Russian Journal of Plant Physiology

, Volume 60, Issue 4, pp 500–506 | Cite as

Plant cell proliferation and its regulators

  • G. V. NovikovaEmail author
  • A. V. Nosov
  • N. S. Stepanchenko
  • A. A. Fomenkov
  • A. S. Mamaeva
  • I. E. Moshkov


Plant growth, where one of the key processes is cell division, is controlled by phytohormones. In this mini-review, an analysis of the literature on the molecular mechanisms controlling plant cell proliferation by phytohormones is presented.


higher plants phytohormones cell proliferation cell cycle 



aminocyclopropan-1-carboxylic acid




CDF-activated kinase


cyclin-dependent protein kinase


CDK inhibitor


calcium-dependent protein kinase




KIP (kinase inhibitory protein)-related protein


retinoblastoma-related protein


prereplicative complex


quiscent center


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  1. 1.
    Francis, D., The plant cell cycle — 15 years on, New Phytol., 2007, vol. 174, pp. 261–278.PubMedCrossRefGoogle Scholar
  2. 2.
    Jurado, S., Trivino, S.D., Abraham, Z., Manzano, C., Gutierrez, C., and del Pozo, C., SKP2A protein, an F-box that regulates cell division, is degraded via the ubiquitin pathway, Plant Signal. Behav., 2008, vol. 10, pp. 810–812.CrossRefGoogle Scholar
  3. 3.
    Berkmans, B. and de Veylder, L., Transcriptional control of the cell cycle, Curr. Opin. Plant Biol., 2009, vol. 12, pp. 599–605.CrossRefGoogle Scholar
  4. 4.
    Doonan, J.H. and Kitsios, G., Functional evolution of cyclin-dependent kinases, Mol. Biotechnol., 2009, vol. 42, pp. 14–29.PubMedCrossRefGoogle Scholar
  5. 5.
    Vandepoele, K., Raes, J., de Veylder, L., Rouze, P., Rombauts, S., and Inze, D., Genome-wide analysis of core cell cycle genes in Arabidopsis, Plant Cell, 2002, vol. 14, pp. 903–916.PubMedCrossRefGoogle Scholar
  6. 6.
    Boruc, J., Daele, H., Hollunder, J., Rombauts, S., Mylle, E., Hilson, P., Inze, D., de Veylder, L., and Russinova, E., Functional modules in the Arabidopsis core cell cycle binary protein-protein interaction network, Plant Cell, 2010, vol. 22, pp. 1264–1280.PubMedCrossRefGoogle Scholar
  7. 7.
    Inze, D. and de Veylder, L., Cell cycle regulation in plant development, Ann. Rev. Genet., 2006, vol. 4, pp. 77–105.CrossRefGoogle Scholar
  8. 8.
    Takatsuka, H., Ohno, R., and Umeda, M., The Arabidopsis cyclin-dependent kinase-activating kinase CDKF;1 is a major regulator of cell proliferation and cell expansion but is dispensable for CDKA activation, Plant J., 2009, vol. 59, pp. 475–487.PubMedCrossRefGoogle Scholar
  9. 9.
    Dewitte, W. and Murray, J.A., The plant cell cycle, Annu. Rev. Plant Biol., 2003, vol. 54, pp. 235–264.PubMedCrossRefGoogle Scholar
  10. 10.
    Wang, G., Kong, H., Sun, Y., Zhang, X., Zhang, W., Altman, N., de Pamphilis, C.W., and Ma, H., Genome-wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin-like proteins, Plant Physiol., 2004, vol. 135, pp. 1084–1099.PubMedCrossRefGoogle Scholar
  11. 11.
    Menges, M., de Jager, S.M., Gruissem, W., and Murray, J.A.H., Global analysis of the core cell cycle regulators of Arabidopsis identifies novel genes, reveals multiple and highly specific profiles of expression and provides a coherent model for plant cell cycle control, Plant J., 2005, vol. 41, pp. 546–566.PubMedCrossRefGoogle Scholar
  12. 12.
    De Veylder, L., Beeckman, T., Beemster, G.T.S., Krols, L., Terras, F., Landrieu, I., van der Schueren, E., Maes, S., Naudts, M., and Inze, D., Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis, Plant Cell, 2001, vol. 13, pp. 1653–1668.PubMedGoogle Scholar
  13. 13.
    Verkest, A., Manes, C.L.D., Vercruysse, S., Maes, S., van der Schueren, E., Beekman, R.T., Genschik, P., Kuiper, M., Inze, D., and de Veylder, I., The cyclin-dependent kinase inhibitor KRP2 controls the onset of the endoreduplication cycle during Arabidopsis leaf development through inhibition of mitotic CDKA;1 kinase complexes, Plant Cell, 2005, vol. 17, pp. 1723–1736.PubMedCrossRefGoogle Scholar
  14. 14.
    Nakai, T., Kato, K., Shinmyo, A., and Sekine, M., Arabidopsis KRPs have distinct inhibitory activity toward cyclin D2-associated kinases, including plant-specific B-type cyclin-dependent kinase, FEBS Lett., 2006, vol. 580, pp. 336–340.PubMedCrossRefGoogle Scholar
  15. 15.
    Joubes, J. and Chevalier, C., Endoreduplication in higher plants, Plant Mol. Biol., 2000, vol. 43, pp. 735–745.PubMedCrossRefGoogle Scholar
  16. 16.
    De Veylder, L., Joubes, J., and Inze, D., Plant cell cycle transitions, Curr. Opin. Plant Biol., 2003, vol. 6, pp. 536–543.PubMedCrossRefGoogle Scholar
  17. 17.
    Tyson, J.J. and Novak, B., Temporal organization of the cell cycle, Curr. Biol., 2008, vol. 18, pp. 759–768.CrossRefGoogle Scholar
  18. 18.
    Shimotohno, A., Ohno, R., Bisova, K., Sakaguchi, N., Huang, J., Koncz, C., Uchimiya, H., and Umeda, M., Diverse phosphoregulatory mechanisms controlling cyclin-dependent kinase activating kinases in Arabidopsis, Plant J., 2006, vol. 47, pp. 701–710.PubMedCrossRefGoogle Scholar
  19. 19.
    Landrieu, I., Costa, M., de Veylder, L., Dewitte, F., Vandepoele, K., Hassan, S., Wieruszeski, J.-M., Faure, J.-D., van Montagu, M., Inze, D., and Lippens, G., A small CDC25 dual specificity tyrosine-phosphatase isoform in Arabidopsis thaliana, Proc. Natl. Acad. Sci. USA, 2004, vol. 101, pp. 13380–13385.PubMedCrossRefGoogle Scholar
  20. 20.
    Sorrell, D.A., Chrimes, D., Dickinson, J.R., Rogers, H.J., and Francis, D., The Arabidopsis CDC25 induces a short cell length when overexpressed in fission yeast: evidence for cell cycle function, New Phytol., 2005, vol. 165, pp. 425–428.PubMedCrossRefGoogle Scholar
  21. 21.
    Del Pozo, J.C., Lopez-Matas, M.A., Ramirez-Parra, E., and Gutierrez, C., Hormonal control of plant cell cycle, Physiol. Plant., 2005, vol. 123, pp. 173–183.CrossRefGoogle Scholar
  22. 22.
    Hartig, K. and Beck, E., Crosstalk between auxin, cytokinins, and sugars in the plant cell cycle, Plant Biol., 2006, vol. 8, pp. 389–396.PubMedCrossRefGoogle Scholar
  23. 23.
    Cho, H.-J., Kwon, H.-K., and Wang, M.-H., Expression of Kip-Related Protein 4 Gene (KRP4) in response to auxin and cytokinin during growth of Arabidopsis thaliana, BMB Rep., 2010, vol. 43, pp. 273–278.PubMedCrossRefGoogle Scholar
  24. 24.
    Perrot-Rechenmann, C., Cellular responses to auxin: division versus expansion, Cold Spring Harbor Perspect., Biol., 2010, vol. 2, p. a001446.CrossRefGoogle Scholar
  25. 25.
    Peret, B., de Rybel, B., Casimiro, I., Benkova, E., Swarup, R., Laplaze, L., Beeckman, T., and Bennett, M.J., Arabidopsis lateral root development: an emerging story, Trends Plant Sci., 2009, vol. 14, pp. 399–408.PubMedCrossRefGoogle Scholar
  26. 26.
    Nieuwland, J., Maughan, S., Dewitte, W., Scofield, S., Sanz, L., and Murray, J.A.H., The D-type cyclin CYCD4;1 modulates lateral root density in Arabidopsis by affecting the basal meristem region, Proc. Natl. Acad. Sci. USA, 2009, vol. 106, pp. 22528–22533.PubMedCrossRefGoogle Scholar
  27. 27.
    De Smet, I., Lau, S., Voss, U., Vanneste, S., Benjamins, R., Rademacher, E.H., Schlereth, A., de Rybel, B., Vassileva, V., Grunewald, W., Naudts, M., Levesque, M.P., Ehrismann, J.S., Inze, D., Luschnig, C., Benfey, P.N., Weijers, D., van Montagu, M.C., Bennett, M.J., Jurgens, G., and Beeckman, T., Bimodular auxin response controls organogenesis in Arabidopsis, Proc. Natl. Acad. Sci. USA, 2010, vol. 107, pp. 2705–2710.PubMedCrossRefGoogle Scholar
  28. 28.
    Vanneste, S., de Rybel, B., Beemster, G.T., Ljung, K., de Smet, I., van Isterdael, G., Naudts, M., Iida, R., Gruissem, W., Tasaka, M., Inze, D., Fukaki, H., and Beeckman, T., Cell cycle progression in the pericycle is not sufficient for SOLITARY ROOT/IAA14-mediated lateral root initiation in Arabidopsis thaliana, Plant Cell, 2005, vol. 17, pp. 3035–3050.PubMedCrossRefGoogle Scholar
  29. 29.
    Sozzani, R., Cui, H., Moreno-Risueno, M.A., Bush, W., van Norman, J.M., Vernoux, T., Brady, S.M., Dewitte, W., Murray, J.A.H., and Benfey, P.N., Spatiotemporal regulation of cell-cycle genes by SHORT-ROOT links patterning and growth, Nature, 2010, vol. 466, pp. 128–132.PubMedCrossRefGoogle Scholar
  30. 30.
    Pasternak, T.P., Otvos, K., Domoki, M., and Feher, A., Linked activation of cell division and oxidative stress defense in alfalfa leaf protoplast-derived cells is dependent on exogenous auxin, Plant Growth Regul., 2007, vol. 51, pp. 109–117.CrossRefGoogle Scholar
  31. 31.
    Orchard, C.B., Siciliano, I., Sorrell, D.A., Marchbank, A., Hilary, J., Rogers, H.J., Francis, D., Herbert, R.J., Suchomelova, P., Lipavska, H., Azmi, A., and van Onckelen, H., Tobacco BY-2 cells expressing fission yeast cdc25 bypass a G2/M block on the cell cycle, Plant J., 2005, vol. 44, pp. 290–299.PubMedCrossRefGoogle Scholar
  32. 32.
    Cutler, S.R., Rodriguez, P.L., Finkelstein, R.R., and Abrams, S.R., Abscisic acid: emergence of a core signalling network, Annu. Rev. Plant Biol., 2010, vol. 61, pp. 651–679.PubMedCrossRefGoogle Scholar
  33. 33.
    Swiatek, A., Lenjou, M., van Bockstaele, D., Inze, D., and van Onckelen, H., Differential effect of jasmonic acid and abscisic acid on cell cycle progression in tobacco BY-2 cells, Plant Physiol., 2002, vol. 128, pp. 201–211.PubMedCrossRefGoogle Scholar
  34. 34.
    Castellano, M.M., Boniotti, M.B., Caro, E., Schnittger, A., and Gutierrez, C., DNA replication licensing affects cell proliferation or endoreplication in a cell type-specific manner, Plant Cell, 2004, vol. 16, pp. 2380–2393.CrossRefGoogle Scholar
  35. 35.
    Mudgil, Y., Singh, B.N., Upadhyaya, K.C., Sopory, S.K., and Reddy, M.K., Cloning and characterization of a cell cycle-regulated gene encoding topoisomerase I from Nicotiana tabacum that is inducible by light, low temperature and abscisic acid, Mol. Genet. Genom., 2002, vol. 267, pp. 380–390.CrossRefGoogle Scholar
  36. 36.
    Meszaros, T., Miskolczi, P., Ayaydin, F., Pettko-Szandtner, A., Peres, A., Magyar, Z., Horvath, G.V., Bako, L., Feher, A., and Dudits, D., Multiple cyclin-dependent kinase complexes and phosphatases control G2/M progression in alfalfa cells, Plant. Mol. Biol., 2000, vol. 43, pp. 595–605.PubMedCrossRefGoogle Scholar
  37. 37.
    Granier, C., Inze, D., and Tardieu, F., Spatial distribution of cell division rate can be deduced from that of p34 (cdc2) kinase activity in maize leaves grown at contrasting temperatures and soil water conditions, Plant Physiol., 2000, vol. 124, pp. 1393–1402.PubMedCrossRefGoogle Scholar
  38. 38.
    West, G., Inze, D., and Beemster, G.T., Cell cycle modulation in the response of the primary root of Arabidopsis to salt stress, Plant Physiol., 2004, vol. 135, pp. 1050–1058.PubMedCrossRefGoogle Scholar
  39. 39.
    Wang, H., Zhou, Y., Bird, D.A., and Fowke, L.C., Functions, regulation and cellular localization of plant cyclin-dependent kinase inhibitors, J. Microscopy, 2008, vol. 231, pp. 234–246.CrossRefGoogle Scholar
  40. 40.
    Lui, J., Wang, H., Delong, C., Fowke, L.C., Crosby, W.L., and Fobert, P.R., The Arabidopsis Cdc2a-interacting protein ICK2 is structurally related to ICK1 and is a potent inhibitor of cyclin-dependent kinase activity in vitro, Plant J., 2000, vol. 21, pp. 379–385.PubMedCrossRefGoogle Scholar
  41. 41.
    Zhou, Y., Fowke, L.C., and Wang, H., Plant CDK inhibitors: studies of interaction with cell cycle regulators in the yeast two-hybrid system and functional comparison in transgenic Arabidopsis plants, Plant Cell Rep., 2002, vol. 20, pp. 967–975.CrossRefGoogle Scholar
  42. 42.
    Weinl, C., Marquardt, S., Kuijt, S.J., Nowack, M.K., Jakoby, M.J., Hulskamp, M., and Schnittder, A., Novel functions of plant cyclin-dependent kinase inhibitors, ICK1/KRP1, can act non-cell-autonomously and inhibit entry into mitosis, Plant Cell, 2005, vol. 17, pp. 1704–1722.PubMedCrossRefGoogle Scholar
  43. 43.
    Wang, H., Qi, Q., Schorr, P., Cutler, A., Crosby, W.L., and Fowke, L.C., ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis thaliana interacts with both Cdc2a and CycD3, and its expression is induced by abscisic acid, Plant J., 1998, vol. 15, pp. 501–510.PubMedCrossRefGoogle Scholar
  44. 44.
    Pettko-Szandtner, A., Meszaros, T., Horvath, G.V., Baka, L., Csordas-Toth, E., Blastyak, A., Zhiponova, M., Miskolczi, P., and Dudits, D., Activation of an alfalfa cyclin-dependent kinase inhibitor by calmodulin-like domain protein kinase, Plant J., 2006, vol. 46, pp. 111–123.PubMedCrossRefGoogle Scholar
  45. 45.
    Cheng, W.H., Endo, A., Zhou, L., Penney, J., Chen, H.-C., Arroyo, A., Leon, P., Nambara, E., Asami, T., Seo, M., Koshiba, T., and Sheen, J., A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions, Plant Cell, 2002, vol. 14, pp. 2723–2743.PubMedCrossRefGoogle Scholar
  46. 46.
    Sharp, R.E., LeNoble, M.E., Else, M.A., Thorne, E.T., and Gherardi, F., Endogenous ABA maintains shoot growth in tomato independently of effects on plant water balance: evidence for an interaction with ethylene, J. Exp. Bot., 2000, vol. 51, pp. 1575–1584.PubMedCrossRefGoogle Scholar
  47. 47.
    Dan, H., Imaseki, H., Wasteneys, G.O., and Kazama, H., Ethylene stimulates endoreduplication but inhibits cytokinesis in cucumber hypocotyl epidermis, Plant Physiol., 2003, vol. 133, pp. 1726–1731.PubMedCrossRefGoogle Scholar
  48. 48.
    Kazama, H., Dan, H., Imaseki, H., and Wasteneys, G.O., Transient exposure to ethylene stimulates cell division and alters the fate and polarity of hypocotyl epidermal cells, Plant Physiol., 2004, vol. 134, pp. 1614–1623.PubMedCrossRefGoogle Scholar
  49. 49.
    Stepanova, A.N., Hoyt, J.M., Hamilton, A.A., and Alonso, J.M., A link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis, Plant Cell, 2005, vol. 17, pp. 2230–2242.PubMedCrossRefGoogle Scholar
  50. 50.
    Stepanova, A.N., Robertson-Hoyt, J., Yun, J., Benavente, L.M., Xie, D., Dolezal, K., Schlereth, A., Jurgens, G., and Alonso, J.M., TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development, Cell, 2008, vol. 133, pp. 177–191.PubMedCrossRefGoogle Scholar
  51. 51.
    Ruzicka, K., Ljung, K., Vanneste, S., Podhorská, R., Beeckman, T., Friml, J., and Benková, E., Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution, Plant Cell, 2007, vol. 19, pp. 2197–2212.PubMedCrossRefGoogle Scholar
  52. 52.
    Swarup, R., Perry, P., Hagenbeek, D., van der Straeten, D., Beemster, G.T., Sandberg, G., Bhalerao, R., Ljung, K., and Bennett, M.J., Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation, Plant Cell, 2007, vol. 19, pp. 2186–2196.PubMedCrossRefGoogle Scholar
  53. 53.
    Ortega-Martínez, O., Pernas, M., Carol, R.J., and Dolan, L., Ethylene modulates stem cell division in the Arabidopsis thaliana root, Science, 2007, vol. 317, pp. 507–510.PubMedCrossRefGoogle Scholar
  54. 54.
    Thomann, A., Lechner, E., Hansen, M., Dumbliauskas, E., Parmentier, Y., Kieber, J., Scheres, B., and Genschik, P., Arabidopsis CULLIN3 genes regulate primary root growth and patterning by ethylene-dependent and -independent mechanisms, PLoS Genet., 2009, vol. 5, p. e1000328.PubMedCrossRefGoogle Scholar
  55. 55.
    Stepanchenko, N.S., Fomenkov, A.A., Moshkov, I.E., Rakitin, V.Yu., Novikova, G.V., and Nosov, A.V., Phytohormone interplay controls proliferation of in vitro cultivated cells of Arabidopsis thaliana ethylene-insensitive mutants, Dokl. Biol. Sci., 2012, vol. 442, pp. 46–49.PubMedCrossRefGoogle Scholar
  56. 56.
    Gendreau, E., Orbovic, V., Hofte, H., and Traas, J., Gibberellin and ethylene control endoreduplication levels in the Arabidopsis thaliana hypocotyl, Planta, 1999, vol. 209, pp. 513–516.PubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2013

Authors and Affiliations

  • G. V. Novikova
    • 1
    Email author
  • A. V. Nosov
    • 1
  • N. S. Stepanchenko
    • 1
  • A. A. Fomenkov
    • 1
  • A. S. Mamaeva
    • 1
  • I. E. Moshkov
    • 1
  1. 1.Timiryazev Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia

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