Skip to main content
SpringerLink
Log in

H3Ser10 histone phosphorylation in plant cell division

  • Published:
Russian Journal of Genetics: Applied Research

Abstract

Histones, the main protein components of the chromatin, are exposed to posttranslational modifications that influence on peculiarities of structural and functional organization of the chromosomes. Phosphorylation, methylation, acetylation, and ubiquitination are the most spread posttranslational modifications. Phosphorylation of histones mainly happens on N-terminal domains of serines (Ser) and threonines (Thr) and is involved in regulation of different processes in mitotic and meiotic divisions. To date, it was demonstrated that this type of modification is required for the activation of transcription, repair of DNA breaks, and recombination, as well as for the condensation and divergence of chromosomes. Among the four main histones, the presence of a larger number of modification sites is typical for the H3 histone. In plants, H3 histone phosphorylation at serine in positions 10 and 28 and at threonine in positions 3, 11, 32, and 133 are the most well studied. The data known to date on the spatiotemporal distribution of H3 phosphorylation at serine in position 10 (phH3Ser10) in the mitosis and meiosis of different plant species are collected in the review. For most species, phosphorylation of only pericentromeric regions in mitosis and the second division of meiosis and along the entire length of the chromosomes in the first meiotic division is typical. However, there are exceptions in the phH3Ser10 distribution in mosses and in the Cestrum genus, as well as in species with holocentric chromosomes. Controversial data on the phH3Ser10 distribution in mitosis and meiosis in the same species are found. The functional significance of phH3Ser10 in the cellular division in plants is associated with the activity of the centromere, the cohesion of the centromeres and sister chromatids, and chromosome segregation. The involvement of candidates of kinases and phosphatases known to date in the dynamics of H3Ser10 phosphorylation is discussed. The review provides an overview of the role of phH3Ser10 modifications in the chromosome division and segregation in mitosis and meiosis.

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

References

  • Bíró, J., Farkas, I., Domoki, M., Ötvös, K., Bottka, S., Dombrádi, V., and Fehér, A., The histone phosphatase inhibitory property of plant nucleosome assembly proteinrelated proteins (NRPs), Plant Physiol. Biochem., 2012, vol. 52, pp. 162–168. doi 10.1016/j.plaphy.2011.12.010

    Article  PubMed  Google Scholar 

  • Brasileiro-Vidal, A.C., Brammer, S., Puertas, M.J., Zanatta, A.C., Prestes, A., Moraes-Fernandes, M.I.B., and Guerra, M., Mitotic instability in wheat × Thinopyrum ponticum derivatives revealed by chromosome counting, nuclear DNA content and histone H3 phosphorylation pattern, Plant Cell Rep., 2005, vol. 24, pp. 172–178. doi 10.1007/s00299-005-0913-4

    Article  CAS  PubMed  Google Scholar 

  • Cai, X., Dong, F., Edelmann, R.E., and Makaroff, C.A., The Arabidopsis SYN1 cohesin protein is required for sister chromatid arm cohesion and homologous chromosome pairing, J. Cell Sci., 2003, vol. 116, no. 14, pp. 2999–3007. doi 10.1242/jcs.00601

    Article  CAS  PubMed  Google Scholar 

  • Caperta, A.D., Rosa, M., Delgado, M., Karimi, R., Demidov, D., Viegas, W., and Houben, A., Distribution patterns of phosphorylated Thr 3 and Thr 32 of histone H3 in plant mitosis and meiosis, Cytogenet. Genome Res., 2008, vol. 122, pp. 73–79. doi 10.1159/000151319

    Article  CAS  PubMed  Google Scholar 

  • Cobb, J., Miyaike, M., Kikuchi, A., and Handel, M.A., Meiotic events at the centromeric heterochromatin: Histone H3 phosphorylation, topoisomerase IIa localization and chromosome condensation, Chromosoma, 1999, vol. 108, pp. 412–425. doi 10.1007/s004120050393

    Article  CAS  PubMed  Google Scholar 

  • Demidov, D., VanDamme, D., Geelen, D., Blattner, F.R., and Houben, A., Identification and dynamics of two classes of Aurora-like kinases in Arabidopsis and other plants, Plant Cell, 2005, vol. 17, pp. 836–848. doi 10.1105/ tpc.104.029710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Demidov, D., Schubert, V., Kumke, K., Weiss, O., Karimi-Ashtiyani, R., Buttlar, J., Heckmann, S., Wanner, G., Dong, Q., Han, F., and Houben, A., Antiphosphorylated histone H2AThr120: A universal microscopic marker for centromeric chromatin of mono- and holocentric plant species, Cytogenet. Genome Res., 2014, vol. 143, pp. 150–156. doi 10.1159/000360018

    Article  CAS  PubMed  Google Scholar 

  • Dong, Q. and Han, F., Phosphorylation of histone H2A is associated with centromere function and maintenance in meiosis, Plant J., 2012, vol. 71, pp. 800–809. doi 10.1111/j.1365-313X.2012.05029.x

    Article  CAS  PubMed  Google Scholar 

  • Feitoza, L. and Guerra, M., Different types of plant chromatin associated with modified histones H3 and H4 and methylated DNA, Genetics, 2011, vol. 139, pp. 305–314. doi 10.1007/s10709-011-9550-8

    CAS  Google Scholar 

  • Fernandes, T., Yuyama, P.M., Moraes, A.P., and Vanzela, A.L., An uncommon H3/Ser10 phosphorylation pattern in Cestrum strigilatum (Solanaceae), a species with B chromosomes, Genome, 2008, vol. 51, no. 9, pp. 772–777. doi 10.1139/G08-042

    CAS  PubMed  Google Scholar 

  • Fuchs, J., Demidov, D., Houben, A., and Schubert, I., Chromosomal histone modification patterns–from conservation to diversity, Trends Plant Sci., 2006, vol. 11, no. 4, pp. 199–208. doi 10.1016/j.tplants.2006.02.008

    Article  CAS  PubMed  Google Scholar 

  • Gao, Z., Fu, S., Dong, Q., Han, F., and Birchler, J.A., Inactivation of a centromere during the formation of a translocation in maize, Chromosome Res., 2011, vol. 19, pp. 755–761. doi 10.1007/s10577-011-9240-5

    Article  CAS  PubMed  Google Scholar 

  • Gernand, D., Demidov, D., and Houben, A., The temporal and spatial pattern of histone H3 phosphorylation at serine 28 and serine 10 is similar in plants but differs between mono- and polycentric chromosomes, Cytogenet. Genome Res., 2003, vol. 101, pp. 172–176. doi 10.1159/000074175

    Article  CAS  PubMed  Google Scholar 

  • Guerra, M., Brasileiro-Vidal, A.C., Arana, P., and Puertas, M.J., Mitotic microtubule development and histone H3 phosphorylation in the holocentric chromosomes of Rhynchospora tenuis (Cyperaceae), Genetics, 2006, vol. 126, pp. 33–41. doi 10.1007/s10709-005-1430-7

    CAS  Google Scholar 

  • Guo, X.W., Th’ng, J.R.H., Swank, R.A., Anderson, H.J., Tudan, C., Bradbury, E.M., and Roberge, M., Chromosome condensation induced by fostriecin does not require p34CdC2 kinase activity and histone H1 hyperphosphorylation, but is associated with enhanced histone H2A and H3 phosphorylation, EMBO J., 1995, vol. 14, no. 5, pp. 976–985.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Han, F., Lamb, J.C., and Birchler, J.A., High frequency of centromere inactivation resulting in stable dicentric chromosomes of maize, Proc. Natl. Acad. Sci. U.S.A., 2006, vol. 103, pp. 3238–3243. doi 10.1073/pnas.0509650103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han, F., Gao, Z., and Birchler, J.A., Reactivation of an inactive centromere reveals epigenetic and structural components for centromere specification in maize, Plant Cell, 2009, vol. 21, pp. 1929–1939. doi 10.1105/tpc.109.066662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hendzel, M.J., Wei, Y., Mancini, M.A., Van Hooser, A., Ranalli, T., Brinkley, B.R., Bazett-Jones, D.P., and Allis, C.D., Mitosis specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation, Chromosoma, 1997, vol. 106, pp. 348–360. doi 10.1007/s004120050256

    Article  CAS  PubMed  Google Scholar 

  • Houben, A., Wako, T., Furushima-Shimogawara, R., Presting, G., Kunzel, G., Schubert, I., and Fukui, K., Short communication: The cell cycle dependent phosphorylation of histone H3 is correlated with the condensation of plant mitotic chromosomes, Plant J., 1999, vol. 18, pp. 675–679.

    Article  CAS  PubMed  Google Scholar 

  • Houben, A., Demidov, D., Ruttena, T., and Scheidtmann, K.H., Novel phosphorylation of histone H3 at threonine 11 that temporally correlates with condensation of mitotic and meiotic chromosomes in plant cells, Cytogenet Genome Res., 2005, vol. 109, pp. 148–155. doi 10.1159/000082394

    Article  CAS  PubMed  Google Scholar 

  • Houben, A., Demidov, D., Caperta, A.D., Karimi, R., Agueci, F., and Vlasenko, L., Phosphorylation of histone H3 in plants—A dynamic affair, Bioch. Biophys. Acta, 2007, vol. 1769, pp. 308–315. doi 10.1016/j.bbaexp.2007.01.002

    CAS  Google Scholar 

  • Ito, T., Role of histone modification in chromatin dynamics, J. Biochem., 2007, vol. 141, pp. 609–614. doi 10.1093/jb/mvm091

    Article  CAS  PubMed  Google Scholar 

  • Kaszas, E. and Cande, W.Z., Phosphorylation of histone H3 is correlated with changes in the maintenance of sister chromatid cohesion during meiosis in maize, rather than the condensation of the chromatin, J. Cell Sci., 2000, vol. 113, pp. 3217–3226.

    CAS  PubMed  Google Scholar 

  • Kawabe, A., Matsunaga, S., Nakagawa, K., Kurihara, D., Yoneda, A., Hasezawa, S., Uchiyama, S., and Fukui, K., Characterization of plant Aurora kinases during mitosis, Plant. Mol. Biol., 2005, vol. 58, pp. 1–13. doi 10.1007/s11103-005- 3454-x

    Article  CAS  PubMed  Google Scholar 

  • Kurihara, D., Matsunaga, S., Kawabe, A., Fujimoto, S., Noda, M., Uchiyama, S., and Fukui, K., Aurora kinase is required for chromosome segregation in tobacco BY-2 cells, Plant J., 2006, vol. 48, pp. 572–580. doi 10.1111/j.1365- 313X.2006.02893.x

    Article  CAS  PubMed  Google Scholar 

  • Kurihara, D., Matsunaga, S., Omura, T., Higashiyama, T., and Fukui, K., Identification and characterization of plant haspin kinase as a histone H3 threonine kinase, BMC Plant Biol. Database, 2011. doi 10.1186/1471-2229-11-73

    Google Scholar 

  • Li, Y., Butenko, Y., and Grafi, G., Histone deacetylation is required for progression through mitosis in tobacco cells, Plant J., 2005, vol. 41, pp. 346–352. doi 10.1111/j.1365-313X.2004.02301.x

    Article  CAS  PubMed  Google Scholar 

  • Manzanero, S., Rutten, T., Kotseruba, V., and Houben, A., Alterations in the distribution of histone H3 phosphorylation in mitotic plant chromosomes in response to cold treatment and the protein phosphatase inhibitor cantharidin, Chromosome Res., 2002, vol. 10, pp. 467–476. doi 10.1023/A:1020940313841

    Article  CAS  PubMed  Google Scholar 

  • Manzanero, S., Arana, P., Puertas, M.J., and Houben, A., The chromosomal distribution of phosphorylated histone H3 differs between plants and animals at meiosis, Chromosoma, 2000, vol. 109, pp. 308–317. doi 10.1007/s004120000087

    Article  CAS  PubMed  Google Scholar 

  • Marcon-Tavares, A.B., Felinto, F., Feitoza, L., Barrose Silva, A.E., and Guerra, M., Different patterns of chromosomal histone H3 phosphorylation in land plants, Cytogenet. Genome Res., 2014, vol. 143, pp. 136–143. doi 10.1159/000364815

    Article  CAS  PubMed  Google Scholar 

  • Oliver, C., Pradillo, M., Corredor, E., and Cunado, N., The dynamics of histone H3 modifications is species-specific in plant meiosis, Planta, 2013, vol. 238, pp. 23–33. doi 10.1007/s00425-013-1885-1

    Article  CAS  PubMed  Google Scholar 

  • Paula, C.M.P. and Techio, V.H., Souza Sobrinho, F., and Freitas, A.S., Distribution pattern of histone H3 phosphorylation at serine 10 during mitosis and meiosis in Brachiaria species, J. Genet., 2013, vol. 92, no. 2, pp. 259–266. doi 10.1007/s12041-013-0261-z

    Article  CAS  PubMed  Google Scholar 

  • Pedrosa, A., Jantsch, M.F., Moscone, E.A., Ambros, P.F., and Schweizer, D., Characterisation of pericentromeric and sticky intercalary heterochromatin in Ornithogalum longibracteatum (Hyacinthaceae), Chromosoma, 2001, vol. 110, pp. 203–213. doi 10.1007/s004120000125

    Article  CAS  PubMed  Google Scholar 

  • Schroeder-Reiter, E., Houben, A., and Wanner, G., Immunogold labeling of chromosomes for scanning electron microscopy: A closer look at phosphorylated histone H3 in mitotic metaphase chromosomes of Hordeum vulgare, Chromosome Res., 2003, vol. 11, pp. 585–596. doi 10.1023/A:1024952801846

    Article  CAS  PubMed  Google Scholar 

  • Sveshnikov, P.G., Malaitsev, V.V., Bogdanova, I.M., and Solopova, O.N., Vvedenie v molekulyarnuyu immunologiyu i gibridomnuyu tekhnologiyu (Introduction to Molecular Immunology and Hybrid Technology), Moscow: MGU, 2006.

    Google Scholar 

  • Wallace, W., Schaefer, L.H., and Swedlow, J.R., Artifacts and Aberrations in Deconvolution Analysis, Olympus Microscopy Resource Center, 2012. http://www.olympusmicro.com/primer/digitalimaging/deconvolution/deconartifacts.html.

    Google Scholar 

  • Wang, W., Tang, D., Luo, Q., Jin, Y., Shen, Y., Wang, K., and Cheng, Z., BRK1, a Bub1-related kinase, is essential for generating proper tension between homologous kinetochores at metaphase I of rice meiosis, Plant Cell, 2012, vol. 24, pp. 4961–4973. doi 10.1105/tpc.112.105874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, F. and Higgins, J.M.G., Histone modifications and mitosis: Countermarks, landmarks, and bookmarks, Trends Cell Biol., 2013, vol. 23, no. 4, pp. 175–184. doi 10.1016/j.tcb.2012.11.005

    Article  CAS  PubMed  Google Scholar 

  • Wei, Y., Mizzen, C.A., Cook, R.G., Gorovsky, M.A., and Allis, D.C.D., Phosphorylation of histone H3 at serine 10 is correlated with chromosome condensation during mitosis and meiosis in Tetrahymena, Proc. Natl. Acad. Sci. U.S.A., 1998, vol. 95, pp. 7480–7484.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei, Y., Yu, L., Bowen, J., Gorovsky, M.A., and Allis, C.D., Phosphorylation of histone H3 is required for proper chromosome condensation and segregation, Cell, 1999, vol. 97, pp. 99–109. doi 10.1016/S0092-8674(00)80718-7

    Article  CAS  PubMed  Google Scholar 

  • Zhang, B., Lv, Z., Pang, J., Liu, Y., Guo, X., Fu, S., Li, J., Dong, Q., Wu, H.-J., Gao, Z., Wang, X.-J., and Hana, F., Formation of a functional maize centromere after loss of centromeric sequences and gain of ectopic sequences, Plant Cell, 2013, vol. 25, pp. 1979–1989. doi 10.1105/tpc.113.110015

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang, B., Dong, Q., Su, H., Birchler, J.A., and Han, F., Histone phosphorylation: Its role during cell cycle and centromere identity in plants, Cytogenet. Genome Res., 2014, vol. 143, pp. 144–149. doi doi 10.1159/000360435

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Federal Research Center Institute of Cytology and Genetics, Siberian Branch, Russian Academy of Sciences, Novosibirsk, Russia

    D. B. Loginova & O. G. Silkova

Authors
  1. D. B. Loginova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. O. G. Silkova
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. B. Loginova.

Additional information

Original Russian Text © D.B. Loginova, O.G. Silkova, 2016, published in Vavilovskii Zhurnal Genetiki i Selektsii, 2016, Vol. 20, No. 1, pp. 87–95.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Loginova, D.B., Silkova, O.G. H3Ser10 histone phosphorylation in plant cell division. Russ J Genet Appl Res 7, 46–56 (2017). https://doi.org/10.1134/S2079059717010087

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S2079059717010087

Keywords

Search

Navigation