosomes and chromosome segments in wheat. Theoretical and Applied Genetics 84, 778–786. PubMed

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. The Plant Cell 26, 2351–2366. PubMed PMC

Shah FR, Bhat YA, Wani AH. 2018. Subnuclear distribution of proteins: links with genome architecture. Nucleus 9, 42–55. PubMed PMC

Shaw J, Love AJ, Makarova SS, Kalinina NO, Harrison BD, Taliansky ME. 2014. Coilin, the signature protein of Cajal bodies, differentially modulates the interactions of plants with viruses in widely different taxa. Nucleus 5, 85–94. PubMed PMC

Shaw PJ, Brown JW. 2004. Plant nuclear bodies. Current Opinion in Plant Biology 7, 614–620. PubMed

Shibata F, Murata M. 2004. Differential localization of the centromere-specific proteins in the major centromeric satellite of Arabidopsis thaliana. Journal of Cell Science 117, 2963–2970. PubMed

Shin Y, Chang YC, Lee DSW, Berry J, Sanders DW, Ronceray P, Wingreen NS, Haataja M, Brangwynne CP. 2018. Liquid nuclear condensates mechanically sense and restructure the genome. Cell 175, 1481–1491.e13. PubMed PMC

Simon L, Voisin M, Tatout C, Probst AV. 2015. Structure and function of centromeric and pericentromeric heterochromatin in Arabidopsis thaliana. Frontiers in Plant Science 6, 1049. PubMed PMC

Smythe C, Jenkins HE, Hutchison CJ. 2000. Incorporation of the nuclear pore basket protein nup153 into nuclear pore structures is dependent upon lamina assembly: evidence from cell-free extracts of Xenopus eggs. The EMBO Journal 19, 3918–3931. PubMed PMC

Snoek BL, Pavlova P, Tessadori F, Peeters AJM, Bourbousse C, Barneche F, de Jong H, Fransz PF, van Zanten M. 2017. Genetic dissection of morphometric traits reveals that phytochrome B affects nucleus size and heterochromatin organization in Arabidopsis thaliana. G3 7, 2519–2531. PubMed PMC

Sobol M, Krausová A, Yildirim S, et al. . 2018. Nuclear phosphatidylinositol 4,5-bisphosphate islets contribute to efficient RNA polymerase II-dependent transcription. Journal of Cell Science 131, jcs.211094. PubMed

Soppe WJ, 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. The EMBO Journal 21, 6549–6559. PubMed PMC

Sotelo-Silveira M, Chávez Montes RA, Sotelo-Silveira JR, Marsch-Martínez N, de Folter S. 2018. Entering the next dimension: plant genomes in 3D. Trends in Plant Science 23, 598–612. PubMed

Spector DL, Lamond AI. 2011. Nuclear speckles. Cold Spring Harbor Perspectives in Biology 3, 1–12. PubMed PMC

Stam M, Tark-Dame M, Fransz P. 2019. 3D genome organization: a role for phase separation and loop extrusion? Current Opinion in Plant Biology 48, 36–46. PubMed

Staněk D, Fox AH. 2017. Nuclear bodies: news insights into structure and function. Current Opinion in Cell Biology 46, 94–101. PubMed

Stępiński D. 2014. Functional ultrastructure of the plant nucleolus. Protoplasma 251, 1285–1306. PubMed PMC

Strom AR, Brangwynne CP. 2019. The liquid nucleome—phase transitions in the nucleus at a glance. Journal of Cell Science 132, jcs.235093. PubMed PMC

Strom AR, Emelyanov AV, Mir M, Fyodorov DV, Darzacq X, Karpen GH. 2017. Phase separation drives heterochromatin domain formation. Nature 547, 241–245. PubMed PMC

Szabo Q, Bantignies F, Cavalli G. 2019. Principles of genome folding into topologically associating domains. Science Advances 5, eaaw1668. PubMed PMC

Szabo Q, Jost D, Chang JM, et al. . 2018. TADs are 3D structural units of higher-order chromosome organization in Drosophila. Science Advances 4, eaar8082. PubMed PMC

Sztacho M, Sobol M, Balaban C, Escudeiro Lopes SE, Hozák P. 2019. Nuclear phosphoinositides and phase separation: important players in nuclear compartmentalization. Advances in Biological Regulation 71, 111–117. PubMed

Tamura K, Fukao Y, Iwamoto M, Haraguchi T, Hara-Nishimura I. 2010. Identification and characterization of nuclear pore complex components in Arabidopsis thaliana. The Plant Cell 22, 4084–4097. PubMed PMC

Tamura K, Hara-Nishimura I. 2011. Involvement of the nuclear pore complex in morphology of the plant nucleus. Nucleus 2, 168–172. PubMed PMC

Tatavosian R, Kent S, Brown K, Yao T, Duc HN, Huynh TN, Zhen CY, Ma B, Wang H, Ren X. 2019. Nuclear condensates of the Polycomb protein chromobox 2 (CBX2) assemble through phase separation. Journal of Biological Chemistry 294, 1451–1463. PubMed PMC

Tek AL, Kashihara K, Murata M, Nagaki K. 2010. Functional centromeres in soybean include two distinct tandem repeats and a retrotransposon. Chromosome Research 18, 337–347. PubMed

Tek AL, Kashihara K, Murata M, Nagaki K. 2011. Functional centromeres in Astragalus sinicus include a compact centromere-specific histone H3 and a 20-bp tandem repeat. Chromosome Research 19, 969–978. PubMed

Turck F, Roudier F, Farrona S, Martin-Magniette ML, Guillaume E, Buisine N, Gagnot S, Martienssen RA, Coupland G, Colot V. 2007. Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genetics 3, e86. PubMed PMC

Ukmar-Godec T, Hutten S, Grieshop MP, Rezaei-Ghaleh N, Cima-Omori MS, Biernat J, Mandelkow E, Söding J, Dormann D, Zweckstetter M. 2019. Lysine/RNA-interactions drive and regulate biomolecular condensation. Nature Communications 10, 2909. PubMed PMC

Van Buskirk EK, Decker PV, Chen M. 2012. Photobodies in light signaling. Plant Physiology 158, 52–60. PubMed PMC

Van Buskirk EK, Reddy AK, Nagatani A, Chen M. 2014. Photobody localization of phytochrome B is tightly correlated with prolonged and light-dependent inhibition of hypocotyl elongation in the dark. Plant Physiology 165, 595–607. PubMed PMC

van Koningsbruggen S, Gierlinski 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. Molecular Biology of the Cell 21, 3735–3748. PubMed PMC

Vaquero-Sedas MI, Luo C, Vega-Palas MA. 2012. Analysis of the epigenetic status of telomeres by using ChIP-seq data. Nucleic Acids Research 40, e163. PubMed PMC

Vaquero-Sedas MI, Vega-Palas MA. 2013. Differential association of Arabidopsis telomeres and centromeres with histone H3 variants. Scientific Reports 3, 1202. PubMed PMC

Vertii A, Ou J, Yu J, Yan A, Pagès H, Liu H, Zhu LJ, Kaufman PD. 2019. Two contrasting classes of nucleolus-associated domains in mouse fibroblast heterochromatin. Genome Research 29, 1235–1249. PubMed PMC

Vrbsky J, Akimcheva S, Watson JM, Turner TL, Daxinger L, Vyskot B, Aufsatz W, RihaK. 2010. siRNA-mediated methylation of Arabidopsis telomeres. PLoS Genetics 6, e1000986. PubMed PMC

Walker MP, Tian L, Matera AG. 2009. Reduced viability, fertility and fecundity in mice lacking the cajal body marker protein, coilin. PLoS One 4, e6171. PubMed PMC

Wang H, Dittmer TA, Richards EJ. 2013. Arabidopsis CROWDED NUCLEI (CRWN) proteins are required for nuclear size control and heterochromatin organization. BMC Plant Biology 13, 200. PubMed PMC

Wang L, Gao Y, Zheng X, et al. . 2019. Histone modifications regulate chromatin compartmentalization by contributing to a phase separation mechanism. Molecular Cell 76, 646–659. PubMed

Wang M, Wang P, Lin M, Ye Z, Li G, Tu L, Shen C, Li J, Yang Q, Zhang X. 2018. Evolutionary dynamics of 3D genome architecture following polyploidization in cotton. Nature Plants 4, 90–97. PubMed

Wang Q, Sawyer IA, Sung MH, Sturgill D, Shevtsov SP, Pegoraro G, Hakim O, Baek S, Hager GL, Dundr M. 2016. Cajal bodies are linked to genome conformation. Nature Communications 7, 10966. PubMed PMC

Wang RC, Smogorzewska A, de Lange T. 2004. Homologous recombination generates T-loop-sized deletions at human telomeres. Cell 119, 355–368. PubMed

Warner JR, Soeiro R. 1967. Nascent ribosomes from HeLa cells. Proceedings of the National Academy of Sciences, USA 58, 1984–1990. PubMed PMC

Weaver DT. 1998. Telomeres: moonlighting by DNA repair proteins. Current Biology 8, R492–R494. PubMed

West JA, Mito M, Kurosaka S, et al. . 2016. Structural, super-resolution microscopy analysis of paraspeckle nuclear body organization. Journal of Cell Biology 214, 817–830. PubMed PMC

White MR, Mitrea DM, Zhang P, Stanley CB, Cassidy DE, Nourse A, Phillips AH, Tolbert M, Taylor JP, Kriwacki RW. 2019. C9orf72 Poly(PR) dipeptide repeats disturb biomolecular phase separation and disrupt nucleolar function. Molecular Cell 74, 713–728.e6. PubMed PMC

Xin R, Kathare PK, Huq E. 2019. Coordinated regulation of pre-mRNA splicing by the SFPS–RRC1 complex to promote photomorphogenesis. The Plant Cell 31, 2052–2069. PubMed PMC

Xin R, Zhu L, Salomé PA, Mancini E, Marshall CM, Harmon FG, Yanovsky MJ, Weigel D, Huq E. 2017. SPF45-related splicing factor for phytochrome signaling promotes photomorphogenesis by regulating pre-mRNA splicing in Arabidopsis. Proceedings of the National Academy of Sciences, USA 114, E7018–E7027. PubMed PMC

Yao RW, Xu G, Wang Y, et al. . 2019. Nascent pre-rRNA sorting via phase separation drives the assembly of dense fibrillar components in the human nucleolus. Molecular Cell 76, 767–783. PubMed

Yildirim S, Castano E, Sobol M, Philimonenko VV, Dzijak R, Venit T, Hozák P. 2013. Involvement of phosphatidylinositol 4,5-bisphosphate in RNA polymerase I transcription. Journal of Cell Science 126, 2730–2739. PubMed

Yokoyama Y, Takahashi Y, Shinohara A, Lian Z, Xiaoyun W, Niwa K, Tamaya T. 1998. Telomerase activity is found in the epithelial cells but not in the stromal cells in human endometrial cell culture. Molecular Human Reproduction 4, 985–989. PubMed

Yoo CY, Pasoreck EK, Wang H, Cao J, Blaha GM, Weigel D, Chen M. 2019. Phytochrome activates the plastid-encoded RNA polymerase for chloroplast biogenesis via nucleus-to-plastid signaling. Nature Communications 10, 2629. PubMed PMC

Zambrano-Mila MS, Aldaz-Villao MJ, Armando Casas-Mollano J. 2019. Canonical histones and their variants in plants: evolution and functions .In: Alvarez-Venegas R, De-la-Pena C, Cassas-Molano JA, eds. Epigenetics in plants of agronomic importance: fundamentals and applications. Cham: Springer International Publishing, 185–222.

Zhang C, Du X, Tang K, et al. . 2018. Arabidopsis AGDP1 links H3K9me2 to DNA methylation in heterochromatin. Nature Communications 9, 4547. PubMed PMC

Zhang W, Lee HR, Koo DH, Jiang J. 2008. Epigenetic modification of centromeric chromatin: hypomethylation of DNA sequences in the CENH3-associated chromatin in Arabidopsis thaliana and maize. The Plant Cell 20, 25–34. PubMed PMC

Zhang X, Germann S, Blus BJ, Khorasanizadeh S, Gaudin V, Jacobsen SE. 2007. The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trimethylation. Nature Structural & Molecular Biology 14, 869–871. PubMed

Zhang Y, Bertulat B, Tencer AH, Ren X, Wright GM, Black J, Cardoso MC, Kutateladze TG. 2019. MORC3 forms nuclear condensates through phase separation. iScience 17, 182–189. PubMed PMC

Zhao S, Cheng L, Gao Y, Zhang B, Zheng X, Wang L, Li P, Sun Q, Li H. 2019. Plant HP1 protein ADCP1 links multivalent H3K9 methylation readout to heterochromatin formation. Cell Research 29, 54–66. PubMed PMC

Zheng H, Xie W. 2019. The role of 3D genome organization in development and cell differentiation. Nature Reviews. Molecular Cell Biology 20, 535–550. PubMed

Zhou H, Song Z, Zhong S, Zuo L, Qi Z, Qu LJ, Lai L. 2019. Mechanism of DNA-induced phase separation for transcriptional repressor VRN1. Angewandte Chemie 58, 4858–4862. PubMed

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. The Plant Cell 28, 87–101. PubMed PMC

Zhou Y, Wang Y, Krause K, Yang T, Dongus JA, Zhang Y, Turck F. 2018. Telobox motifs recruit CLF/SWN–PRC2 for H3K27me3 deposition via TRB factors in Arabidopsis. Nature Genetics 50, 638–644. PubMed

Zhu L, Brangwynne CP. 2015. Nuclear bodies: the emerging biophysics of nucleoplasmic phases. Current Opinion in Cell Biology 34, 23–30. PubMed PMC

Editorial: Chromatin Stability and Dynamics: Targeting and Recruitment of Chromatin Modifiers

Large tandem duplications affect gene expression, 3D organization, and plant-pathogen response