Abstract
Reversible phosphorylation of proteins by kinases and phosphatases plays a key regulatory role in several eukaryotic cellular functions including the control of the division cycle. Increasing numbers of sequence and biochemical data show the involvement of cyclin-dependent kinases (CDKs) and cyclins in regulation of the cell cycle progression in higher plants. The complexity represented by different types of CDKs and cyclins in a single species such as alfalfa, indicates that multicomponent regulatory pathways control G2/M transition. A set of cdc2-related genes (cdc2Ms A, B, D and F) was expressed in G2 and M cells. Phosphorylation assays also revealed that at least three kinase complexes (Cdc2Ms A/B, D and F) were successively active in G2/M cells after synchronization. Interaction between alfalfa mitotic cyclin (Medsa; CycB2;l) and a kinase partner has been reported previously. The present yeast two-hybrid analyses showed differential interaction between defined D-type cyclins and Cdc2Ms kinases functioning in G2/M phases. Localization of Cdc2Ms F kinase to the preprophase band (PPB), the perinuclear ring in early prophase, the mitotic spindle and the phragmoplast indicated a pivotal role for this kinase in mitotic plant cells. So far limited research efforts have been devoted to the functions of phosphatases in the control of plant cell division. A homologue of dual phosphatase, cdc25, has not been cloned yet from alfalfa; however tyrosine phosphorylation was indicated in the case of Cdc2Ms A kinase and the p13suc1-bound kinase activity was increased by treatment of this complex with recombinant Drosophila Cdc25. The potential role of serine/threonine phosphatases can be concluded from inhibitor studies based on okadaic acid or endothall. Endothall elevated the kinase activity of pl3suc1-bound fractions in G2-phase alfalfa cells. These biochemical data are in accordance with observed cytological abnormalities. The present overview with selected original data outlines a conclusion that emphasizes the complexity of G2/M regulatory events in flowering plants.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Assaad, F.F., Mayer, U., Lukowitz, W. and Jürgens, G. 1997. Cytokinesis in somatic plant cells. Plant Physiol. Biochem. 35: 177–184.
Bögre, L., Zwerger, K., Meskiene, I., Binarova, P., Csizmadia, V., Planck, C., Wagner, E., Hirt, H. and Heberle-Bors, E. 1997. The cdc2Ms kinase is differently regulated in the cytoplasm and in the nucleus. Plant Physiol. 113: 841–852.
Burssens, S., Van Montagu, M. and Inzé, D. 1998. The cell cycle in Arabidopsis. Plant Physiol. Biochem. 36: 9–19.
Citterio, S., Sgorbati, S., Onelli, E., Gatti, M. and Piazza, E. 1997. Cyclin-dependent kinase-like proteins in pea nuclei: their presence and role in cell proliferation. Protoplasma 196: 34–44.
Cohen, P., Holmes, C.F.B. and Tsukitani, Y. 1990. Okadaic acid: a new probe for the study of cellular regulation. Trends Biochem. Sci. 15: 98–102.
Colosanti, J., Cho, S.O., Wick, S. and Sundaresan, V. 1993. Localization of the functional p34cdc2 homolog of maize in root tip and stomatal complex cells: association with predicted division sites. Plant Cell 5: 1101–1111.
Dahl, M., Meskiene, I., Bögre, L., Ha, D.T.C., Swoboda, I., Hubmann, R., Hirt, H. and Heberle-Bors, E. 1995. The D-type alfalfa cyclin gene cycMs-4 complements G1 phase of the cell cycle. Plant Cell 7: 1847–1857.
Davies, P.J. 1995. Plant Hormones: Physiology, Biochemistry and Molecular Biology, Kluwer Academic Publishers, Dordrecht, Netherlands.
De Veylder, L., Segers, G., Glab, N., Casteels, P., Van Montagu, M. and Inzé, D. 1997: The Arabidopsis CkslAt protein binds the cyclin-dependent kinases Cdc2aAt and Cdc2bAt. FEBS Lett. 412: 446–452.
Doerner, P., Jørgensen, J.-E., You, R., Steppuhn, J. and Lamb, C. 1996. Control of root growth and development by cyclin expression. Nature 380: 520–523.
Dombrádi, V. 1997. Comparative analysis of Ser/Thr protein phosphatases. Trends Comp. Biochem. Physiol. 3: 23–48.
Dudits, D., Magyar, Z, Deák, M., Mészáros, T., Miskolczi, P., Feher, A., Brown, S., Kondorosi, É., Athanasiadis, A., Pongor, S., Bakó, L., Koncz, Cs. and Györgyey, J. 1998. Cyclin-dependent and calcium-dependent kinase families: response of cell division cycle to hormone and stress signals. In: D. Francis, D. Dudits and D. Inzé (Eds.) Plant Cell Division, Portland Press, London, pp. 21–45.
Erdödi, B., Tóth, B., Hirano, K., Hirano, M., Hatshorne, D.J. and Gergely, P. 1995. Endothall thioanhydride inhibits protein phosphatases-1 and-2A in vivo. American Physiological Society C1176–C1184.
Ewen, M.E., Sluss, H.K., Sherr, C.J., Matsushime, H., Kato, J. and Livingstone, D.M. 1993. Functional interaction of the retinoblastoma protein with mammalian D-type cyclins. Cell 73: 487–497.
Felix, M.A., Cohen, P. and Karsenti, E. 1990. Cdc2 h1 kinase is negatively regulated by a type 2A phosphatase in the Xenopus early embryonic cell cycle: evidence from the effects of ocadaic acid. EMBO J. 9: 675–683.
Fisher, R.P. 1997. CDKs and cyclins in transition(s). Curr. Opin. Genet. Dev. 7: 32–38.
Hadwiger, J.A., Wittenberg, C., Mendenhall, M.D. and Reed, S.I. 1989. The Saccharomyces cerevisiae CKS1 gene, a homolog of the Schizosaccharomyces pombe sucl+ gene, encodes a subunit of the Cdc28 protein kinase complex. Mol. Cell Biol. 9: 2034–2041.
Harper, J.W. and Elledge, S.J. 1996. Cdk inhibitors in development and cancer. Curr. Opin. Genet. Dev. 6: 56–64.
Hayles, J., Beach, D., Kurkacz, B. and Nurse, P. 1986. The fission yeast cell cycle control gene cdc2: isolation of a sequence sucl that suppresses cdc2 mutant function. Mol. Gen. Genet. 202: 291–293.
Hindley, J. and Phear, G.A. 1984. Sequence of the cell division gene CDC2 from Schizosaccharomyces pombe: patterns of splicing and homology to protein kinases. Gene 31: 129–134.
Hirt, H., Mink, M., Pfosser, M., Bögre, L., Györgyey, J., Jonak, C., Gartner, A., Dudits, D. and Heberle-Bors, E. 1992. Alfalfa cyclins: differential expression during the cell cycle and in plant organs. Plant Cell 4: 1531–1538.
Hunter, T. 1995. Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signalling. Cell 80: 225–236.
James, P., Halladay, J. and Graig, E.A. 1996. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144: 1425–1436.
John, P.C.L., Zhang, K., Dong, C., Diederich, L. and Wightman, F. 1993. p34cdc2 related proteins in control of cell cycle progression: the switch between division and differentiation in tissue development and stimulation of division by auxin and cytokinin. Aust. J. Plant Physiol. 20: 503–526.
Kumagai, A. and Dunphy, W.G. 1992. Regulation of the cdc25 protein during the cell cycle in Xenopus extracts. Cell 70: 139–151.
Lees, E. 1995. Cyclin dependent kinase regulation. Curr. Opin. Cell Biol. 7: 773–780.
Lörincz, A.T. and Reed, S.I. 1984. Primary structure homology between the product of yeast cell division control gene CDC28 and vertebrate oncogenes. Nature 307: 183–185.
Magyar, Z., Bakó, L., Bögre, L., Dedeoglu, D., Kapros, T. and Dudits, D. 1993. Active cdc2 genes and cell cycle phase-specific cdc2-related kinase complexes in hormone-stimulated alfalfa cells. Plant J. 4: 151–161.
Magyar, Z., Mészáros, T., Miskolczi, P., Deák, M., Fehér, A., Brown, S., Kondorosi, É., Athanasiadis, A., Pongor, S., Bilgin, M., Bakó, L., Koncz, Cs. and Dudits, D. 1997. Cell cycle phase specificity of putative cyclin-dependent kinase variants in synchronized alfalfa cells. Plant Cell 9: 223–225.
McKibbin, R.S., Halford, N.G. and Francis, D. 1998. Expression of fission yeast cdc25 alters the frequency of lateral root formation in transgenic tobacco. Plant Mol. Biol. 36: 601–612.
Meskiene, I., Bögre, L., Dahl, M., Pirck, M., Ha, D.T.H., Swoboda, I., Heberle-Bors, E., Ammerer, G. and Hirt, H. 1995. cycMs3, a novel B-type alfalfa cyclin gene, is induced in the G0-to-G1 transition of the cell cycle. Plant Cell 7: 759–771.
Millward, T.A., Zolnierowicz, S. and Hemmings, B.A. 1999. Regulation of protein kinase cascades by protein phosphatase 2A. Trends Biochem. Sci. 24: 186–191.
Mironov, V., Van Montagu, M. and Inzé, D. 1999. Regulation of cell division in plants: an Arabidopsis perspective. Prog. Cell Cycle Res. 3:24–41.
Nakagami, H., Sekine, M., Murakami, H. and Shinmyo, A. 1999. Tobacco retinoblastoma-related protein phosphorylated by a distinct cyclin-dependent kinase complex with Cdc2/cyclin D in vitro. Plant J. 18: 243–252.
Neufeld, T.P., de la Cruz, A.F.A., Johnston, L.A. and Edgar, B.A. 1998. Coordination of growth and cell division in the Drosophila wing. Cell 93: 1183–1193.
Okayama, H., Nagata, A., Jinno, S., Murakami, H., Tanaka, K. and Nakashima, N. 1996. Cell cycle control in fission yeast and mammals: identification of new regulatory mechanisms. Adv. Cancer Res. 69: 17–62.
Osmani, S.A. and Ye, X.S. 1997. Targets of checkpoints controlling mitosis: lessons from lower eukaryotes. Trends Cell Biol. 7: 283–288.
Pines, J. 1995. Cyclins and cyclin-dependent kinases: a biochemical view. Biochem. J. 308: 697–711.
Renaudin, J.P., Doonan, J.H., Freeman, D., Hashimoto, J., Hirt, H., Inzé, D., Jacobs, T., Kouchi, H., Rouzé, P., Sauter, M., Savouré, A., Sorrell, D.A., Sundaresan, V. and Murray, J.A.H. 1996. Plant cyclins: a unified nomenclature for plant A-, B-and D-type cyclins based on sequence organization. Plant Mol. Biol. 32: 1003–1018.
Renaudin, J.P., Savouré, A., Philippe, H., Van Montagu, M., Inzé, D. and Rouzé, P. 1998. Characterization and classification of plant cyclin sequences related to A-and B-type cyclins. In: D. Francis, D. Dudits and D. Inzé (Eds.), Plant Cell Division, Portland Press, London, pp. 67–98.
Riou-Khamlichi, C., Huntley, R., Jacqmard, A. and Murray, J.A.H. 1999. Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283: 1541–1544.
Sabelli, P., Burgess, S.R., Kush, A.K. and Shewry, P.R. 1998. DNA replication initiation and mitosis induction in eukaryotes: the role of MCM and Cdc25. In: D. Francis, D. Dudits and D. Inzé (Eds.) Plant Cell Division, Portland Press, London, pp. 243–268.
Satterwhite, L.L., Lohka, M.H., Wilson, K.L., Scherson, T.Y., Cisek, L.J., Corden, J.L. and Pollard, T.D. 1992. Phosphorylation of myosin-II regulatory light-chain by cyclin-p34cdc2: a mechanism for the timing of cytokinesis. J. Cell Biol. 118: 595–605.
Savouré, A., Fehér, A., Kaló, P., Petrovics, G., Csanádi, G., Szécsi, J., Kiss, G., Brown, S., Kondorosi, Á and Kondorosi, É. 1995. Isolation of a full-length cyclin cDNA clone CycIIIMs from Medicago sativa: chromosomal mapping and expression. Plant Mol. Biol. 27: 1059–1070.
Segers, G., Gadisseur, I., Bergounioux, C., de Almeida, E.L., Jacqmard, A., Van Montagu, M. and Inzé, D. 1996. The Arabidopsis cyclin-dependent kinase gene cdc2bAt is preferentially expressed during S and G2 phases of the cell cycle. Plant J. 10: 601–612.
Shuster, C.B. and Burgess, D.R. 1999. Parameters that specify the timing of cytokinesis. J. Cell Biol. 146: 981–992.
Snaith, H.A., Armstrong, C.G., Guo, Y, Kaiser, K. and Cohen, P.T.W. 1996. Deficiency of protein phophatase 2A uncouples the nuclear and centrosome cycles and prevents attachments of microtubules to the kinetochore in Drosophila microtubule star (mts) embryos. J. Cell Sci. 109: 3001–3012.
Sorrell, D.A., Combettes, B., Chaubet-Gigot, N., Gigot, C. and Murray, J.A.H. 1999. Distinct cyclin D genes show mitotic accumulation or constant levels of transcripts in tobacco bright yellow-2 cells. Plant Physiol. 119: 343–351.
Vissi, E., Csordás Tóth, É., Kovács, I., Magyar, Z., Horváth, V.G., Bagossi, P., Gergely, P., Dudits, D. and Dombrádi, V. 1998. Protein phosphatase 1 catalytic subunit isoforms from alfalfa: biochemical characterization and cDNA cloning. Arch. Biochem. Biophys. 360: 206–214.
Wang, H., Qi, Q., Schorr, P., Cutler, A.J., Crosby, W.L. and Fowke, L.C. 1998. ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis thaliana interacts with both Cdc2a and Cyc2a and CycD3, and its expression is induced by abscisic acid. Plant J. 15:501–510.
Warburton, PE. and Earnshaw, W.C. 1997. Untangling the role of DNA topoisomerase II in mitotic chromosome structure and function. BioEssays 19: 97–99.
Yamaguchi, M., Umeda, M. and Uchimiya, H. 1998. A rice homolog of Cdk7/M015 phosphorylates both cyclin-dependent protein kinases and the carboxy-terminal domain of RNA polymerase II. Plant J. 16: 613–619.
Yamashita, K., Yasuda, H., Pines, J., Yasumoto, K., Nishitani, H., Ohtsubo, M., Hunter, T., Sugimura, T. and Nishimoto, T. 1990. Okadaic acid, a potent inhibitor of type 1 and type 2A protein phosphatases, activates cdc2/H1 kinase and transiently induces a premature mitosis-like state in BHK21 cells. EMBO J. 3: 4331–4338.
Yang, J. and Kornbluth, S. 1999. All board the cyclin train: subcellular trafficking of cyclins and their CDK partners. Trends Cell Biol. 9: 207–210.
Zhang, K., Tsukitani, Y and John, P.C.L. 1992. Mitotic arrest in tobacco caused by the phosphoprotein phosphatase inhibitor okadaic acid. Plant Cell Physiol. 33: 677–688.
Zhang, K., Letham, D.A. and John, P.C.L. 1996. Cytokinin controls the cell cycle at mitosis by stimulating the tyrosine dephosphorylation and activation of p34cdc2-like HI histone kinase. Planta 200: 2–12.
Zhang, K., Diederich, L., Sek, F.J., Larkin, P.J., Letham, D.S. and John, P.C.L. 1998. Cytokinin acts on cell division through Cdc25 phosphatase. Poster abstract, 16th International Conference on Plant Growth Substances, Makuhari Messe, Japan, 13–17 August.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2000 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
Mészáros, T. et al. (2000). Multiple cyclin-dependent kinase complexes and phosphatases control G2/M progression in alfalfa cells. In: Inzé, D. (eds) The Plant Cell Cycle. Springer, Dordrecht. https://doi.org/10.1007/978-94-010-0936-2_5
Download citation
DOI: https://doi.org/10.1007/978-94-010-0936-2_5
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-010-3798-3
Online ISBN: 978-94-010-0936-2
eBook Packages: Springer Book Archive