Abstract
In recent years, the study of plant three-dimensional nuclear architecture received increasing attention. Enabled by technological advances, our knowledge on nuclear architecture has greatly increased and we can now access large data sets describing its manifold aspects. The principles of nuclear organization in plants do not significantly differ from those in animals. Plant nuclear organization comprises various scales, ranging from gene loops to topologically associating domains to nuclear compartmentalization. However, whether plant three-dimensional chromosomal features also exert similar functions as in animals is less clear. This review discusses recent advances in the fields of three-dimensional chromosome folding and nuclear compartmentalization and describes a novel silencing mechanism, which is closely linked to nuclear architecture.
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References
Alexandre CM, Hennig L (2008) FLC or not FLC: the other side of vernalization. J Exp Bot 59:1127–1135
Alipour E, Marko JF (2012) Self-organization of domain structures by DNA-loop-extruding enzymes. Nucleic Acids Res 40:11202–11212
Andrey P, Kiêu K, Kress C, Lehmann G, Tirichine L, Liu Z, Biot E, Adenot PG, Hue-Beauvais C, Houba-Hérin N et al (2010) Statistical analysis of 3D images detects regular spatial distributions of centromeres and chromocenters in animal and plant nuclei. PLoS Comput Biol 6:27
Ariel F, Jegu T, Latrasse D, Romero-Barrios N, Christ A, Benhamed M, Crespi M (2014) Noncoding transcription by alternative RNA polymerases dynamically regulates an auxin-driven chromatin loop. Mol Cell 55:383–396
Armstrong SJ, Franklin FC, Jones GH (2001) Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. J Cell Sci 114:4207–4217
Arteaga-Vazquez M, Sidorenko L, Rabanal FA, Shrivistava R, Nobuta K, Green PJ, Meyers BC, Chandler VL (2010) RNA-mediated trans-communication can establish paramutation at the b1 locus in maize. Proc Natl Acad Sci 107:12986–12991
Barneche F, Malapeira J, Paloma M (2014) The impact of chromatin dynamics on plant light responses and circadian clock function. J Exp Bot 65:2895–2913
Bi X, Cheng Y, Hu B, Ma X, Wu R, Wang J (2017) Nonrandom domain organization of the Arabidopsis genome at the nuclear periphery. Genome Res 27:1162–1173
Bonev B, Cavalli G (2016) Organization and function of the 3D genome. Nat Rev Genet 17:772
Cao S, Kumimoto RW, Gnesutta N, Calogero AM, Mantovani R, Holt BF (2014) A distal CCAAT/NUCLEAR FACTOR Y complex promotes chromatin looping at the FLOWERING LOCUS T promoter and regulates the timing of flowering in Arabidopsis. Plant Cell 26:1009–1017
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 30:177–190
Cook PR, Marenduzzo D (2018) Transcription-driven genome organization: a model for chromosome structure and the regulation of gene expression tested through simulations. Nucleic Acids Res 46:9895–9906
Cremer T, Cremer C (2001) Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat Rev Genet 2:292–301
Crevillén P, Sonmez C, Wu Z, Dean C (2013) A gene loop containing the floral repressor FLC is disrupted in the early phase of vernalization. EMBO J 32:140–148
Dekker J, Rippe K, Dekker M, Kleckner N (2002) Capturing chromosome conformation. Science 295:1306–1311
Dittmer TA, Stacey NJ, Sugimoto-Shirasu K, Richards EJ (2007) LITTLE NUCLEI genes affecting nuclear morphology in Arabidopsis thaliana. Plant Cell 19:2793–2803
Doğan ES, Liu C (2018) Three-dimensional chromatin packing and positioning of plant genomes. Nat Plants 4:521–529
Dong P, Tu X, Chu P, Peitao L, Zhu N, Grierson D, Du B, Li P, Zhong S (2017) 3D chromatin architecture of large plant genomes determined by local A/B compartments. Mol Plant 10:1497–1509
Dong Q, Li N, Li X, Yuan Z, Xie D, Wang X, Li J, Yu Y, Wang J, Ding B et al (2018) Genome-wide Hi-C analysis reveals extensive hierarchical chromatin interactions in rice. Plant J 94:1141–1156
Dong P, Tu X, Li H, Zhang J, Grierson D, Li P, Zhong S (2019) Tissue-specific Hi-C analyses of rice, foxtail millet and maize suggest non-canonical function of plant chromatin domains. J Integr Plant Biol 20:20
Fang Y, Spector DL (2005) Centromere positioning and dynamics in living Arabidopsis plants. Mol Biol Cell 16:5710–5718
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
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 USA 99:14584–14589
Grob S (2019) Three-dimensional chromosome organization in flowering plants. Brief Funct Genom 20:024
Grob S, Grossniklaus U (2017) Chromosome conformation capture-based studies reveal novel features of plant nuclear architecture. Curr Opin Plant Biol 36:149–157
Grob S, Grossniklaus U (2019) Invasive DNA elements modify the nuclear architecture of their insertion site by KNOT-linked silencing in Arabidopsis thaliana. Genome Biol 20:120
Grob S, Schmid MW, Luedtke NW, Wicker T, Grossniklaus U (2013) Characterization of chromosomal architecture in Arabidopsis by chromosome conformation capture. Genome Biol 14:R129
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
Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB, Talhout W, Eussen BH, de Klein A, Wessels L, De Laat W et al (2008) Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453:948–951
Guo Y, Xu Q, Canzio D, Krainer AR, Maniatis T, Guo Y, Xu Q, Canzio D, Shou J, Li J et al (2015) CRISPR inversion of CTCF sites alters genome topology and enhancer/promoter function. Cell 162:900–910
Guo L, Cao X, Liu Y, Li J, Li Y, Li D, Zhang K, Gao C, Dong A, Liu X (2018) A chromatin loop represses WUSCHEL expression in Arabidopsis. Plant J 94:1083–1097
Heitz E (1928) Das Heterochromatin der Moose. Jahrbücher Für Wissenschaftliche Bot 69:762–818
Hollick JB (2016) Paramutation and related phenomena in diverse species. Nat Rev Genet 18:5–23
Hu B, Wang N, Bi X, Karaaslan ES, Weber A, Zhu W, Berendzen KW, Liu C (2019a) Plant lamin-like proteins mediate chromatin tethering at the nuclear periphery. Genome Biol 20:20
Hu L, Xu Z, Wang M, Fan R, Yuan D, Wu B, Wu H, Qin X, Yan L, Tan L et al (2019b) The chromosome-scale reference genome of black pepper provides insight into piperine biosynthesis. Nat Commun 10:4702
Hu Y, Chen J, Fang L, Zhang Z, Ma W, Niu Y, Ju L, Deng J, Zhao T, Lian J et al (2019c) Gossypium barbadense and Gossypium hirsutum genomes provide insights into the origin and evolution of allotetraploid cotton. Nat Genet 51:739–748
Jegu T, Latrasse D, Delarue M, Hirt H, Domenichini S, Ariel F, Crespi M, Bergounioux C, Raynaud C, Benhamed M (2014) The BAF60 subunit of the SWI/SNF chromatin-remodeling complex directly controls the formation of a gene loop at FLOWERING LOCUS C in Arabidopsis. Plant Cell 26:538–551
Jégu T, Domenichini S, Blein T, Ariel F, Christ A, Kim S, Crespi M, Boutet-Mercey S, Mouille G, Bourge M et al (2015) A SWI/SNF chromatin remodelling protein controls cytokinin production through the regulation of chromatin architecture. PLoS ONE 10:e0138276
Jégu T, Veluchamy A, Ramirez-prado JS, Rizzi-paillet C, Perez M, Lhomme A, Latrasse D, Coleno E, Vicaire S, Legras S et al (2017) The Arabidopsis SWI/SNF protein BAF60 mediates seedling growth control by modulating DNA accessibility. Genome Biol 18:1–16
Jibran R, Dzierzon H, Bassil N, Bushakra JM, Edger PP, Sullivan S, Finn CE, Dossett M, Vining KJ, Vanburen R et al (2018) Chromosome-scale scaffolding of the black raspberry (Rubus occidentalis L.) genome based on chromatin interaction data. Hortic Res 20:5
Kaiserli E, Pa K, Donnell LO, Nusinow DA, Kay SA, Chory J, Donnell LO, Batalov O, Pedmale UV, Nusinow DA et al (2015) Integration of light and photoperiodic signaling in transcriptional nuclear foci. Dev Cell 20:311–321
Kind J, Pagie L, Ortabozkoyun H, Boyle S, de Vries SS, Janssen H, Amendola M, Nolen LD, Bickmore WA, van Steensel B (2013) Single-cell dynamics of genome–nuclear lamina interactions. Cell 153:178–192
van Köningsbruggen 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
Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-hernandez M et al (2012) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 40:1202–1210
Li E, Liu H, Huang L, Zhang X, Dong X, Song W, Zhao H, Lai J (2019) Long-range interactions between proximal and distal regulatory regions in maize. Nat Commun 10:2633
Lieberman-Aiden E, Van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie BR, Sabo PJ, Dorschner MO et al (2009) Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326:289–293
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 133:523–536
Liu C, Teo ZWN, Bi Y, Song S, Xi W, Yang X, Yin Z, Yu H (2013) A conserved genetic pathway determines inflorescence architecture in arabidopsis and rice. Dev Cell 24:612–622
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 26:1057–1068
Liu C, Cheng Y-J, Wang J-W, Weigel D (2017) Prominent topologically associated domains differentiate global chromatin packing in rice from Arabidopsis. Nat Plants 3:742–748
Louwers M, Bader R, Haring M, Van Driel R, De Laat W, Stam M (2009) Tissue- and expression level-specific chromatin looping at maize b1 epialleles. Plant Cell 21:832–842
Maccaferri M, Harris NS, Twardziok SO, Pasam RK, Gundlach H, Spannagl M, Ormanbekova D, Lux T, Prade VM, Milner SG et al (2019) Durum wheat genome highlights past domestication signatures and future improvement targets. Nat Genet 51:885–895
Mascher M, Gundlach H, Himmelbach A, Beier S, Twardziok SO, Wicker T, Radchuk V, Dockter C, Hedley PE, Russell J et al (2017) A chromosome conformation capture ordered sequence of the barley genome. Nature 544:427–433
McEachern LA, Lloyd VK (2012) The maize b1 paramutation control region causes epigenetic silencing in Drosophila melanogaster. Mol Genet Genom 287:591–606
Mikulski P, Hohenstatt ML, Farrona S, Smaczniak C, Stahl Y, Kaufmann K, Angenent G, Schubert D (2019) The chromatin-associated protein PWO1 interacts with plant nuclear lamin-like components to regulate nuclear size. Plant Cell 31:1141–1154
Moissiard G, Cokus SJ, Cary J, Feng S, Billi AC, Stroud H, Husmann D, Zhan Y, Lajoie BR, McCord RP et al (2012) MORC family ATPases required for heterochromatin condensation and gene silencing. Science 336:1448–1451
Montacié C, Durut N, Opsomer A, Palm D, Comella P, Picart C, Carpentier M-C, Pontvianne F, Carapito C, Schleiff E et al (2017) Nucleolar proteome analysis and proteasomal activity assays reveal a link between nucleolus and 26S proteasome in A. thaliana. Front Plant Sci 8:1815
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 6:1–11
Pavet V, Quintero C, Cecchini NM, Rosa AL, Alvarez ME (2006) Arabidopsis displays centromeric dna hypomethylation and cytological alterations of heterochromatin upon attack by Pseudomonas syringae. Mol Plant-Microbe Interact 19:577–587
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
Pecinka A, Dinh HQ, Baubec T, Rosa M, Lettner N, Scheid OM (2010) Epigenetic regulation of repetitive elements is attenuated by prolonged heat stress in Arabidopsis. Plant Cell 22:3118–3129
Peng Y, Xiong D, Zhao L, Ouyang W, Wang S, Sun J, Zhang Q, Guan P, Xie L, Li W et al (2019) Chromatin interaction maps reveal genetic regulation for quantitative traits in maize. Nat Commun 10:2632
Phillips JE, Corces VG (2009) CTCF: master weaver of the genome. Cell 137:1194–1211
Picart C, Pontvianne F (2017) Plant nucleolar DNA: green light shed on the role of Nucleolin in genome organization. Nucleus 8:11–16
Picart-Picolo A, Picault N, Pontvianne F (2019) Ribosomal RNA genes shape chromatin domains associating with the nucleolus. Nucleus 10:67–72
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
Pontvianne F, Blevins T, Hassel C, Pontes OMF, Muchova V, Tucker S, Mokros P, Muchova V, Fajkus J, Pikaard CS (2013) Subnuclear partitioning of rRNA genes between the nucleolus and nucleoplasm reflects alternative epiallelic states. Genes Dev 27:1545–1550
Pontvianne F, Boyer-Clavel M, Sáez-Vásquez J (2016a) Fluorescence-activated nucleolus sorting in Arabidopsis. In: Németh A (ed) The nucleolus: methods and protocols. Springer, New York, pp 203–211
Pontvianne F, Carpentier MC, Durut N, Pavlištová V, Jaške K, Schořová Š, Parrinello H, Rohmer M, Pikaard CS, Fojtová M et al (2016b) 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
Poulet A, Duc C, Voisin M, Desset S, Tutois S, Vanrobays E, Benoit M, Evans DE, Probst AV, Tatout C (2017) The LINC complex contributes to heterochromatin organisation and transcriptional gene silencing in plants. J. Cell Sci. 130:590–601
Quinodoz SA, Ollikainen N, Tabak B, Palla A, Schmidt JM, Detmar E, Lai MM, Shishkin AA, Bhat P, Takei Y et al (2018) Higher-Order Inter-chromosomal hubs shape 3D genome organization in the nucleus. Cell 174:744–757.e24
Rada-Iglesias A, Grosveld FG, Papantonis A (2018) Forces driving the three-dimensional folding of eukaryotic genomes. Mol Syst Biol 14:e8214
Raymond O, Gouzy J, Just J, Badouin H, Verdenaud M, Lemainque A, Vergne P, Moja S, Choisne N, Pont C et al (2018) The Rosa genome provides new insights into the domestication of modern roses. Nat Genet 50:772–777
Richter R, Kinoshita A, Vincent C, Martinez-Gallegos R, Gao H, van Driel AD, Hyun Y, Mateos JL, Coupland G (2019) Floral regulators FLC and SOC1 directly regulate expression of the B3-type transcription factor TARGET OF FLC AND SVP 1 at the Arabidopsis shoot apex via antagonistic chromatin modifications. PLoS Genet 15:e1008065
Rowley MJ, Corces VG (2018) Organizational principles of 3D genome architecture. Nat Rev Genet 19:789–800
Rowley MJ, Nichols MH, Lyu X, Ando-Kuri M, Riviera SM, Hermetz K, Wang P, Ruan Y, Corces VG (2017) Evolutionarily conserved principles predict 3D chromatin organization. Mol Cell 67:837–852.e7
Sáez-Vásquez J, Delseny M (2019) Ribosome biogenesis in plants: from functional 45S ribosomal DNA organization to ribosome assembly factors. Plant Cell 31:1945–1967
Sakamoto Y, Takagi S (2013) LITTLE NUCLEI 1 and 4 regulate nuclear morphology in Arabidopsis thaliana. Plant Cell Physiol 54:622–633
Sanborn AL, Rao SSP, Huang S, Durand NC, Huntley MH, Jewett AI, Bochkow ID, Chinnappan D, Cutkosky A, Jian L et al (2015) Chromatin extrusion explains key features of loop and domain formation in wild-type and engineered genomes. Proc Natl Acad Sci US A 112:E6456–E6465
Santos AP, Shaw P (2004) Interphase chromosomes and the Rabl configuration: does genome size matter? J Microsc 214:201–206
dos Santos G, Schroeder AJ, Goodman JL, Strelets VB, Crosby MA, Thurmond J, Emmert DB, Gelbart WM (2015) FlyBase: introduction of the Drosophila melanogaster Release 6 reference genome assembly and large-scale migration of genome annotations. Nucleic Acids Res. 43:D690–D697
Schubert V, Weißleder A, Ali H, Fuchs J, Lermontova I, Meister A, Schubert I (2009) Cohesin gene defects may impair sister chromatid alignment and genome stability in Arabidopsis thaliana. Chromosoma 118:591–605
Schwarzer W, Abdennur N, Goloborodko A, Pekowska A, Fudenberg G, Loe-mie Y, Fonseca NA, Huber W, Haering CH, Mirny L et al (2017) Two independent modes of chromatin organization revealed by cohesin removal. Nature 551:51–56
Sexton T, Cavalli G (2015) The role of chromosome domains in shaping the functional genome. Cell 160:1049–1059
Sexton T, Yaffe E, Kenigsberg E, Bantignies F, Leblanc B, Hoichman M, Parrinello H, Tanay A, Cavalli G (2012) Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 148:458–472
Shi J, Ma X, Zhang J, Zhou Y, Liu M, Huang L, Sun S, Zhang X, Gao X, Zhan W et al (2019) Chromosome conformation capture resolved near complete genome assembly of broomcorn millet. Nat Commun 10:464
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 Plant Sci 23:598–612
Stam M, Tark-dame M, Fransz P (2019) 3D genome organization: a role for phase separation and loop extrusion? Curr Opin Plant Biol 48:36–46
Strom AR, Emelyanov AV, Mir M, Fyodorov DV, Darzacq X, Karpen GH (2017) Phase separation drives heterochromatin domain formation. Nature 547:241–245
Stroud H, Do T, Du J, Zhong X, Feng S, Johnson L, Patel DJ, Jacobsen SE (2014) Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat Struct Mol Biol 21:64–72
Swiezewski S, Liu F, Magusin A, Dean C (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462:799–802
Szabo Q, Jost D, Chang J, Cattoni DI, Papadopoulos GL, Bonev B, Sexton T, Gurgo J, Jacquier C, Nollmann M et al (2018) TADs are 3D structural units of higher-order chromosome organization in Drosophila. Sci Adv 4:eaar8082
Szabo Q, Bantignies F, Cavalli G (2019) Principles of genome folding into topologically associating domains. Sci Adv 5:eaaw1668
Tessadori F, Schulkes RK, Driel RV, Fransz P (2007) Light-regulated large-scale reorganization of chromatin during the floral transition in Arabidopsis. Plant J 2:848–857
VanBuren R, Wai CM, Pardo J, Giarola V, Ambrosini S, Song X, Bartels D (2018) Desiccation tolerance evolved through gene duplication and network rewiring in Lindernia. Plant Cell 30:2943–2958
Vertii A, Ou J, Yu J, Yan A, Pagès H, Liu H, Zhu LJ (2019) Two contrasting classes of nucleolus-associated domains in mouse fibroblast heterochromatin. Genome Res 29:1235–1249
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. Nat Plants 4:90–97
Wang H, Li S, Li Y, Xu Y, Wang Y, Zhang R, Sun W, Chen Q, Wang X, Li C et al (2019) MED25 connects enhancer–promoter looping and MYC2-dependent activation of jasmonate signalling. Nat Plants 5:616–625
Weis BL, Kovacevic J, Missbach S, Schleiff E (2015) Plant-specific features of ribosome biogenesis. Trends Plant Sci 20:729–740
Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW-L, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE et al (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126:1189–1201
Zhang L, Cai X, Wu J, Liu M, Grob S, Cheng F, Liang J, Cai C, Liu Z, Liu B et al (2018) Improved Brassica rapa reference genome by single-molecule sequencing and chromosome conformation capture technologies. Hortic Res 20:5
Zhu W, Hu B, Becker C, Süheyla E, Berendzen KW (2017) Altered chromatin compaction and histone methylation drive non-additive gene expression in an interspecific Arabidopsis hybrid. Genome Biol 18:157
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FP is supported by CNRS, the ANR JCJC NucleoReg [ANR-15-CE12-0013-01] and the French Laboratory of Excellence project TULIP (ANR-10-LABX-41 and ANR-11-IDEX-0002-02). SG is supported by the University of Zurich.
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Pontvianne, F., Grob, S. Three-dimensional nuclear organization in Arabidopsis thaliana. J Plant Res 133, 479–488 (2020). https://doi.org/10.1007/s10265-020-01185-0
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DOI: https://doi.org/10.1007/s10265-020-01185-0