Skip to main content
SpringerLink
Log in

The 4D Nucleome: Genome Compartmentalization in an Evolutionary Context

  • Review
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

4D nucleome research aims to understand the impact of nuclear organization in space and time on nuclear functions, such as gene expression patterns, chromatin replication, and the maintenance of genome integrity. In this review we describe evidence that the origin of 4D genome compartmentalization can be traced back to the prokaryotic world. In cell nuclei of animals and plants chromosomes occupy distinct territories, built up from ~1 Mb chromatin domains, which in turn are composed of smaller chromatin subdomains and also form larger chromatin domain clusters. Microscopic evidence for this higher order chromatin landscape was strengthened by chromosome conformation capture studies, in particular Hi-C. This approach demonstrated ~1 Mb sized, topologically associating domains in mammalian cell nuclei separated by boundaries. Mutations, which destroy boundaries, can result in developmental disorders and cancer. Nucleosomes appeared first as tetramers in the Archaea kingdom and later evolved to octamers built up each from two H2A, two H2B, two H3, and two H4 proteins. Notably, nucleosomes were lost during the evolution of the Dinoflagellata phylum. Dinoflagellate chromosomes remain condensed during the entire cell cycle, but their chromosome architecture differs radically from the architecture of other eukaryotes. In summary, the conservation of fundamental features of higher order chromatin arrangements throughout the evolution of metazoan animals suggests the existence of conserved, but still unknown mechanism(s) controlling this architecture. Notwithstanding this conservation, a comparison of metazoans and protists also demonstrates species-specific structural and functional features of nuclear organization.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ANC-INC:

active nuclear compartment/inactive nuclear compartment

CD:

chromatin domain

CDC:

chromatin domain cluster

CT:

chromosome territory

DAPI:

4′,6-diamidino-2-phenylindole

IC:

interchromatin compartment

PR:

perichromatin region

SIM:

structured illumination microscopy

TAD:

topologically associating domain

TF:

transcription factor

References

  1. Tashiro, S., and Lanctot, C. (2015) The International Nucleome Consortium, Nucleus, 6, 89–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Cremer, T., and Cremer, M. (2010) Chromosome territories, Cold Spring Harb. Perspect. Biol., 2, a003889.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Cremer, T., Kreth, G., Koester, H., Fink, R. H., Heintzmann, R., Cremer, M., Solovei, I., Zink, D., and Cremer, C. (2000) Chromosome territories, interchromatin domain compartment, and nuclear matrix: an integrated view of the functional nuclear architecture, Crit. Rev. Eukaryot. Gene Expr., 10, 179–212.

    Article  CAS  PubMed  Google Scholar 

  4. Cremer, T., and Cremer, C. (2001) Chromosome territories, nuclear architecture and gene regulation in mammalian cells, Nat. Rev. Genet., 2, 292–301.

    Article  CAS  PubMed  Google Scholar 

  5. Smeets, D., Markaki, Y., Schmid, V. J., Kraus, F., Tattermusch, A., Cerase, A., Sterr, M., Fiedler, S., Demmerle, J., Popken, J., Leonhardt, H., Brockdorff, N., Cremer, T., Schermelleh, L., and Cremer, M. (2014) Three-dimensional super-resolution microscopy of the inactive X chromosome territory reveals a collapse of its active nuclear compartment harboring distinct Xist RNA foci, Epigenetics Chromatin, 7, 8.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Cremer, T., Cremer, M., Hubner, B., Strickfaden, H., Smeets, D., Popken, J., Sterr, M., Markaki, Y., Rippe, K., and Cremer, C. (2015) The 4D nucleome: evidence for a dynamic nuclear landscape based on co-aligned active and inactive nuclear compartments, FEBS Lett., 589, 2931–2943.

    Article  CAS  PubMed  Google Scholar 

  7. Schmid, V. J., Cremer, M., and Cremer, T. (2017) Quantitative analyses of the 3D nuclear landscape recorded with super-resolved fluorescence microscopy, Methods, 123, 33–46.

    Article  CAS  PubMed  Google Scholar 

  8. Hubner, B., Lomiento, M., Mammoli, F., Illner, D., Markaki, Y., Ferrari, S., Cremer, M., and Cremer, T. (2015) Remodeling of nuclear landscapes during human myelopoietic cell differentiation maintains co-aligned active and inactive nuclear compartments, Epigenetics Chromatin, 8, 47.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Borsos, M., and Torres-Padilla, M. E. (2016) Building up the nucleus: nuclear organization in the establishment of totipotency and pluripotency during mammalian development, Genes Dev., 30, 611–621.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Brero, A., Easwaran, H. P., Nowak, D., Grunewald, I., Cremer, T., Leonhardt, H., and Cardoso, M. C. (2005) Methyl CpG-binding proteins induce large-scale chromatin reorganization during terminal differentiation, J. Cell Biol., 169, 733–743.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Mayer, R., Brero, A., von Hase, J., Schroeder, T., Cremer, T., and Dietzel, S. (2005) Common themes and cell type specific variations of higher order chromatin arrangements in the mouse, BMC Cell Biol., 6, 44.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Solovei, I., Grandi, N., Knoth, R., Volk, B., and Cremer, T. (2004) Positional changes of pericentromeric heterochromatin and nucleoli in postmitotic Purkinje cells during murine cerebellum development, Cytogenet. Genome Res., 105, 302–310.

    Article  Google Scholar 

  13. Solovei, I., Kreysing, M., Lanctot, C., Kosem, S., Peichl, L., Cremer, T., Guck, J., and Joffe, B. (2009) Nuclear architecture of rod photoreceptor cells adapts to vision in mammalian evolution, Cell, 137, 356–368.

    Article  CAS  PubMed  Google Scholar 

  14. Cremer, T., and Cremer, C. (2006) Rise, fall and resurrection of chromosome territories: a historical perspective. Part I. The rise of chromosome territories, Eur. J. Histochem., 50, 161–176.

    PubMed  Google Scholar 

  15. Razin, S. V., and Vassetzky, Y. S. (2017) 3D genomics imposes evolution of the domain model of eukaryotic genome organization, Chromosoma, 126, 59–69.

    Article  CAS  PubMed  Google Scholar 

  16. Bodnar, J. W. (1988) A domain model for eukaryotic DNA organization: a molecular basis for cell differentiation and chromosome evolution, J. Theor. Biol., 132, 479–507.

    Article  CAS  PubMed  Google Scholar 

  17. Goldman, M. A. (1988) The chromatin domain as a unit of gene regulation, Bioessays, 9, 50–55.

    Article  CAS  PubMed  Google Scholar 

  18. Monneron, A., and Bernhard, W. (1969) Fine structural organization of the interphase nucleus in some mammalian cells, J. Ultrastruct. Res., 27, 266–288.

    Article  CAS  PubMed  Google Scholar 

  19. Fakan, S. (2004) The functional architecture of the nucleus as analysed by ultrastructural cytochemistry, Histochem. Cell Biol., 122, 83–93.

    Article  CAS  PubMed  Google Scholar 

  20. Fakan, S., and van Driel, R. (2007) The perichromatin region: a functional compartment in the nucleus that determines large-scale chromatin folding, Semin. Cell Dev. Biol., 18, 676–681.

    Article  CAS  PubMed  Google Scholar 

  21. Rouquette, J., Cremer, C., Cremer, T., and Fakan, S. (2010) Functional nuclear architecture studied by microscopy: present and future, Int. Rev. Cell Mol. Biol., 282, 1–90.

    Article  CAS  PubMed  Google Scholar 

  22. Cmarko, D., Verschure, P. J., Martin, T. E., Dahmus, M. E., Krause, S., Fu, X. D., van Driel, R., and Fakan, S. (1999) Ultrastructural analysis of transcription and splicing in the cell nucleus after bromo-UTP microinjection, Mol. Biol. Cell, 10, 211–223.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Jaunin, F., Visser, A. E., Cmarko, D., Aten, J. A., and Fakan, S. (2000) Fine structural in situ analysis of nascent DNA movement following DNA replication, Exp. Cell Res., 260, 313–323.

    Article  CAS  PubMed  Google Scholar 

  24. Bornfleth, H., Edelmann, P., Zink, D., Cremer, T., and Cremer, C. (1999) Quantitative motion analysis of subchromosomal foci in living cells using four-dimensional microscopy, Biophys. J., 77, 2871–2886.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Strickfaden, H., Zunhammer, A., van Koningsbruggen, S., Kohler, D., and Cremer, T. (2010) 4D chromatin dynamics in cycling cells: Theodor Boveri’s hypotheses revisited, Nucleus, 1, 284–297.

    PubMed  PubMed Central  Google Scholar 

  26. Cremer, M., Schmid, V. J., Kraus, F., Markaki, Y., Hellmann, I., Maiser, A., Leonhardt, H., John, S., Stamatoyannopoulos, J., and Cremer, T. (2017) Initial high-resolution microscopic mapping of active and inactive regulatory sequences proves non-random 3D arrangements in chromatin domain clusters, Epigenetics Chromatin, 10, 39.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Popken, J., Brero, A., Koehler, D., Schmid, V. J., Strauss, A., Wuensch, A., Guengoer, T., Graf, A., Krebs, S., Blum, H., Zakhartchenko, V., Wolf, E., and Cremer, T. (2014) Reprogramming of fibroblast nuclei in cloned bovine embryos involves major structural remodeling with both striking similarities and differences to nuclear phenotypes of in vitro fertilized embryos, Nucleus, 5, 555–589.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Popken, J., Graf, A., Krebs, S., Blum, H., Schmid, V. J., Strauss, A., Guengoer, T., Zakhartchenko, V., Wolf, E., and Cremer, T. (2015) Remodeling of the nuclear envelope and lamina during bovine preimplantation development and its functional implications, PLoS One, 10, e0124619.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Chow, K. H., Factor, R. E., and Ullman, K. S. (2012) The nuclear envelope environment and its cancer connections, Nat. Rev. Cancer, 12, 196–209.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Zink, D., Fischer, A. H., and Nickerson, J. A. (2004) Nuclear structure in cancer cells, Nat. Rev. Cancer, 4, 677–687.

    Article  CAS  PubMed  Google Scholar 

  31. Razin, S. V., and Ulianov, S. V. (2017) Gene functioning and storage within a folded genome, Cell. Mol. Biol. Lett., 22, 18.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Ulianov, S. V., Gavrilov, A. A., and Razin, S. V. (2015) Nuclear compartments, genome folding, and enhancer–promoter communication, Int. Rev. Cell Mol. Biol., 315, 183–244.

    Article  PubMed  Google Scholar 

  33. Dekker, J., Rippe, K., Dekker, M., and Kleckner, N. (2002) Capturing chromosome conformation, Science, 295, 1306–1311.

    Article  CAS  PubMed  Google Scholar 

  34. Lieberman-Aiden, E., van Berkum, N. L., Williams, L., Imakaev, M., Ragoczy, T., Telling, A., Amit, I., Lajoie, B. R., Sabo, P. J., Dorschner, M. O., Sandstrom, R., Bernstein, B., Bender, M. A., Groudine, M., Gnirke, A., Stamatoyannopoulos, J., Mirny, L. A., Lander, E. S., and Dekker, J. (2009) Comprehensive mapping of long-range interactions reveals folding principles of the human genome, Science, 326, 289–293.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Le Dily, F., Serra, F., and Marti-Renom, M. A. (2017) 3D modeling of chromatin structure: is there a way to integrate and reconcile single cell and population experimental data? WIREs Comput. Mol. Sci., 7, e1308.

    Article  CAS  Google Scholar 

  36. Dixon, J. R., Gorkin, D. U., and Ren, B. (2016) Chromatin domains: the unit of chromosome organization, Mol. Cell, 62, 668–680.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Dixon, J. R., Selvaraj, S., Yue, F., Kim, A., Li, Y., Shen, Y., Hu, M., Liu, J. S., and Ren, B. (2012) Topological domains in mammalian genomes identified by analysis of chromatin interactions, Nature, 485, 376–380.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Fraser, J., Ferrai, C., Chiariello, A. M., Schueler, M., Rito, T., Laudanno, G., Barbieri, M., Moore, B. L., Kraemer, D. C., Aitken, S., Xie, S. Q., Morris, K. J., Itoh, M., Kawaji, H., Jaeger, I., Hayashizaki, Y., Carninci, P., Forrest, A. R., FANTOM Consortium, Semple, C. A., Dostie, J., Pombo, A., and Nicodemi, M. (2015) Hierarchical folding and reorganization of chromosomes are linked to transcriptional changes in cellular differentiation, Mol. Syst. Biol., 11, 852.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Rao, S. S., Huntley, M. H., Durand, N. C., Stamenova, E. K., Bochkov, I. D., Robinson, J. T., Sanborn, A. L., Machol, I., Omer, A. D., Lander, E. S., and Aiden, E. L. (2014) A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping, Cell, 159, 1665–1680.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Furlan-Magaril, M., Varnai, C., Nagano, T., and Fraser, P. (2015) 3D genome architecture from populations to single cells, Curr. Opin. Genet. Dev., 31, 36–41.

    Article  CAS  PubMed  Google Scholar 

  41. Nagano, T., Lubling, Y., Stevens, T. J., Schoenfelder, S., Yaffe, E., Dean, W., Laue, E. D., Tanay, A., and Fraser, P. (2013) Single-cell Hi-C reveals cell-to-cell variability in chromosome structure, Nature, 502, 59–64.

    Article  CAS  PubMed  Google Scholar 

  42. Nagano, T., Lubling, Y., Yaffe, E., Wingett, S. W., Dean, W., Tanay, A., and Fraser, P. (2015) Single-cell Hi-C for genome-wide detection of chromatin interactions that occur simultaneously in a single cell, Nat. Protoc., 10, 1986–2003.

    Article  CAS  PubMed  Google Scholar 

  43. Stevens, T. J., Lando, D., Basu, S., Atkinson, L. P., Cao, Y., Lee, S. F., Leeb, M., Wohlfahrt, K. J., Boucher, W., O’Shaughnessy-Kirwan, A., Cramard, J., Faure, A. J., Ralser, M., Blanco, E., Morey, L., Sanso, M., Palayret, M. G. S., Lehner, B., Di Croce, L., Wutz, A., Hendrich, B., Klenerman, D., and Laue, E. D. (2017) 3D structures of individual mammalian genomes studied by single-cell Hi-C, Nature, 544, 59–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Ulianov, S. V., Tachibana-Konwalski, K., and Razin, S. V. (2017) Single-cell Hi-C bridges microscopy and genome-wide sequencing approaches to study 3D chromatin organization, Bioessays, 39, No. 10; doi: 10.1002/bies.201700104; Epub 2017 Aug 9.

  45. Fullwood, M. J., and Ruan, Y. (2009) ChIP-based methods for the identification of long-range chromatin interactions, J. Cell. Biochem., 107, 30–39.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Ji, X., Dadon, D. B., Powell, B. E., Fan, Z. P., Borges-Rivera, D., Shachar, S., Weintraub, A. S., Hnisz, D., Pegoraro, G., Lee, T. I., Misteli, T., Jaenisch, R., and Young, R. A. (2016) 3D chromosome regulatory landscape of human pluripotent cells, Cell Stem Cell, 18, 262–275.

    Article  CAS  PubMed  Google Scholar 

  47. Ong, C. T., and Corces, V. G. (2014) CTCF: an architectural protein bridging genome topology and function, Nat. Rev. Genet., 15, 234–246.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Sanborn, A. L., Rao, S. S., Huang, S. C., Durand, N. C., Huntley, M. H., Jewett, A. I., Bochkov, I. D., Chinnappan, D., Cutkosky, A., Li, J., Geeting, K. P., Gnirke, A., Melnikov, A., McKenna, D., Stamenova, E. K., Lander, E. S., and Aiden, E. L. (2015) Chromatin extrusion explains key features of loop and domain formation in wild-type and engineered genomes, Proc. Natl. Acad. Sci. USA, 112, e6456-6465.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Rao, S. S. P., Huang, S. C., Glenn St Hilaire, B., Engreitz, J. M., Perez, E. M., Kieffer-Kwon, K. R., Sanborn, A. L., Johnstone, S. E., Bascom, G. D., Bochkov, I. D., Huang, X., Shamim, M. S., Shin, J., Turner, D., Ye, Z., Omer, A. D., Robinson, J. T., Schlick, T., Bernstein, B. E., Casellas, R., Lander, E. S., and Aiden, E. L. (2017) Cohesin loss eliminates all loop domains, Cell, 171, 305–320.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Franke, M., Ibrahim, D. M., Andrey, G., Schwarzer, W., Heinrich, V., Schopflin, R., Kraft, K., Kempfer, R., Jerkovic, I., Chan, W. L., Spielmann, M., Timmermann, B., Wittler, L., Kurth, I., Cambiaso, P., Zuffardi, O., Houge, G., Lambie, L., Brancati, F., Pombo, A., Vingron, M., Spitz, F., and Mundlos, S. (2016) Formation of new chromatin domains determines pathogenicity of genomic duplications, Nature, 538, 265–269.

    Article  CAS  PubMed  Google Scholar 

  51. Lupianez, D. G., Spielmann, M., and Mundlos, S. (2016) Breaking TADs: how alterations of chromatin domains result in disease, Trends Genet., 32, 225–237.

    Article  CAS  PubMed  Google Scholar 

  52. Achinger-Kawecka, J., and Clark, S. J. (2017) Disruption of the 3D cancer genome blueprint, Epigenomics, 9, 47–55.

    Article  CAS  PubMed  Google Scholar 

  53. Flavahan, W. A., Drier, Y., Liau, B. B., Gillespie, S. M., Venteicher, A. S., Stemmer-Rachamimov, A. O., Suva, M. L., and Bernstein, B. E. (2016) Insulator dysfunction and oncogene activation in IDH mutant gliomas, Nature, 529, 110–114.

    Article  CAS  PubMed  Google Scholar 

  54. Harmston, N., Ing-Simmons, E., Tan, G., Perry, M., Merkenschlager, M., and Lenhard, B. (2017) Topologically associating domains are ancient features that coincide with metazoan clusters of extreme noncoding conservation, Nat. Commun., 8, 441.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  55. Acemel, R. D., Maeso, I., and Gomez-Skarmeta, J. L. (2017) Topologically associated domains: a successful scaffold for the evolution of gene regulation in animals, Wiley Interdiscip. Rev. Dev. Biol., 6, No. 3; doi: 10.1002/wdev.265; Epub 2017 Mar 2.

  56. Rowley, M. J., Nichols, M. H., Lyu, X., Ando-Kuri, M., Rivera, I. S. M., Hermetz, K., Wang, P., Ruan, Y., and Corces, V. G. (2017) Evolutionarily conserved principles predict 3D chromatin organization, Mol. Cell., 67, 837–852.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Liu, C., Cheng, Y. J., Wang, J. W., and Weigel, D. (2017) Prominent topologically associated domains differentiate global chromatin packing in rice from Arabidopsis, Nat. Plants, 3, 742–748.

    Article  CAS  PubMed  Google Scholar 

  58. Feng, S., Cokus, S. J., Schubert, V., Zhai, J., Pellegrini, M., and Jacobsen, S. E. (2014) Genome-wide Hi-C analy-ses in wild-type and mutants reveal high-resolution chromatin interactions in Arabidopsis, Mol. Cell., 55, 694–707.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Bickmore, W. A. (2013) The spatial organization of the human genome, Annu. Rev. Genom. Hum. Genet., 14, 67–84.

    Article  CAS  Google Scholar 

  60. Bolzer, A., Kreth, G., Solovei, I., Koehler, D., Saracoglu, K., Fauth, C., Muller, S., Eils, R., Cremer, C., Speicher, M. R., and Cremer, T. (2005) Three-dimensional maps of all chromosomes in human male fibroblast nuclei and prometaphase rosettes, PLoS Biol., 3, e157.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Boyle, S., Gilchrist, S., Bridger, J. M., Mahy, N. L., Ellis, J. A., and Bickmore, W. A. (2001) The spatial organization of human chromosomes within the nuclei of normal and emerin-mutant cells, Hum. Mol. Genet., 10, 211–219.

    Article  CAS  PubMed  Google Scholar 

  62. Cremer, M., von Hase, J., Volm, T., Brero, A., Kreth, G., Walter, J., Fischer, C., Solovei, I., Cremer, C., and Cremer, T. (2001) Non-random radial higher-order chromatin arrangements in nuclei of diploid human cells, Chromosome Res., 9, 541–567.

    Article  CAS  PubMed  Google Scholar 

  63. Croft, J. A., Bridger, J. M., Boyle, S., Perry, P., Teague, P., and Bickmore, W. A. (1999) Differences in the localization and morphology of chromosomes in the human nucleus, J. Cell Biol., 145, 1119–1131.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Tanabe, H., Muller, S., Neusser, M., von Hase, J., Calcagno, E., Cremer, M., Solovei, I., Cremer, C., and Cremer, T. (2002) Evolutionary conservation of chromosome territory arrangements in cell nuclei from higher primates, Proc. Natl. Acad. Sci. USA, 99, 4424–4429.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Habermann, F. A., Cremer, M., Walter, J., Kreth, G., von Hase, J., Bauer, K., Wienberg, J., Cremer, C., Cremer, T., and Solovei, I. (2001) Arrangements of macro-and microchromosomes in chicken cells, Chromosome Res., 9, 569–584.

    Article  CAS  PubMed  Google Scholar 

  66. Alexandrova, O., Solovei, I., Cremer, T., and David, C. N. (2003) Replication labeling patterns and chromosome territories typical of mammalian nuclei are conserved in the early metazoan Hydra, Chromosoma, 112, 190–200.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  68. Fransz, P., and de Jong, H. (2011) From nucleosome to chromosome: a dynamic organization of genetic information, Plant J., 66, 4–17.

    Article  CAS  PubMed  Google Scholar 

  69. Grob, S., and Grossniklaus, U. (2017) Chromosome conformation capture-based studies reveal novel features of plant nuclear architecture, Curr. Opin. Plant Biol., 36, 149–157.

    Article  CAS  PubMed  Google Scholar 

  70. Heslop-Harrison, J. S., and Schwarzacher, T. (2011) Organisation of the plant genome in chromosomes, Plant J., 66, 18–33.

    Article  CAS  PubMed  Google Scholar 

  71. Liu, C., and Weigel, D. (2015) Chromatin in 3D: progress and prospects for plants, Genome Biol., 16, 170.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Pawlowski, W. P. (2010) Chromosome organization and dynamics in plants, Curr. Opin. Plant Biol., 13, 640–645.

    Article  CAS  PubMed  Google Scholar 

  73. Schubert, I., and Shaw, P. (2011) Organization and dynamics of plant interphase chromosomes, Trends Plant. Sci., 16, 273–281.

    Article  CAS  PubMed  Google Scholar 

  74. Schubert, V., Meister, A., Tsujimoto, H., Endo, T. R., and Houben, A. (2011) Similar rye A and B chromosome organization in meristematic and differentiated interphase nuclei, Chromosome Res., 19, 645–655.

    Article  CAS  PubMed  Google Scholar 

  75. Vergara, Z., and Gutierrez, C. (2017) Emerging roles of chromatin in the maintenance of genome organization and function in plants, Genome Biol., 18, 96.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Wang, C., Liu, C., Roqueiro, D., Grimm, D., Schwab, R., Becker, C., Lanz, C., and Weigel, D. (2015) Genome-wide analysis of local chromatin packing in Arabidopsis thaliana, Genome Res., 25, 246–256.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  77. Perrella, G., and Kaiserli, E. (2016) Light behind the curtain: photoregulation of nuclear architecture and chromatin dynamics in plants, New Phytol., 212, 908–919.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Joffe, B., Peichl, P., Hendrickson, A., Leonhardt, H., and Solovei, I. (2014) Diurnality and nocturnality in primates: an analysis from the rod photoreceptor nuclei perspective, Evol. Biol., 41, 1–11.

    Article  Google Scholar 

  79. Kizilyaprak, C., Spehner, D., Devys, D., and Schultz, P. (2010) In vivo chromatin organization of mouse rod photoreceptors correlates with histone modifications, PLoS One, 5, e11039.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. Solovei, I., Wang, A. S., Thanisch, K., Schmidt, C. S., Krebs, S., Zwerger, M., Cohen, T. V., Devys, D., Foisner, R., Peichl, L., Herrmann, H., Blum, H., Engelkamp, D., Stewart, C. L., Leonhardt, H., and Joffe, B. (2013) LBR and lamin A/C sequentially tether peripheral heterochromatin and inversely regulate differentiation, Cell, 152, 584–598.

    Article  CAS  PubMed  Google Scholar 

  81. Blaszczak, Z., Kreysing, M., and Guck, J. (2014) Direct observation of light focusing by single photoreceptor cell nuclei, Opt. Express, 22, 11043–11060.

    Article  PubMed  Google Scholar 

  82. Kreysing, M., Boyde, L., Guck, J., and Chalut, K. J. (2010) Physical insight into light scattering by photoreceptor cell nuclei, Opt. Lett., 35, 2639–2641.

    Article  PubMed  Google Scholar 

  83. Ma, Y., and Buttitta, L. (2017) Chromatin organization changes during the establishment and maintenance of the postmitotic state, Epigenetics Chromatin, 10, 53.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  84. Bickmore, W. A., and van Steensel, B. (2013) Genome architecture: domain organization of interphase chromosomes, Cell, 152, 1270–1284.

    Article  CAS  PubMed  Google Scholar 

  85. Van Steensel, B., and Belmont, A. S. (2017) Lamina-associated domains: links with chromosome architecture, heterochromatin, and gene repression, Cell, 169, 780–791.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. Bi, X., Cheng, Y. J., Hu, B., Ma, X., Wu, R., Wang, J. W., and Liu, C. (2017) Nonrandom domain organization of the Arabidopsis genome at the nuclear periphery, Genome Res., 27, 1162–1173.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Hsu, T. C. (1975) A possible function of constitutive heterochromatin: the bodyguard hypothesis, Genetics, 79 (Suppl.), 137–150.

    PubMed  Google Scholar 

  88. Gazave, E., Gautier, P., Gilchrist, S., and Bickmore, W. A. (2005) Does radial nuclear organisation influence DNA damage? Chromosome Res., 13, 377–388.

    Article  CAS  PubMed  Google Scholar 

  89. Smith, K. S., Liu, L. L., Ganesan, S., Michor, F., and De, S. (2017) Nuclear topology modulates the mutational landscapes of cancer genomes, Nat. Struct. Mol. Biol., 24, 1000–1006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Qiu, G. H. (2015) Protection of the genome and central protein-coding sequences by non-coding DNA against DNA damage from radiation, Mutat. Res. Rev. Mutat. Res., 764, 108–117.

    Article  CAS  PubMed  Google Scholar 

  91. Belousov, V. V., Enikolopov, G. N., and Mishina, N. M. (2013) Compartmentalization of ROS-mediated signal transduction, Bioorg. Khim., 39, 383–399.

    CAS  PubMed  Google Scholar 

  92. Yakes, F. M., and Van Houten, B. (1997) Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress, Proc. Natl. Acad. Sci. USA, 94, 514–519.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Obe, G., Pfeiffer, P., Savage, J. R., Johannes, C., Goedecke, W., Jeppesen, P., Natarajan, A. T., Martinez-Lopez, W., Folle, G. A., and Drets, M. E. (2002) Chromosomal aberrations: formation, identification and distribution, Mutat. Res., 504, 17–36.

    CAS  Google Scholar 

  94. Martin, W., Baross, J., Kelley, D., and Russell, M. J. (2008) Hydrothermal vents and the origin of life, Nat. Rev. Microbiol., 6, 805–814.

    Article  CAS  PubMed  Google Scholar 

  95. Mulkidjanian, A. Y., Bychkov, A. Y., Dibrova, D. V., Galperin, M. Y., and Koonin, E. V. (2012) Origin of first cells at terrestrial, anoxic geothermal fields, Proc. Natl. Acad. Sci. USA, 109, e821–830.

    Article  CAS  PubMed  Google Scholar 

  96. Speijer, D. (2015) Birth of the eukaryotes by a set of reactive innovations: new insights force us to relinquish gradual models, Bioessays, 37, 1268–1276.

    Article  CAS  PubMed  Google Scholar 

  97. Postberg, J., Lipps, H. J., and Cremer, T. (2010) Evolutionary origin of the cell nucleus and its functional architecture, Essays Biochem., 48, 1–24.

    Article  CAS  PubMed  Google Scholar 

  98. Pereira, S. L., Grayling, R. A., Lurz, R., and Reeve, J. N. (1997) Archaeal nucleosomes, Proc. Natl. Acad. Sci. USA, 94, 12633–12637.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Mattiroli, F., Bhattacharyya, S., Dyer, P. N., White, A. E., Sandman, K., Burkhart, B. W., Byrne, K. R., Lee, T., Ahn, N. G., Santangelo, T. J., Reeve, J. N., and Luger, K. (2017) Structure of histone-based chromatin in Archaea, Science, 357, 609–612.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Luger, K., Mader, A. W., Richmond, R. K., Sargent, D. F., and Richmond, T. J. (1997) Crystal structure of the nucleosome core particle at 2.8 Å resolution, Nature, 389, 251–260.

    Article  CAS  PubMed  Google Scholar 

  101. Tanizawa, H., Kim, K. D., Iwasaki, O., and Noma, K. I. (2017) Architectural alterations of the fission yeast genome during the cell cycle, Nat. Struct. Mol. Biol., 24, 965–976.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Gursoy, G., Xu, Y., and Liang, J. (2017) Spatial organization of the budding yeast genome in the cell nucleus and identification of specific chromatin interactions from multi-chromosome constrained chromatin model, PLoS Comput. Biol., 13, e1005658.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  103. Iwasaki, O., Corcoran, C. J., and Noma, K. (2016) Involvement of condensin-directed gene associations in the organization and regulation of chromosome territories during the cell cycle, Nucleic Acids Res., 44, 3618–3628.

    Article  CAS  PubMed  Google Scholar 

  104. Gasser, S. M. (2002) Visualizing chromatin dynamics in interphase nuclei, Science, 296, 1412–1416.

    Article  CAS  PubMed  Google Scholar 

  105. Taddei, A., and Gasser, S. M. (2012) Structure and function in the budding yeast nucleus, Genetics, 192, 107–129.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Chubb, J. R., and Bickmore, W. A. (2003) Considering nuclear compartmentalization in the light of nuclear dynamics, Cell, 112, 403–406.

    Article  CAS  PubMed  Google Scholar 

  107. Selig, S., Okumura, K., Ward, D. C., and Cedar, H. (1992) Delineation of DNA replication time zones by fluorescence in situ hybridization, EMBO J., 11, 1217–1225.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Yalon, M., Gal, S., Segev, Y., Selig, S., and Skorecki, K. L. (2004) Sister chromatid separation at human telomeric regions, J. Cell Sci., 117, 1961–1970.

    Article  CAS  PubMed  Google Scholar 

  109. Amitai, A., Seeber, A., Gasser, S. M., and Holcman, D. (2017) Visualization of chromatin decompaction and break site extrusion as predicted by statistical polymer modeling of single-locus trajectories, Cell Rep., 18, 1200–1214.

    Article  CAS  PubMed  Google Scholar 

  110. Seeber, A., and Gasser, S. M. (2017) Chromatin organization and dynamics in double-strand break repair, Curr. Opin. Genet. Dev., 43, 9–16.

    Article  CAS  PubMed  Google Scholar 

  111. Shen, Y., Buick, R., and Canfield, D. E. (2001) Isotopic evidence for microbial sulphate reduction in the early archaean era, Nature, 410, 77–81.

    Article  CAS  PubMed  Google Scholar 

  112. Knoll, A. H. (1999) A new molecular window on early life, Science, 285, 1025–1026.

    Article  CAS  PubMed  Google Scholar 

  113. Levi-Setti, R., Gavrilov, K. L., and Rizzo, P. J. (2008) Divalent cation distribution in dinoflagellate chromosomes imaged by high-resolution ion probe mass spectrometry, Eur. J. Cell Biol., 87, 963–976.

    Article  CAS  PubMed  Google Scholar 

  114. Chan, Y. H., and Wong, J. T. (2007) Concentration-dependent organization of DNA by the dinoflagellate histone-like protein HCc3, Nucleic Acids Res., 35, 2573–2583.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Marbouty, M., Le Gall, A., Cattoni, D. I., Cournac, A., Koh, A., Fiche, J. B., Mozziconacci, J., Murray, H., Koszul, R., and Nollmann, M. (2015) Condensin-and replication-mediated bacterial chromosome folding and origin condensation revealed by Hi-C and super-resolution imaging, Mol. Cell, 59, 588–602.

    Article  CAS  PubMed  Google Scholar 

  116. Gornik, S. G., Ford, K. L., Mulhern, T. D., Bacic, A., McFadden, G. I., and Waller, R. F. (2012) Loss of nucleosomal DNA condensation coincides with appearance of a novel nuclear protein in dinoflagellates, Curr. Biol., 22, 2303–2312.

    Article  CAS  PubMed  Google Scholar 

  117. Wong, J. T., New, D. C., Wong, J. C., and Hung, V. K. (2003) Histonelike proteins of the dinoflagellate Crypthecodinium cohnii have homologies to bacterial DNA-binding proteins, Eukaryot. Cell, 2, 646–650.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Eltsov, M., and Zuber, B. (2006) Transmission electron microscopy of the bacterial nucleoid, J. Struct. Biol., 156, 246–254.

    Article  CAS  PubMed  Google Scholar 

  119. Feijoo-Siota, L., Rama, J. L. R., Sanchez-Perez, A., and Villa, T. G. (2017) Considerations on bacterial nucleoids, Appl. Microbiol. Biotechnol., 101, 5591–5602.

    Article  CAS  PubMed  Google Scholar 

  120. Fisher, J. K., Bourniquel, A., Witz, G., Weiner, B., Prentiss, M., and Kleckner, N. (2013) Four-dimensional imaging of E. coli nucleoid organization and dynamics in living cells, Cell, 153, 882–895.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Macvanin, M., and Adhya, S. (2012) Architectural organization in E. coli nucleoid, Biochim. Biophys. Acta, 1819, 830–835.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Peeters, E., Driessen, R. P., Werner, F., and Dame, R. T. (2015) The interplay between nucleoid organization and transcription in archaeal genomes, Nat. Rev. Microbiol., 13, 333–341.

    Article  CAS  PubMed  Google Scholar 

  123. Smits, W. K., Goranov, A. I., and Grossman, A. D. (2010) Ordered association of helicase loader proteins with the Bacillus subtilis origin of replication in vivo, Mol. Microbiol., 75, 452–461.

    Article  CAS  PubMed  Google Scholar 

  124. Archibald, J. M. (2011) Origin of eukaryotic cells: 40 years on, Symbiosis, 54, 69–86.

    Article  Google Scholar 

  125. Takata, H., Hanafusa, T., Mori, T., Shimura, M., Iida, Y., Ishikawa, K., Yoshikawa, K., Yoshikawa, Y., and Maeshima, K. (2013) Chromatin compaction protects genomic DNA from radiation damage, PLoS One, 8, e75622.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Biocenter, Department of Biology II, Ludwig Maximilian University (LMU), Munich, 82152 Martinsried, Germany

    T. Cremer & M. Cremer

  2. Institute of Molecular Biology (IMB) Mainz, 55128, Mainz, Germany

    C. Cremer

Authors
  1. T. Cremer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Cremer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. Cremer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to T. Cremer.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cremer, T., Cremer, M. & Cremer, C. The 4D Nucleome: Genome Compartmentalization in an Evolutionary Context. Biochemistry Moscow 83, 313–325 (2018). https://doi.org/10.1134/S000629791804003X

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S000629791804003X

Keywords

Search

Navigation