Abstract
The cell cycle is an important research field in cell biology and it is genetically and developmentally regulated in animals and plants. The aim of this study was to review knowledge about the biochemical regulation of the cell cycle by plant growth regulators through molecular checkpoints that regulate the transition from GO-G1-S-phase and G2-M in higher plants. Recent research has shown that zeatin treatment led to the up-regulation of CycD3 inArabidopsis. Benzyladenine treatment can also shorten the duration of S-phase through recruitment of latent origins of DNA replication. Kinetin is involved in the phosphoregulation of the G2-M checkpoint; the major cyclin-dependent kinase (Cdk) at this checkpoint has recently shown to be dephosphorylated as a result of cytokinin treatment, an effect that can also be mimicked by the fission yeast Cdc25 phosphatase. Gibberellic acid (GA) treatment induces internode elongation in deepwater rice, this response is mediated by a GA-induced up-regulation of a cyclin-Cdk at the G2-M checkpoint. Recent evidence has also linked abscisic acid to a cyclin-dependent kinase inhibitor. A new D-type cyclin, recently discovered inArabidopsis may have a key role in this process. A brief review on plant growth regulator-cell cycle interfacing during development and a cytokinin-induced continuum of cell cycle activation through the up-regulation of a plant D-type cyclin at the G1 checkpoint and the phosphoregulation of the Cdk at the G2/M checkpoint had been concluded. This review could be valuable to research on cell and developmental biology in plants.
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Ach, R.A., Durfee T., Miller, A.B., Zambryski, P.C. and Gruissem, W. 1997.RRB1 andRRB2 encode maize retinoblastoma-related proteins [J]. Mol. Cell Biol.,17: 5077–5086.
Berridge M.J. 1995. Calcium signalling and cell proliferation [J]. Bioessays17: 491–500.
Blakely, L.M., Durham, M., Evans, T.A. and Blakely, R.M. 1982. Experimental studies on lateral root formation in radish seedlings. I General methods developmental stages, and spontaneous formation of laterals [J]. Bot. Gaz.,143: 341–352.
Bleeker, A.B., Schuette, J.L. and Kende, H. 1986. Anatomical analysis of growth and developmental patterns of deepwater rice [J] Planta,169: 490–497.
Celenza, J.L., Grisafi, P.L. and Fink, G.R. 1995. A pathway for lateral root formation inArabidopsis thaliana [J]. Genes Dev.,9: 2131–2142
Dahi, 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 genecycMs4 complements G1 cyclin-deficient yeast and is induced in the G1 phase of the cell cycle [J]. Plant Cell,7: 1847–1857.
Daykin A., Scott, IM., Causton D.R. and Francis, D. 1997. Gibberellin does not accelerate rates of cell division in the dwart pea shoot apical meristem [J]. J. Exp. Bot.,48: 1147–1150.
De Veylder, L., Almedia Engler, J de, Burssens, S, Manevski A, Lescure, B, Van Montague, M, Engler, G and Inze, D 1999. A new D-type cyclin ofArabidopsis thaliana expressed during lateral root primordia formation [J]. Planta,208: 453–462.
Doonan J.H. 1998.Cell division during floral morphogenesis inAntirrinum majus [C]. In: Francis D, Dudits D and Inzé D. (eds) Plant Cell Division. London: Portland Press, pp 207–222.
Elledge, S.J., 1996. Cell cycle checkpoints: preventing an, identity crisis [J]. Science,274: 1664–1672.
Evans, L.S. and Vant Hof, J. 1973 Cell arrest in G2 in root meristems [J] Exp. Cell Res.,82: 471–473.
Evans, L.S. and Vant Hof, J. 1974. Promotion of cell arrest in root and shoot meristems inPisum by factor from the cotyledons [J]. Exp. Cell Res.87: 259–264.
Fosket, D.E. 1977. Regulation of the cell cycle by cytokinin [C]. In: Rost TL (eds) Mechanism and Control of Cell Division. Stroudsberg Pennsylvania: Dowden, Hutchinson and Ross, pp 62–91.
Francis, D. 1998. Cell size and organ development in higher plants [C]. In: Francis D, Dudits D and Inze D (eds) Plant Cell Division. Colchester: Portland Press, pp 187–206.
Francis, D. and Lyndon, R.F. 1985. The control of the cell cycle in relation to floral induction. In: Bryant JA (eds) The Cell Division Cycle in Plants. Cambridge: Cambridge University Press, pp 199–215.
Francis, D. and Sorrell, D. 2001. The interface between the cell cycle and plant growth regulators: a mini review [J]. Plant Growth Reg.,33: 1–12.
Gonthier, R. Jacqmard, A. and Bernier, G. 1987. Changes in cell cycle duration and growth fraction in the shoot meristems ofSinapis during floral transition [J]. Planta,170: 55–59.
Green, P.B. 1994. Connecting gene and hormone action to form, pattern and organogenesis: biophysical transduction [J]. J. Exp. Bot.45 (special issue): 1775–1788.
Hartwell, L.H. and Weinert, T.A. 1989. Checkpoints: controls that ensure the order of cell cycle events [J]. Science,246: 629–634.
Hemerly A.S., Ferreira, P., Van Montague, M., Engler, G. and Inze, D. 1993. cdc2a expression inArabidopsis is linked with competence for cell division [J]. Plant Cell,5: 1711–1723.
Houssa, C., Jacqmard, A. and Bernier, G., 1990. Activation of replicon orgins as possible targets for cytokinins in shoot meristems ofSinapis [J]. Planta,181: 324–326.
Huntley, R., Healy S., Freeman, D., Lavender, P., de Jager, S., Greenwood, J., Makkerh, J., Walker, E., Jackman M., Xie, Q., Bannister, A.J., Kouzarides T., Gutiérrez, C., Doonan, J.H. and Murray, J.A.H. 1998. The maize retinoblastoma protein homologue ZmRb-1 is regulated during leaf development and displays conserved interactions with G1/S regulators and plant cyclin D (CycD) proteins [J]. Plant Mol. Biol.,37: 155–169.
Jackson A.L., Pahl, P.M., Harrison, K., Rosamond, J. and Sclafani, R.A. 1993. Cell cycle regulation of the yeast Cdc7 protein kinase by association with the Dbf4 protein [J]. Mol. Cell Bio.,13: 2899–2908.
Jacobs, T.W. 1997. Why do plant cells divide? [J]. Plant Cell,9: 1021–1029.
Jacqmard, A., Houssa, C. and Bernier, G. 1995. Abscisic acid antagonizes the effect of cytokinin on DNA-replication, origins [J]. J. Exp. Bot.,46: 663–666.
Jiang, W. and Hunter, T. 1997. Identification and characterization of a human protein kinase related to budding yeast Cdc7p [J]. Proc Natl Acad Sci USA,94: 14320–14325.
Laureys, F., Dewitte, W., Witters, E., Van Montague, M., Inze, D. and Van Onckelen, H. 1998. Zeatin is indispensable for the G2-M transition in tobacco BY-2 cells [J]. FEBS Lett.,426: 29–32.
Levine, A.J. 1997. p53, the cellular gatekeeper for growth and division [J]. Cell,88: 323–331.
Lyndon, R.F. 1977. Interacting processes in development at the shoot apex [J]. Symp SEB.,31: 221–250.
Masuda, Y. 1990. Auxin-induced cell elongation and cell wall changes [J]. Bot. Mag.,103: 345–370.
Mazzuca, S., Bitonti, M.B., Pranno, S. and Innocenti, A.M. 1997. Nuclear metabolic changes in root meristem ofLactuca sativa induced by trigonelline [J]. Cytobios,89: 39–50.
Miller, C.O., Skoog, F. and Strong, F.M. 1955. Kinetin, a cell division factor from deoxyribonucleic acid [J]. J. Am. Chem. Soc.,77: 1392.
Mitchell, E.K. and Davies, P.J. 1975. Evidence for three different systems of movement of indoleacetic acid in intact roots ofPhaseolus coccineus [J]. Physiol. Plant,33: 290–294.
Murray, J.A.H., Freeman, D., Greenwood, J., Huntley, R., Makkerh, J., Riou-Khamlichi, C., Sorrell, D.A., Cockcroft, C., Carmichael, J.P., Soni, R. and Shah, Z.H. 1998. Plant D cyclins and retinoblastoma protein homologues [C]. In: Francis D, Dudits D and Inzé D (eds) Plant Cell Division. London: Portland Press, pp 99–127.
Norbury, C. and Nurse, P. 1992. Animal cell cycles and their control [J]. Ann. Rev. Biochem.,61: 441–470.
Nougarede, A., Silveira, C.E. and Rondet, P. 1996. In nature dormant buds andin vitro dormant-like buds ofFraxinus excelsior L [J]. Protoplasma,190: 16–24.
Paulovich, A.G., Toczyski, D.P. and Hartwell, L.H. 1997. When checkpoints fail [J]. Cell,88: 315–321.
Ramírez-Parra, E., Xie, Q., Boniotti, M.B. and Gutierrez, C. 1999. The cloning of plant E2F, a retinoblastoma-binding protein, reveals unique and conserved features with animal G1/S regulators [J]. Nucleic Acids Res.,27: 3527–3533.
Redig, P., Shaul, O., Inze, D., Van Montague, M. and Van Onckelen, H. 1996. Levels of endogenous cytokinins, indole- 3-acetic acid and abscisic acid during the cell cycle of synchronised tobacco BY-2 cells [J]. FEBS Lett.,391: 175–180.
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: unified nomenclature for plant A-, B- and D-type cyclins based on sequence organization [J]. Plant Mol. Biol.,32: 1003–1018.
Rhind, P. and Russell, P. 1998. Mitotic DNA damage and replication checkpoints in yeast [J]. Curr Op Cell Biol.,10: 749–758.
Riou-Khamlichi, C., Huntley, R., Jacqmard A. and Murray, J.A.H. 1999. Cytokinin activation ofArabidopsis cell division through a D-type cyclin [J]. Science,283: 1541–1544.
Sauter, M. and Kende, H. 1992. Gibberellin-induced growth and regulation of the cell division cycle in deepwater rice. Planta 188: 362–368.
Sauter, M., Mekhedov, S.L. and Kende, H. 1995. Gibberellin promotes histone H1 kinase activity and the expression of cdc2 and cyclin genes during the induction of rapid growth in deepwater rice internodes [J]. Plant Journal,7: 623–632.
Scott, T.K. 1972. Auxins and roots. Ann Rev Plant Physiol 23: 235–258.
Sekine, M., Ito, M., Uemukai, K., Maeda, Y., Nakagami, H. and Shinmyo, A. 1999. Isolation and characterisation of, the E2Flike gene in plants [J]. FEBS Lett.,460: 117–122.
Sherr, C.J. 1993. Mammalian G1 cyclins [J]. Cell,73: 1059–1065.
Shibaoka, H. 1994. Plant hormone-induced changes in the orientation of cortical microtubules: Alterations in the crosslinking between microtubules and the plasma membrane [J]. Ann. Rev. Plant. Physiol. Plant Mol. Biol.,45: 527–544.
Soni, R., Camichael, J.P., Shah, Z.H. and Murray, J.A.H. 1995. A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif [J]. Plant Cell,7: 85–103.
Sorrell, D.A. 1999. CycD cyclins and cyclin-dependent kinases in tobacco BY-2 cells [D]. PhD thesis, Cambridge University, UK.
Sorrell, D.A., Combettes, B., Chaubet-Gigot, N., Gigot, C. and Murray, J.A.H. 1999a. Distinct cyclin D genes show mitotic accumulation or constant levels of transcripts in tobacco Bright Yellow-2 cells [J]. Plant Physiol.,119: 343–351.
Sorrell, D.A., Riou-Khamlichi, C., Chaubet-Gigot, N., Combettes, B., Gigot, C. and Murray, J.A.H. 1999b. Plant D-type (CycD) cyclins and the regulation of the plant cell cycle [C]. In: Altmann, A. (eds) Plant Biotechnology and in vitro Biology in the 21th Century. Dordrecht: Kluwer Academic Publishers, pp 441–444.
Taylor, J.H. 1963. DNA systhesis in relation to chromosome reproduction and the reunion of breaks [J]. J Cell Comp Physiol.,62: 73–80.
Trewavas, A.J. 1985. Growth substances, calcium and the regulation of the cell cycle [C]. In: Bryant JA (eds) The Cell Division Cycle in Plants. Cambridge: Cambridge Univ Press, pp 133–156.
Tsurumi, S. and Ohwaki, Y. 1978. Transport of 14C-labeled indoleacetic acid in Vicia root segment [J]. Plant Cell Physiol.,19: 1195–1206.
Vantard, M., and Lambert, A.-M., 1998. Cell cycle dependent nucleation and assembly of plant microtubular proteins [C]. In: Francis D, (eds) Plant Cell Division, Colchester UK: Portland Press, pp 301–318.
VantHof, J. 1973. The regulation of cell division in higher plants [J]. Brookhaven Symp,25: 152–165.
VantHof, J. 1987. Functional chromosomal structure: the replicon [C]. In: Bryant J and Dunham VL (eds) DNA replication in Plants. Boca Raton, Florida: CRC Press, pp 1–16.
VantHof, J., Hoppin, D.P. and Yagi, S. 1973. Cell arrest in G1 and G2 of the mitotic cell cycle ofVicia faba root meristems [J]. Am. J. Bot.,60: 889–895.
Wang, H., Fowke, L.C. and Crosby, W.L. 1997. A plant cyclindependent kinase inhibitor gene [J]. Nature,386: 451.
Zhang, K., Letham, D.S. and John, P.C.L. 1996. Cytokinin controls the cell cycle at mitosis by stimulating the tyrosine dephosphorylation and activation of p34cdc2-like H1 histone kinase [J]. Planta,200: 2–12.
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Biography: TANG Wei (1964-) male, Ph. Doctor, V. Assistant Professor, Department of Biology, Howell Science Complex. East Carolina University, Greenville, NC 27858-4353, USA.
Responsible editor: Chai Ruihai
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Tang, W., Harris, L. & Newton, R.J. The biochemical control of the cell cycle by growth regulators in higher plants. J. of For. Res. 15, 227–232 (2004). https://doi.org/10.1007/BF02911031
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DOI: https://doi.org/10.1007/BF02911031