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Plant Molecular Biology

, Volume 43, Issue 5–6, pp 607–620 | Cite as

CDK-related protein kinases in plants

  • Jérôme Joubès
  • Christian Chevalier
  • Denes Dudits
  • Erwin Heberle-Bors
  • Dirk Inzé
  • Masaaki Umeda
  • Jean-Pierre Renaudin
Article

Abstract

Cyclin-dependent kinases (CDK) form a conserved superfamily of eukaryotic serine-threonine protein kinases, which require binding to a cyclin protein for activity. CDK are involved in different aspects of cell biology and notably in cell cycle regulation. The comparison of nearly 50 plant CDK-related cDNAs with a selected set of their animal and yeast counterparts reveals five classes of these genes in plants. These are described here with respect to their phylogenetic, structural and functional properties. A plant-wide nomenclature of CDK-related genes is proposed, using a system similar to that of the plant cyclin genes. The most numerous class, CDKA, includes genes coding for CDK with the PSTAIRE canonical motif. CDKB makes up a class of plant-specific CDK divided into two groups: CDKB1 and CDKB2. CDKC, CDKD and CDKE form less numerous classes. The CDKD class includes the plant orthologues of metazoan CDK7, which correspond to the CDK-activating kinase (CAK). At present, no functional information is available in plants for CDKC and CDKE.

CDK cell cycle nomenclature 

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References

  1. Andrews, B. and Measday, V. 1998. The cyclin family of budding yeast: abundant use of a good idea. Trends Genet. 14: 66–72.PubMedGoogle Scholar
  2. Brotherton, D.H., Dhanaraj, V., Wick, S., Brizuela, L., Domaille, P.J., Volyanik, E., Xu, X., Parisini, E., Smith, B.O., Archer, S.J., Serrano, M., Brenner, S.L., Blundell, T.L. and Laue, E.D. 1998. Crystal structure of the complex of the cyclin D dependent kinase Cdk6 bound to the cell-cycle inhibitor p19(INK4d). Nature 395: 244–250.PubMedGoogle Scholar
  3. Burssens, S., Van Montagu, M. and Inzé, D. 1998. The cell cycle in Arabidopsis. Plant Physiol. Biochem. 36: 9–19.Google Scholar
  4. Coenen, C. and Lomax, T.L. 1997. Auxin-cytokinin interactions in higher plants: old problems and new tools. Trends Plant Sci. 2: 351–356.CrossRefPubMedGoogle Scholar
  5. Colasanti, J., Tyers, M. and Sundaresan, V. 1991. Identification and characterization of cDNA clones encoding a functional p34cdc2 homologue from Zea mays. Proc. Natl. Acad. Sci. USA 88: 3377–3381.PubMedGoogle Scholar
  6. DeBondt, H.L., Rosenblatt, J., Jancarik, J., Jones, H.D., Morgan, D.O. and Kim, S.H. 1993. Crystal structure of cyclin-dependent kinase 2. Nature 363: 595–602.PubMedGoogle Scholar
  7. Defalco, G. and Giordano, A. 1998. CDK9 (PITALRE): a multifunctional cdc2-related kinase. J. Cell Physiol. 177: 501–506.PubMedGoogle Scholar
  8. Deveylder, L., Segers, G., Glab, N., Casteels, P., Van Montagu, M. and Inzé, D. 1997. The Arabidopsis Cks1At protein binds the cyclin-dependent kinases Cdc2aAt and Cdc2bAt. FEBS Lett. 412: 446–452.PubMedGoogle Scholar
  9. Deveylder, L., Segers, G., Glab, N., Van Montagu, M. and Inzé, D. 1997. Identification of proteins interacting with the Arabidopsis Cdc2aAt protein. J. Exp. Bot. 48: 2113–2114.Google Scholar
  10. Ducommun, B., Brambilla, P., Felix, M. A., Franza, B., Karsenti, E. and Draetta, G. 1991. cdc2 phosphorylation is required for its interaction with cyclin. EMBO J. 10: 3311–3319.PubMedGoogle Scholar
  11. Dudits, D., Magyar, Z., Deak, M., Meszaros, T., Miskolczi, P., Feher, A., Brown, S., Kondorosi, E., Athanasiadis, A., Pongor, S., Bako, L., Koncz, C. and Gyorgyey, 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/Miami, pp. 21–45.Google Scholar
  12. Dynlacht, B.D. 1997. Regulation of transcription by proteins that control the cell cycle. Nature 389: 149–152.PubMedGoogle Scholar
  13. Espinoza, F.H., Farrell, A., Erdjument-Bromage, H., Tempst, P. and Morgan, D.O. 1996. A cyclin-dependent kinase-activating kinase (CAK) in budding yeast unrelated to vertebrate CAK. Science 273: 1714–1717.PubMedGoogle Scholar
  14. Feiler, H. and Jacobs, T. 1991. Cloning of the pea cdc2 homologue by efficient immunological screening of PCR products. Plant Mol. Biol. 17: 321–333.PubMedGoogle Scholar
  15. Ferreira, P.C.G., Hemerly, A.S., Villaroel, R., Van Montagu, M. and Inzé, D. 1991. The Arabidopsis functional homolog of the p34cdc2 protein kinase. Plant Cell 3: 531–540.PubMedGoogle Scholar
  16. Fobert, P.R., Gaudin, V., Lunness, P., Coen, E.S. and Doonan, J.H. 1996. Distinct classes of cdc2-related genes are differentially expressed during the cell division cycle in plants. Plant Cell 8: 1465–1476.PubMedGoogle Scholar
  17. Fowler, J.E. and Quatrano, R.S. 1997. Plant cell morphogenesis: plasma membrane interactions with the cytoskeleton and cell wall. Annu. Rev. Cell. Dev. Biol. 13: 697–743.PubMedGoogle Scholar
  18. Francis, D. and Halford, N.G. 1995. The plant cell cycle. Physiol. Plant. 93: 365–374.Google Scholar
  19. Goldsmith, E.J. and Cobb, M.H. 1994. Protein kinases. Curr. Opin. Struct. Biol. 4: 833–840.PubMedGoogle Scholar
  20. Grafi, G., Burnett, R.J., Helentjaris, T., Larkins, B.A., Decaprio, J.A., Sellers, W.R. and Kaelin, W.G. 1996. A maize cDNA encoding a member of the retinoblastoma protein family: involvement in endoreduplication. Proc. Natl. Acad. Sci. USA 93: 8962–8967.Google Scholar
  21. Hanks, S.K., Quinn, A.M. and Hunter, T. 1988 The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241: 42–52.PubMedGoogle Scholar
  22. Harper, J.W. and Elledge, S.J. 1998. The role of Cdk7 in CAK function, a retro-retrospective. Genes Dev. 12: 285–289.PubMedGoogle Scholar
  23. Hashimoto, J., Hirabayashi, T., Hayano, Y., Hata, S., Ohashi, Y., Suzuka I, Utsugi, T., Toh-E, A. and Kikuchi, Y. 1992. Isolation and characterization of cDNA clones encoding cdc2 homologues from Oryza sativa: a functional homologue and cognate variants. Mol. Gen. Genet. 12: 865–876.Google Scholar
  24. Hata, S. 1991. cDNA cloning of a novel cdc2+/CDC28-related protein kinase from rice. FEBS Lett. 279: 149–152.PubMedGoogle Scholar
  25. Hata, S., Kouchi, H., Suzuka, I. and Ishii, T. 1991. Isolation and characterization of cDNA clones for plant cyclins. EMBO J. 10: 2681–2688.PubMedGoogle Scholar
  26. Heese, M., Mayer, U. and Jurgens, G. 1998. Cytokinesis in flowering plants: cellular process and developmental integration. Curr. Opin. Plant Biol. 1: 486–491.PubMedGoogle Scholar
  27. Hemerly, A., Bergounioux, C., Van Montagu, M., Inzé, D. and Ferreira, P. 1992. Genes regulating the plant cell cycle: isolation of a mitotic-like cyclin from Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 89: 3295–3299.PubMedGoogle Scholar
  28. Hemerly, A.S., Ferreira, P.J.E., Van Montagu, M., Engler, G. and Inzé, D. 1993. cdc2a expression in Arabidopsis is linked with the competence for cell division. Plant Cell 5: 1711–1723.CrossRefPubMedGoogle Scholar
  29. Hirt, H., Pay, A., Bogre, L., Meskiene, I. and Heberle-Bors, E. 1993. cdc2MsB, a cognate cdc2 gene from alfalfa, complements the G1/S but not the G2/M transition of budding yeast cdc28 mutants. Plant J. 4: 61–69.PubMedGoogle Scholar
  30. Hirt, H., Pay, A., Gyorgyev, J., Bako, L., Nemeth, K., Bogre, L., Schweyen, R. J., Heberle-Bors, E. and Dudits, D. 1991. Complementation of a yeast cell cycle mutant by an alfalfa cDNA encoding a protein kinase homologous to p34cdc2. Proc. Natl. Acad. Sci. USA 88: 1636–1640.PubMedGoogle Scholar
  31. Hong, Z., Miao, G. and Verma, D. 1993. p34cdc2 protein kinase homolog from mothbean (Vigna aconitifolia). Plant Physiol. 101: 1399–1400.PubMedGoogle Scholar
  32. Hunter, T. and Plowman, G.D. 1997. The protein kinases of budding yeast: six score and more. Science 22: 18–22.Google Scholar
  33. Imajuku, Y., Hirayama, T., Endoh, H. and Oka, A. 1992. Exonintron organization of the Arabidopsis thaliana protein kinase genes CDC2a and CDC2b. FEBS Lett. 304: 73–77.Google Scholar
  34. Jacobs, T.W. 1995. Cell cycle control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46: 317–339.Google Scholar
  35. Jeffrey, P.D., Russo, A.A., Polyak, K., Gibbs, E., Hurwitz, J., Massagué, J. and Pavletich, N.P. 1995. Mechanism of cdk activation revealed by the structure of a cyclinA-CDK2 complex. Nature 376: 313–320.PubMedGoogle Scholar
  36. Joubès, J., Phan, T.H., Just, D., Rothan, C., Bergounioux, C., Raymond, P. and Chevalier, C. 1999. Molecular and biochemical characterization of the involvement of cyclin-dependent kinase A during the early development of tomato fruit. Plant Physiol. 121: 857–869.Google Scholar
  37. Kaldis, P. 1999. The cdk-activating kinase (CAK): from yeast to mammals. Cell 55: 284–296.Google Scholar
  38. Kidou, S., Umeda, M. and Uchimiya, H. 1992. Nucleotide sequence of rice (Oryza sativa L.) cDNA homologous to cdc2 gene. DNA Seq. 5: 125–129.Google Scholar
  39. Kvarnheden, A., Tandre, K. and Engstrom, P. 1995. A cdc2 homologue and closely related processed retropseudogenes from Norway spruce. Plant Mol. Biol 27: 391–403.PubMedGoogle Scholar
  40. Kvarnheden, A., Albert, V.A. and Engstrom, P. 1998. Molecular evolution of cdc2 pseudogenes in spruce (Picea). Plant Mol. Biol. 36: 767–774.PubMedGoogle Scholar
  41. Lapidot-Lifson, Y., Patinkin, D., Prody, C.A., Ehrlich, G., Seidman, S., Ben-Aziz, R., Benseler, F., Eckstein, F., Zakut, H. and Soreq, H. 1992. Cloning and antisense oligodeoxynucleotide inhibition of a human homolog of cdc2 required in hematopoiesis. Proc. Natl. Acad. Sci. USA 89: 579–583.PubMedGoogle Scholar
  42. Lenburg, M.E. and Oshea, E.K. 1996. Signaling phosphate starvation. Trends Biochem. Sci. 21: 383–387.PubMedGoogle Scholar
  43. Logemann, E., Wu, S.C., Schroder, J., Schmelzer, E., Somssich, I.E. and Hahlbrock, K. 1995. Gene activation by UV light, fungal elicitor or fungal infection in Petroselinum crispum is correlated with repression of cell cycle-related genes. Plant J. 8: 865–876.PubMedGoogle Scholar
  44. Lorbiecke, R. and Sauter, M. 1999. Adventitious root growth and cell-cycle induction in deepwater rice. Plant Physiol. 119: 21–29.PubMedGoogle Scholar
  45. Magyar, Z., Meszaros, T., Miskolczi, P., Deak, M., Feher, A., Brown, S., Kondorosi, E., Athanasiadis, A., Pongor, S., Bilgin, M., Bako, L., Koncz, C. and Dudits, D. 1997. Cell cycle phase specificity of putative cyclin-dependent kinase variants in synchronized alfalfa cells. Plant Cell 9: 223–235.CrossRefPubMedGoogle Scholar
  46. Martinez, M.C., Jorgensen, J.E., Lawton, M.A., Lamb, C.J. and Doerner, P.W. 1992. Spatial pattern of cdc2 expression in relation to meristem activity and cell proliferation during plant development. Proc. Natl. Acad. Sci. USA 89: 7360–7364.PubMedGoogle Scholar
  47. Mendenhall, M.D. and Hodge, A.E. 1998. Regulation of cdc28 cyclin-dependent protein kinase activity during the cell cycle of the yeast Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 62: 1191–1243.PubMedGoogle Scholar
  48. Meyerowitz, E.M. 1997. Genetic control of cell division patterns in developing plants. Cell 88: 299–308.CrossRefPubMedGoogle Scholar
  49. Meyerson, M., Enders, G.H., Wu, C.L., Su, L.K., Gorka, C., Nelson, C., Harlow, E. and Tsai, L.H. 1992. A family of human cdc2-related protein kinases. EMBO J. 11: 2909–2917.PubMedGoogle Scholar
  50. Miao, G., Hong, Z. and Verma, D. 1991. Two functional soybean genes encoding p34cdc2 protein kinases are regulated by different plant developmental pathways. Proc. Natl. Acad. Sci. USA 90: 943–947.Google Scholar
  51. Michaelis, C. and Weeks, G. 1992. Isolation and characterization of a cdc2 cDNA from Dictyostelium discoideum. Biochim. Biophys. Acta 1132: 35–42.PubMedGoogle Scholar
  52. Mironov, V., Deveylder, L., Van Montagu, M. and Inzé, D. 1999. Cyclin-dependent kinases and cell division in plants: the nexus. Plant Cell 11: 509–521.PubMedGoogle Scholar
  53. Morgan, D.O. 1997. Cyclin-dependent kinases: engines, clocks, and microprocessors. Annu. Rev. Cell. Dev. Biol. 13: 261–291.PubMedGoogle Scholar
  54. 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.PubMedGoogle Scholar
  55. Newman, T., de Bruijn, F.J., Green, P., Keegstra, K., Kende, H., McIntosh, L., Ohlrogge, J., Raikhel, N., Somerville, S., Thomashow, M., Retzel, E. and Somerville, C. 1994. Genes galore: a summary of methods for accessing results from large-scale partial sequencing of anonymous Arabidopsis cDNA clones. Plant Physiol. 106: 1241–1255.PubMedGoogle Scholar
  56. Nigg, E.A. 1995. Cyclin-dependent protein kinases: key regulators of the eukaryotic cell cycle. Bioessays 17: 471–480.PubMedGoogle Scholar
  57. Norbury, C. and Nurse, P. 1992. Animal cell cycles and their control. Annu. Rev. Biochem. 61: 441–470.PubMedGoogle Scholar
  58. Porat, R., Lu, P.Z. and Oneill, S.D. 1998. Arabidopsis SKP1, a homologue of a cell cycle regulator gene, is predominantly expressed in meristematic cells. Planta 204: 345–351.PubMedGoogle Scholar
  59. Price, C.A., Reardon, E.M. and Lonsdale, D.M. 1996. A guide to naming sequenced plant genes. Plant Mol. Biol. 30: 225–227.PubMedGoogle Scholar
  60. Renaudin, J.P., Doonan, J.H., Freeman, D., Hashimoto, J., Hirt, H., Inzé, D., Jacobs, T., Kouchi, H., Rouze, P., Sauter, M., Savoure, 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.PubMedGoogle Scholar
  61. Rickert, P., Seghezzi, W., Shanahan, F., Cho, H. and Lees, E. 1996. Cyclin C/CDK8 is a novel CTD kinase associated with RNA polymerase II. Oncogene 12: 2631–2640.PubMedGoogle Scholar
  62. Russo, A.A., Jeffrey, P.D., Patten, A.K., Massague, J. and Pavletich, N.P. 1996a. Crystal structure of the p27(Kip1) cyclin-dependentkinase inhibitor bound to the cyclin A Cdk2 complex. Nature 382: 325–331.CrossRefPubMedGoogle Scholar
  63. Russo, A.A., Jeffrey, P.D. and Pavletich, N.P. 1996b. Structural basis of cyclin-dependent kinase activation by phosphorylation. Nature Struct. Biol. 3: 696–700.PubMedGoogle Scholar
  64. Russo, A.A., Tong, L., Lee, J.O., Jeffrey, P.D. and Pavletich, N.P. 1998. Structural basis for inhibition of the cyclin-dependent kinase Cdk6 by the tumour suppressor p16(INK4a). Nature 395: 237–243.PubMedGoogle Scholar
  65. Sauter, M. 1997. Differential expression of a CAK (cdc2-activating kinase)-like protein kinase, cyclins and cdc2 genes from rice during the cell cycle and in response to gibberellin. Plant J. 11: 181–190.PubMedGoogle Scholar
  66. Segers, G., Gadisseur, I., Bergounioux, C., Engler, J.D., Jacqmard, A., Van Montagu, M. and Inzé, D. 1996. The Arabidopsis cyclin-dependent kinase gene cdc2bAt is preferentially expressed during S and G(2) phases of the cell cycle. Plant J. 10: 601–612.PubMedGoogle Scholar
  67. Serizawa, H., Makela, T.P., Conaway, J.W., Conaway, R.C., Weinberg, R.A. and Young, R.A. 1995. Association of CDKactivating kinase subunits with transcription factor TFIIH. Nature 374: 280–282.PubMedGoogle Scholar
  68. Setiady, Y.Y., Sekine, M., Hariguchi, N., Kouchi, H. and Shinmyo, A. 1996. Molecular cloning and characterization of a cDNA clone that encodes a Cdc2 homolog from Nicotiana tabacum. Plant Cell Physiol. 37: 369–376.PubMedGoogle Scholar
  69. Shaul, O., Van Montagu, M. and Inzé, D. 1996. Regulation of cell division in Arabidopsis. Crit. Rev. Plant Sci. 15: 97–112.Google Scholar
  70. Shimizu, S. and Mori, H. 1998. Analysis of cycles of dormancy and growth in pea axillary buds based on mRNA accumulation patterns of cell cycle-related genes. Plant Cell Physiol. 39: 255–262.PubMedGoogle Scholar
  71. Soni, R., Carmichael, 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. Plant Cell 7: 85–103.CrossRefPubMedGoogle Scholar
  72. Sopory, S.K. and Munshi, M. 1998. Protein kinases and phosphatases and their role in cellular signaling in plants. Crit. Rev. Plant Sci. 17: 245–318.Google Scholar
  73. 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.CrossRefPubMedGoogle Scholar
  74. Sun, Y.J., Dilkes, B.P., Zhang, C.S., Dante, R.A., Carneiro, N.P., Lowe, K.S., Jung, R., Gordon-Kamm, W.J. and Larkins, B.A. 1999. Characterization of maize (Zea mays L.) Wee1 and its activity in developing endosperm. Proc. Natl. Acad. Sci. USA 96: 4180–4185.PubMedGoogle Scholar
  75. Tassan, J.P., Jaquenoud, M., Leopold, P., Schultz, S.J. and Nigg, E.A. 1995. Identification of human cyclin-dependent kinase 8, a putative protein kinase partner for cyclin C. Proc. Natl. Acad. Sci. USA 92: 8871–8875.PubMedGoogle Scholar
  76. Thuret, J.Y., Valay, J.G., Faye, G. and Mann, C. 1996. Civ1 (CAK in vivo), a novel Cdk-activating kinase. Cell 86: 565–576.PubMedGoogle Scholar
  77. Trehin, C., Planchais, S., Glab, N., Perennes, C., Tregear, J. and Bergounioux, C. 1998. Cell cycle regulation by plant growth regulators: involvement of auxin and cytokinin in the re-entry of Petunia protoplasts into the cell cycle. Planta 206: 215–224.PubMedGoogle Scholar
  78. Umeda, M., Bhalerao, R.P., Schell, J., Uchimiya, H. and Koncz, C. 1998. A distinct cyclin-dependent kinase-activating kinase of Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 95: 5021–5026.PubMedGoogle Scholar
  79. Umeda, M., Umedahara, C., Yamaguchi, M., Hashimoto, J. and Uchimiya, H. 1999. Differential expression of genes for cyclindependent protein kinases in rice plants. Plant Physiol. 119: 31–40.PubMedGoogle Scholar
  80. Wang, H., Fowke, L.C. and Crosby, W.L. 1997. A plant cyclindependent kinase inhibitor gene. Nature 386: 451–452.CrossRefPubMedGoogle Scholar
  81. Wang, H., Qi, Q.G., 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 CycD3, and its expression is induced by abscisic acid. Plant J. 15: 501–510.PubMedGoogle Scholar
  82. Xie, Q., Sanzburgos, P., Hannon, G. J. and Gutierrez, C. 1996. Plant cells contain a novel member of the retinoblastoma family of growth regulatory proteins. EMBO J. 15: 4900–4908.PubMedGoogle Scholar
  83. Yamaguchi, M., Umeda, M. and Uchimiya, H. 1998. A rice homolog of Cdk7/MO15 phosphorylates both cyclin-dependent protein kinases and the carboxy-terminal domain of RNA polymerase II. Plant J. 16: 613–619.CrossRefPubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Jérôme Joubès
    • 1
  • Christian Chevalier
    • 1
  • Denes Dudits
    • 2
  • Erwin Heberle-Bors
    • 3
  • Dirk Inzé
    • 4
  • Masaaki Umeda
    • 5
  • Jean-Pierre Renaudin
    • 6
  1. 1.Laboratory of Plant PhysiologyNational Institute for Agronomic Research INRAVillenave d'Ornon CedexFrance
  2. 2.Institute of Plant Biology, Biological Research CenterHungarian Academy of SciencesSzegedHungary
  3. 3.Institute of Microbiology and GeneticsUniversity of ViennaViennaAustria
  4. 4.Department of GeneticsUniversity of GentGentBelgium
  5. 5.Institute of Molecular and Cellular BiosciencesUniversity of TokyoTokyoJapan
  6. 6.Laboratory of Plant Cellular and Molecular Developmental BiologyUniversity Bordeaux 1Talence Cedex

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