Nuclear organization in crucifer genomes: nucleolus-associated telomere clustering is not a universal interphase configuration in Brassicaceae
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
34390055
DOI
10.1111/tpj.15459
Knihovny.cz E-zdroje
- Klíčová slova
- Arabidopsis thaliana, Crucifereae, Rabl, centromere, chromocenter-loop model, interphase, nucleolus, telomere,
- MeSH
- Arabidopsis genetika MeSH
- Arabis genetika MeSH
- Brassicaceae genetika MeSH
- buněčné jadérko genetika MeSH
- centromera genetika MeSH
- chromatin genetika MeSH
- délka genomu MeSH
- fylogeneze MeSH
- genom rostlinný * MeSH
- heterochromatin genetika MeSH
- hybridizace in situ fluorescenční MeSH
- interfáze MeSH
- ribozomální DNA genetika MeSH
- telomery genetika MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- chromatin MeSH
- heterochromatin MeSH
- ribozomální DNA MeSH
Arabidopsis thaliana has become a major plant research model, where interphase nuclear organization exhibits unique features, including nucleolus-associated telomere clustering. The chromocenter (CC)-loop model, or rosette-like configuration, describes intranuclear chromatin organization in Arabidopsis as megabase-long loops anchored in, and emanating from, peripherally positioned CCs, with those containing telomeres associating with the nucleolus. To investigate whether the CC-loop organization is universal across the mustard family (crucifers), the nuclear distributions of centromeres, telomeres and nucleoli were analyzed by fluorescence in situ hybridization in seven diploid species (2n = 10-16) representing major crucifer clades with an up to 26-fold variation in genome size (160-4260 Mb). Nucleolus-associated telomere clustering was confirmed in Arabidopsis (157 Mb) and was newly identified as the major nuclear phenotype in other species with a small genome (215-381 Mb). In large-genome species (2611-4264 Mb), centromeres and telomeres adopted a Rabl-like configuration or dispersed distribution in the nuclear interior; telomeres only rarely associated with the nucleolus. In Arabis cypria (381 Mb) and Bunias orientalis (2611 Mb), tissue-specific patterns deviating from the major nuclear phenotypes were observed in anther and stem tissues, respectively. The rosette-like configuration, including nucleolus-associated telomere clustering in small-genome species from different infrafamiliar clades, suggests that genomic properties rather than phylogenetic position determine the interphase nuclear organization. Our data suggest that nuclear genome size, average chromosome size and degree of longitudinal chromosome compartmentalization affect interphase chromosome organization in crucifer genomes.
Zobrazit více v PubMed
Armstrong, S.J., Franklin, F.C.H. & Jones, G.H. (2001) Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. Journal of Cell Science, 114, 4207-4217.
Bennett, M.D., Leitch, I.J., Price, H.J. & Johnston, J.S. (2003) Comparisons with Caenorhabditis (approximately 100 Mb) and Drosophila (approximately 175 Mb) using flow cytometry show genome size in Arabidopsis to be approximately 157 Mb and thus approximately 25% larger than the Arabidopsis genome initiative estimate of approximately 125 Mb. Annals of Botany, 91, 547-557.
Berr, A., Pecinka, A., Meister, A., Kreth, G., Fuchs, J., Blattner, F.R. et al. (2006) Chromosome arrangement and nuclear architecture but not centromeric sequences are conserved between Arabidopsis thaliana and Arabidopsis lyrata. The Plant Journal, 48, 771-783.
Bi, X., Cheng, Y.J., Hu, B., Ma, X., Wu, R., Wang, J.W. et al. (2017) Nonrandom domain organization of the Arabidopsis genome at the nuclear periphery. Genome Research, 27, 1162-1173.
Cerqueira, A.V. & Lemos, B. (2019) Ribosomal DNA and the nucleolus as keystones of nuclear architecture, organization, and function. Trends in Genetics, 35, 710-723.
Doğan, E.S. & Liu, C. (2018) Three-dimensional chromatin packing and positioning of plant genomes. Nat. Plants, 4, 521-529.
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.
Dong, P., Tu, X., Liang, Z., Kang, B.H. & Zhong, S. (2020) Plant and animal chromatin three-dimensional organization: similar structures but different functions. Journal of Experimental Botany, 71, 5119-5128.
Edger, P.P., Hall, J.C., Harkess, A., Tang, M., Coombs, J., Mohammadin, S. et al. (2018) Brassicales phylogeny inferred from 72 plastid genes: A reanalysis of the phylogenetic localization of two paleopolyploid events and origin of novel chemical defenses. American Journal of Botany, 105, 463-469.
Evans, D.E., Mermet, S. & Tatout, C. (2020) Advancing knowledge of the plant nuclear periphery and its application for crop science. Nucleus, 11, 347-363.
Fang, Y. & Spector, D.L. (2005) Centromere positioning and dynamics in living Arabidopsis plants. Molecular Biology of the Cell, 16, 5710-5718.
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.
Fujimoto, S., Ito, M., Matsunaga, S. & Fukui, K. (2005) An upper limit of the ratio of DNA volume to nuclear volume exists in plants. Genes & Genetic Systems, 80, 345-350.
Grob, S., Schmid, M.W., Luedtke, N.W., Wicker, T. & Grossniklaus, U. (2013) Characterization of chromosomal architecture in Arabidopsis by chromosome conformation capture. Genome Biology, 14, R129.
Hloušková, P., Mandáková, T., Pouch, M., Trávníček, P. & Lysak, M.A. (2019) The large genome size variation in the Hesperis clade was shaped by the prevalent proliferation of DNA repeats and rarer genome downsizing. Annals of Botany, 124, 103-120.
Hoencamp, C., Dudchenko, O., Elbatsh, A.M.O., Brahmachari, S., Raaijmakers, J.A., van Schaik, T. et al. (2021) 3D genomics across the tree of life reveals condensin II as a determinant of architecture type. Science, 372, 984-989.
Houben, A., Demidov, D., Gernand, D., Meister, A., Leach, C.R. & Schubert, I. (2003) Methylation of histone H3 in euchromatin of plant chromosomes depends on basic nuclear DNA content. The Plant Journal, 33, 967-973.
Howe, E.S., Murphy, S.P. & Bass, H.W. (2013) Three-dimensional acrylamide fluorescence in situ hybridization for plant cells. Methods in Molecular Biology, 990, 53-66.
Hu, B., Wang, N., Bi, X., Karaaslan, E.S., Weber, A.L., Zhu, W. et al. (2019) Plant lamin-like proteins mediate chromatin tethering at the nuclear periphery. Genome Biology, 20, 1-18.
Huang, Y., Rodriguez-Granados, N.Y., Latrasse, D., Raynaud, C., Benhamed, M. & Ramirez-Prado, J.S. (2020) The matrix revolutions: towards the decoding of the plant chromatin three-dimensional reality. Journal of Experimental Botany, 71, 5129-5147.
Hurel, A., Phillips, D., Vrielynck, N., Mézard, C., Grelon, M. & Christophorou, N. (2018) A cytological approach to studying meiotic recombination and chromosome dynamics in Arabidopsis thaliana male meiocytes in three dimensions. The Plant Journal, 95, 385-396.
Idziak, D., Robaszkiewicz, E. & Hasterok, R. (2015) Spatial distribution of centromeres and telomeres at interphase varies among Brachypodium species. Journal of Experimental Botany, 66, 6623-6634.
Ijdo, J.W., Wells, R.A., Baldini, A. & Reeders, S.T. (1991) Improved telomere detection using a telomere repeat probe (TTAGGG)n generated by PCR. Nucleic Acids Research, 19, 4780.
Laibach, F. (1907) Zur Frage nach der Individualität der Chromosomen im Pflanzenreich. Beih. Botan. Zentralbl., 22, 191-210.
Lysak, M.A. (2018) Brassicales: an update on chromosomal evolution and ancient polyploidy. Plant Systematics and Evolution, 304, 757-762.
Lysak, M.A., Koch, M.A., Beaulieu, J.M., Meister, A. & Leitch, I.J. (2009) The dynamic ups and downs of genome size evolution in Brassicaceae. Molecular Biology and Evolution, 26, 85-98.
Mandáková, T., Hloušková, P., German, D.A. & Lysak, M.A. (2017) Monophyletic origin and evolution of the largest crucifer genomes. Plant Physiology, 174, 2062-2071.
Mandáková, T., Hlousková, P., Koch, M.A. & Lysak, M.A. (2020) Genome evolution in Arabideae was marked by frequent centromere repositioning. The Plant Cell, 32, 650-665.
Mandáková, T., Kovařík, A., Zozomová-Lihová, J., Shimizu-Inatsugi, R., Shimizu, K.K., Mummenhoff, K. et al. (2013) The more the merrier: recent hybridization and polyploidy in Cardamine. The Plant Cell, 25, 3280-3295.
Mandáková, T. & Lysak, M.A. (2016a) Chromosome preparation for cytogenetic analyses in Arabidopsis. Current Protocols in Plant Biology, 1, 43-51.
Mandáková, T. & Lysak, M.A. (2016b) Painting of Arabidopsis chromosomes with chromosome-specific BAC clones. Current Protocols in Plant Biology, 1, 359-371.
Nagaki, K., Talbert, P.B., Zhong, C.X., Dawe, R.K., 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.
Nikolov, L.A., Shushkov, P., Nevado, B., Gan, X., Al-Shehbaz, I.A. et al. (2019) Resolving the backbone of the Brassicaceae phylogeny for investigating trait diversity. New Phytologist, 222, 1638-1651.
Novák, P., Neumann, P., Pech, J., Steinhaisl, J. & Macas, J. (2013) RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics, 29, 792-793.
Novák, P., Robledillo, L.Á., Koblížková, A., Vrbová, I., Neumann, P. & Macas, J. (2017) TAREAN: a computational tool for identification and characterization of satellite DNA from unassembled short reads. Nucleic Acids Research, 45, e111.
Oko, Y., Ito, N. & Sakamoto, T. (2020) The mechanisms and significance of the positional control of centromeres and telomeres in plants. Journal of Plant Research, 133, 471-478.
Pecinka, A., Schubert, V., Meister, A., Kreth, G., Klatte, M., Lysak, M.A. et al. (2004) Chromosome territory arrangement and homologous pairing in nuclei of Arabidopsis thaliana are predominantly random except for NOR-bearing chromosomes. Chromosoma, 113, 258-269.
Pontvianne, F., Carpentier, M.C., Durut, N., Pavlištová, V., Jaške, K., Schořová, Š. et al. (2016) 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.
Pontvianne, F. & Grob, S. (2020) Three-dimensional nuclear organization in Arabidopsis thaliana. Journal of Plant Research, 133, 479-488.
Poulet, A., Duc, C., Voisin, M., Desset, S., Tutois, S., Vanrobays, E. et al. (2017) The LINC complex contributes to heterochromatin organisation and transcriptional gene silencing in plants. Journal of Cell Science, 130, 590-601.
Prieto, P., Santos, A.P., Moore, G. & Shaw, P. (2004) Chromosomes associate premeiotically and in xylem vessel cells via their telomeres and centromeres in diploid rice (Oryza sativa). Chromosoma, 112, 300-307.
Rabl, C. (1885) Uber Zelltheilung. Morphologisches Jahrbuch, 10, 214-330.
Roberts, N.Y., Osman, K. & Armstrong, S.J. (2009) Telomere distribution and dynamics in somatic and meiotic nuclei of Arabidopsis thaliana. Cytogenetic and Genome Research, 124, 193-201.
Schubert, I. & Shaw, P. (2011) Organization and dynamics of plant interphase chromosomes. Trends in Plant Science, 16, 273-281.
Shu, H., Wildhaber, T., Siretskiy, A., Gruissem, W. & Hennig, L. (2012) Distinct modes of DNA accessibility in plant chromatin. Nature Communications, 3, 1281.
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.
Steinitz-Sears, L.M. (1963) Chromosome studies in Arabidopsis thaliana. Genetics, 48, 483-490.
Tiang, C.L., He, Y. & Pawlowski, W.P. (2012) Chromosome organization and dynamics during interphase, mitosis, and meiosis in plants. Plant Physiology, 158, 26-34.
Willing, E.M., Rawat, V., Mandáková, T. et al. (2015) Genome expansion of Arabis alpina linked with retrotransposition and reduced symmetric DNA methylation. Nature Plants, 1, 1-5.
Xie, T., Zhang, F.G., Zhang, H.Y., Wang, X.T., Hu, J.H. & Wu, X.M. (2019) Biased gene retention during diploidization in Brassica linked to three-dimensional genome organization. Nature Plants, 5, 822-832.
Zhou, S., Jiang, W., Zhao, Y. & Zhou, D.X. (2019) Single-cell three-dimensional genome structures of rice gametes and unicellular zygotes. Nature Plants, 5, 795-800.
Insight into chromatin compaction and spatial organization in rice interphase nuclei
Image analysis workflows to reveal the spatial organization of cell nuclei and chromosomes