Global nuclear reorganization during heterochromatin replication in the giant-genome plant Nigella damascena L.

Publisher: Blackwell Scientific Publishers and BIOS Scientific Publishers in association with the Society for Experimental Biology Country of Publication: England NLM ID: 9207397 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1365-313X (Electronic) Linking ISSN: 09607412 NLM ISO Abbreviation: Plant J Subsets: MEDLINE

Original Publication: Oxford : Blackwell Scientific Publishers and BIOS Scientific Publishers in association with the Society for Experimental Biology, c1991-

Heterochromatin*/genetics ; Heterochromatin*/metabolism ; Genome, Plant*/genetics ; Cell Nucleus*/metabolism ; Cell Nucleus*/genetics ; DNA Replication*; Meristem/genetics ; Meristem/ultrastructure ; Interphase/genetics ; DNA, Plant/genetics ; DNA, Plant/metabolism

Among flowering plants, genome size varies remarkably, by >2200-fold, and this variation depends on the loss and gain of noncoding DNA sequences that form distinct heterochromatin complexes during interphase. In plants with giant genomes, most chromatin remains condensed during interphase, forming a dense network of heterochromatin threads called interphase chromonemata. Using super-resolution light and electron microscopy, we studied the ultrastructure of chromonemata during and after replication in root meristem nuclei of Nigella damascena L. During S-phase, heterochromatin undergoes transient decondensation locally at DNA replication sites. Due to the abundance of heterochromatin, the replication leads to a robust disassembly of the chromonema meshwork and a general reorganization of the nuclear morphology visible even by conventional light microscopy. After replication, heterochromatin recondenses, restoring the chromonema structure. Thus, we show that heterochromatin replication in interphase nuclei of giant-genome plants induces a global nuclear reorganization.
(© 2024 Society for Experimental Biology and John Wiley & Sons Ltd.)

Arifulin, E.A. (2015) Ultrastructural organization of replicating chromatin in prematurely condensed chromosomes. Biopolymers and Cell, 31, 249–254.
Arumuganathan, K. & Earle, E.D. (1991) Nuclear DNA content of some important plant species. Plant Molecular Biology Reporter, 9, 208–218.
Bai, C., Alverson, W.S., Follansbee, A. & Waller, D.M. (2012) New reports of nuclear DNA content for 407 vascular plant taxa from the United States. Annals of Botany, 110, 1623–1629.
Baranetzky, J. (1880) Die Kerntheilung in den Pollenmutterzellen einiger Tradescantien. Botanische Zeitschrift, 38, 281–296.
Baranyi, M. & Greilhuber, J. (1999) Genome size in Allium: in quest of reproducible data. Annals of Botany, 83, 687–695.
Barow, M. & Meister, A. (2003) Endopolyploidy in seed plants is differently correlated to systematics, organ, life strategy and genome size. Plant, Cell & Environment, 26, 571–584.
Bass, H.W., Hoffman, G.G., Lee, T.‐J., Wear, E.E., Joseph, S.R., Allen, G.C. et al. (2015) Defining multiple, distinct, and shared spatiotemporal patterns of DNA replication and endoreduplication from 3D image analysis of developing maize (Zea mays L.) root tip nuclei. Plant Molecular Biology, 89, 339–351.
Bennett, M.D. & Smith, J.B. (1976) Nuclear DNA amounts in angiosperms. Philosophical Transactions of the Royal Society, B: Biological Sciences, 274, 227–274.
Câmara, A.S., Kubalová, I. & Schubert, V. (2024) Helical chromonema coiling is conserved in eukaryotes. The Plant Journal, 118, 1284–1300.
Ceccarelli, M., Morosi, L. & Cionini, P.G. (1998) Chromocenter association in plant cell nuclei: determinants, functional significance, and evolutionary implications. Genome, 41, 96–103.
Chagin, V.O., Reinhart, B., Becker, A., Mortusewicz, O., Jost, K.L., Rapp, A. et al. (2019) Processive DNA synthesis is associated with localized decompaction of constitutive heterochromatin at the sites of DNA replication and repair. Nucleus, 10, 231–253.
Chen, M.‐S., Niu, L., Zhao, M.‐L., Xu, C., Pan, B.Z., Fu, Q. et al. (2020) De novo genome assembly and Hi‐C analysis reveal an association between chromatin architecture alterations and sex differentiation in the woody plant Jatropha curcas. GigaScience, 9, giaa009.
de la Torre, C., Sacristán‐Gárate, A. & Navarrete, M.H. (1975) Structural changes in chromatin during interphase. Chromosoma, 51, 183–198.
Dong, P., Tu, X., Chu, P.‐Y., Lü, P., Zhu, N., Grierson, D. et al. (2017) 3D chromatin architecture of large plant genomes determined by local A/B compartments. Molecular Plant, 10, 1497–1509.
Doyle, J.J. & Doyle, J.L. (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin, 19, 11–15.
Falk, M., Feodorova, Y., Naumova, N., Imakaev, M., Lajoie, B.R., Leonhardt, H. et al. (2019) Heterochromatin drives compartmentalization of inverted and conventional nuclei. Nature, 570, 395–399.
Feodorova, Y., Falk, M., Mirny, L.A. & Solovei, I. (2020) Viewing nuclear architecture through the eyes of nocturnal mammals. Trends in Cell Biology, 30, 276–289.
Fleischmann, A., Michael, T.P., Rivadavia, F., Sousa, A., Wang, W., Temsch, E.M. et al. (2014) Evolution of genome size and chromosome number in the carnivorous plant genus Genlisea (Lentibulariaceae), with a new estimate of the minimum genome size in angiosperms. Annals of Botany, 114, 1651–1663.
Fransz, P. & de Jong, H. (2011) From nucleosome to chromosome: a dynamic organization of genetic information. The Plant Journal, 66, 4–17.
Fransz, P., de Jong, J.H., Lysak, M., Castiglione, M.R. & 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 of the United States of America, 99, 14584–14589.
Gregory, T.R. (2005) The C‐value enigma in plants and animals: a review of parallels and an appeal for partnership. Annals of Botany, 95, 133–146.
Gregory, T.R. (2011) The evolution of the genome. San Diego: Elsevier.
Grime, J.P. & Mowforth, M.A. (1982) Variation in genome size—an ecological interpretation. Nature, 299, 151–153.
Guillotin, B., Rahni, R., Passalacqua, M., Mohammed, M.A., Xu, X., Raju, S.K. et al. (2023) A pan‐grass transcriptome reveals patterns of cellular divergence in crops. Nature, 617, 785–791.
Hao, S., Jiao, M., Zhao, J., Xing, M. & Huang, B. (1994) Reorganization and condensation of chromatin in mitotic prophase nuclei of Allium cepa. Chromosoma, 103, 432–440.
Hendrix, B. & Stewart, J.M. (2005) Estimation of the nuclear DNA content of gossypium species. Annals of Botany, 95, 789–797.
Jakob, S.S., Meister, A. & Blattner, F.R. (2004) The considerable genome size variation of Hordeum species (Poaceae) is linked to phylogeny, life form, ecology, and speciation rates. Molecular Biology and Evolution, 21, 860–869.
Jasencakova, Z., Meister, A. & Schubert, I. (2001) Chromatin organization and its relation to replication and histone acetylation during the cell cycle in barley. Chromosoma, 110, 83–92.
Johnston, J.S., Pepper, A.E., Hall, A.E., Chen, Z.J., Hodnett, G., Drabek, J. et al. (2005) Evolution of genome size in Brassicaceae. Annals of Botany, 95, 229–235.
Kapusta, A., Suh, A. & Feschotte, C. (2017) Dynamics of genome size evolution in birds and mammals. Proceedings of the National Academy of Sciences of the United States of America, 114, E1460–E1469.
Klásterská, I. & Natarajan, A.T. (1975) Distribution of heterochromatin in the chromosomes of Nigella damascena and Vicia faba. Hereditas, 79, 154–156.
Kron, P. & Husband, B.C. (2012) Using flow cytometry to estimate pollen DNA content: improved methodology and applications. Annals of Botany, 110, 1067–1078.
Kubalová, I., Câmara, A.S., Cápal, P., Beseda, T., Rouillard, J.M., Krause, G.M. et al. (2023) Helical coiling of metaphase chromatids. Nucleic Acids Research, 51, 2641–2654.
Kubalová, I., Němečková, A., Weisshart, K., Hřibová, E. & Schubert, V. (2021) Comparing super‐resolution microscopy techniques to analyze chromosomes. International Journal of Molecular Sciences, 22, 1903.
Kubešová, M., Moravcova, L., Suda, J., Jarošík, V. & Pyšek, P. (2010) Naturalized plants have smaller genomes than their non‐invading relatives: a flow cytometric analysis of the Czech alien flora. Preslia, 82, 81–96.
Kuznetsova, M.A., Chaban, I.A. & Sheval, E.V. (2017) Visualization of chromosome condensation in plants with large chromosomes. BMC Plant Biology, 17, 153.
Kuznetsova, M.A. & Sheval, E.V. (2016) Chromatin fibers: from classical descriptions to modern interpretation. Cell Biology International, 40, 1140–1151.
Lafontaine, J.G. & Lord, A. (1974) An ultrastructural and radioautographic study of the evolution of the interphase nucleus in plant meristematic cells (Allium porrum). Journal of Cell Science, 14, 263–287.
Lee, S.‐I. & Kim, N.‐S. (2014) Transposable elements and genome size variations in plants. Genomics & Informatics, 12, 87–97.
Leitch, I.J., Hanson, L., Lim, K.Y., Kovarik, A., Chase, M.W., Clarkson, J.J. et al. (2008) The ups and downs of genome size evolution in polyploid species of Nicotiana (Solanaceae). Annals of Botany, 101, 805–814.
Li, B., Lin, D., Zhai, X., Fan, G., Zhao, Z., Cao, X. et al. (2022) Conformational changes in three‐dimensional chromatin structure in Paulownia fortunei after Phytoplasma infection. Phytopathology, 112, 373–386.
Li, Z., McKibben, M.T.W., Finch, G.S., Blischak, P.D., Sutherland, B.L. & Barker, M.S. (2021) Patterns and processes of diploidization in land plants. Annual Review of Plant Biology, 72, 387–410.
Lieberman‐Aiden, E., van Berkum, N.L., Williams, L., Imakaev, M., Ragoczy, T., Telling, A. et al. (2009) Comprehensive mapping of long‐range interactions reveals folding principles of the human genome. Science, 326, 289–293.
Manton, I. (1950) The spiral structure of chromosomes. Biological Reviews of the Cambridge Philosophical Society, 25, 486–508.
Marie, D. & Brown, S.C. (1993) A cytometric exercise in plant DNA histograms, with 2C values for 70 species. Biology of the Cell, 78, 41–51.
Michael, T.P. (2014) Plant genome size variation: bloating and purging DNA. Briefings in Functional Genomics, 13, 308–317.
Montgomery, S.A., Tanizawa, Y., Galik, B., Wang, N., Ito, T., Mochizuki, T. et al. (2020) Chromatin organization in early land plants reveals an ancestral association between H3K27me3, transposons, and constitutive heterochromatin. Current Biology, 30, 573–588.e7.
Murray, B.G., Hammett, K.R.W. & Standring, L.S. (1992) Genomic constancy during the development of Lathyrus odoratus cultivars. Heredity, 68, 321–327.
Nagl, W. (1985) Chromatin organization and the control of gene activity. International Review of Cytology, 94, 21–56.
Nagl, W. & Bachmann, K. (1980) Condensed chromatin in diploid and allopolyploid microseris species with different genome size: a quantitative electron microscopic study. Theoretical and Applied Genetics, 57, 107–111.
Nagl, W. & Fusenig, H.‐P. (1979) Types of chromatin organization in plant nuclei. In: Nagl, W., Hemleben, V. & Ehrendorfer, F. (Eds.) Genome and chromatin: organization, evolution, function: Symposium, Kaiserslautern, October 13–15, 1978. Vienna: Springer, pp. 221–233.
Nagl, W., Jeanjour, M., Kling, H., Kuhner, S., Michels, I., Muller, T. et al. (1983) Genome and chromatin organization in higher‐plants. Biologisches Zentralblatt, 102, 129–148.
Natarajan, A.T. & Ahnström, G. (1969) Heterochromatin and chromosome aberrations. Chromosoma, 28, 48–61.
Němečková, A., Koláčková, V., Vrána, J., Doležel, J. & Hřibová, E. (2020) DNA replication and chromosome positioning throughout the interphase in three‐dimensional space of plant nuclei. Journal of Experimental Botany, 71, 6262–6272.
Novák, P., Neumann, P. & Macas, J. (2020) Global analysis of repetitive DNA from unassembled sequence reads using RepeatExplorer2. Nature Protocols, 15, 3745–3776.
Nowicka, A., Sliwinska, E., Grzebelus, D., Baranski, R., Simon, P.W., Nothnagel, T. et al. (2016) Nuclear DNA content variation within the genus Daucus (Apiaceae) determined by flow cytometry. Scientia Horticulturae, 209, 132–138.
Obermayer, R., Leitch, I.J., Hanson, L. & Bennett, M.D. (2002) Nuclear DNA C‐values in 30 species double the familial representation in pteridophytes. Annals of Botany, 90, 209–217.
Ohri, D., Fritsch, R.M. & Hanelt, P. (1998) Evolution of genome size in Allium (Alliaceae). Oesterreichische botanische Zeitschrift, 210, 57–86.
O'Keefe, R.T., Henderson, S.C. & Spector, D.L. (1992) Dynamic organization of DNA replication in mammalian cell nuclei: spatially and temporally defined replication of chromosome‐specific alpha‐satellite DNA sequences. The Journal of Cell Biology, 116, 1095–1110.
Olszewska, M.J. & Osiecka, R. (1983) The relationship between 2 C DNA content, life cycle type, systematic position and the dynamics of DNA endoreplication in parenchyma nuclei during growth and differentiation of roots in some dicotyledonous herbaceous species. Biochemie und Physiologie der Pflanzen, 178, 581–599.
Orooji, F., Mirzaghaderi, G., Kuo, Y.‐T. & Fuchs, J. (2022) Variation in the number and position of rDNA loci contributes to the diversification and speciation in Nigella (Ranunculaceae). Frontiers in Plant Science, 13, 917310.
Pellicer, J., Fay, M.F. & Leitch, I.J. (2010) The largest eukaryotic genome of them all? Botanical Journal of the Linnean Society, 164, 10–15.
Pellicer, J. & Leitch, I.J. (2020) The Plant DNA C‐values database (release 7.1): an updated online repository of plant genome size data for comparative studies. New Phytologist, 226, 301–305.
Pustahija, F., Brown, S.C., Bogunić, F., Bašić, N., Muratović, E., Ollier, S. et al. (2013) Small genomes dominate in plants growing on serpentine soils in West Balkans, an exhaustive study of 8 habitats covering 308 taxa. Plant and Soil, 373, 427–453.
Ramachandran, C. & Narayan, R.K. (1985) Chromosomal DNA variation in Cucumis. Theoretical and Applied Genetics, 69, 497–502.
Redi, C.A. & Capanna, E. (2012) Genome size evolution: sizing mammalian genomes. Cytogenetic and Genome Research, 137, 97–112.
Rees, H., Cameron, F.M., Hazarika, M.H. & Jones, G.H. (1966) Nuclear variation between diploid angiosperms. Nature, 211, 828–830.
Sanchez, P.L., Costich, D.E., Friebe, B., Coffelt, T.A., Jenks, M.A. & Gore, M.A. (2014) Genome size variation in guayule and mariola: fundamental descriptors for polyploid plant taxa. Industrial Crops and Products, 54, 1–5.
Schmuths, H., Meister, A., Horres, R. & Bachmann, K. (2004) Genome size variation among accessions of Arabidopsis thaliana. Annals of Botany, 93, 317–321.
Schubert, V., Berr, A. & Meister, A. (2012) Interphase chromatin organisation in Arabidopsis nuclei: constraints versus randomness. Chromosoma, 121, 369–387.
Sheval, E.V. (2018) Analysis of сhromosome сondensation/decondensation during mitosis by EdU incorporation in Nigella damascena L. seedling roots. Bio‐Protocol, 8, e2726.
Shinke, N. (1930) On the spiral structure of chromosomes in some higher plants. Memoirs of the College of Science, Kyoto Imperial University. Series B, 5, 239–245.
Solovei, I., Kreysing, M., Lanctôt, C., Kösem, S., Peichl, L., Cremer, T. et al. (2009) Nuclear architecture of rod photoreceptor cells adapts to vision in mammalian evolution. Cell, 137, 356–368.
Solovei, I., Thanisch, K. & Feodorova, Y. (2016) How to rule the nucleus: divide et impera. Current Opinion in Cell Biology, 40, 47–59.
Sorokin, D.V., Arifulin, E.A., Vassetzky, Y.S. & Sheval, E.V. (2020) Live‐cell imaging and analysis of nuclear body mobility. Methods in Molecular Biology, 2175, 1–9.
Sorokin, D.V., Peterlik, I., Tektonidis, M., Rohr, K. & Matula, P. (2018) Non‐rigid contour‐based registration of cell nuclei in 2‐D live cell microscopy images using a dynamic elasticity model. IEEE Transactions on Medical Imaging, 37, 173–184.
Sparvoli, E., Gay, H. & Kaufmann, B.P. (1965) Number and pattern of association of chromonemata in the chromosomes of Tradescantia. Chromosoma, 16, 415–435.
Temsch, E.M., Greilhuber, J., Hammett, K.R.W. & Murray, B.G. (2008) Genome size in Dahlia Cav. (Asteraceae–Coreopsideae). Plant Systematics and Evolution, 276, 157–166.
van de Peer, Y., Mizrachi, E. & Marchal, K. (2017) The evolutionary significance of polyploidy. Nature Reviews Genetics, 18, 411–424.
van Steensel, B. & Belmont, A.S. (2017) Lamina‐associated domains: links with chromosome architecture, heterochromatin, and gene repression. Cell, 169, 780–791.
Vejdovsky, F. (1912) Zum Problem der Vererbungsträger. Prag: Verlag der Königlich Böhmischen Gesellschaft der Wissenschaften, p. 184.
Weisshart, K., Fuchs, J. & Schubert, V. (2016) Structured illumination microscopy (SIM) and photoactivated localization microscopy (PALM) to analyze the abundance and distribution of RNA polymerase II molecules on flow‐sorted Arabidopsis nuclei. Bio‐Protocol, 6, e1725.
Zhang, X., Pandey, M.K., Wang, J., Zhao, K., Ma, X., Li, Z. et al. (2021) Chromatin spatial organization of wild type and mutant peanuts reveals high‐resolution genomic architecture and interaction alterations. Genome Biology, 22, 315.
Zonneveld, B.J.M., Leitch, I.J. & Bennett, M.D. (2005) First nuclear DNA amounts in more than 300 Angiosperms. Annals of Botany, 96, 229–244.

Schu 762/12-1 Deutsche Forschungsgemeinschaft; 20-54-12016 Russian Foundation for Basic Research

Keywords: Nigella damascena L.; chromatin; chromonema; genome size; replication; super‐resolution microscopy; transmission electron microscopy

0 (Heterochromatin)
0 (DNA, Plant)

Date Created: 20241021 Date Completed: 20241118 Latest Revision: 20241118

20241118

10.1111/tpj.17063

39432689