Plant Growth Regulation

, Volume 34, Issue 3, pp 253–265 | Cite as

The role of protein kinases in the regulation of plant growth and development

  • Sophie Laurie
  • Nigel G. Halford


We review the role of protein kinases in plant hormone-mediatedsignalling, nutrient signalling and cell cycle control and in the crosstalkbetween these different contributors to plant growth regulation. The areas ofhormone-mediated signalling covered include ABA-mediated responses to osmoticstress, wounding and pathogen attack, as well as ethylene and cytokininsignalling pathways. These areas involve members of several major protein kinasefamilies, including the SNFl-related protein kinase-2 (SnRK2) subfamily, thecalcium-dependent protein kinase (CDPK) family, the mitogen activated protein(MAP) kinase family, the glycogen synthase kinase (GSK)- 3/shaggy family and thereceptor-like protein kinase (RPK) family. In the section on nutrient signallingwe review the role of SnRK1 protein kinases in the global regulation of carbonmetabolism, including aspects of sugar sensing and assimilate partitioning, andwhat is known about nitrogen and sulphur nutrient signalling. In the cell cyclesection, we summarise progress in the elucidation of cell cycle control systemsin plants and discuss the interaction between cell cycle control anddevelopment. We expand further on the hypothesis of crosstalk between differentsignalling pathways in a separate section in which we discuss evidence forinteraction between plant growth regulators and the cell cycle, betweendifferent nutrient signalling pathways, between nutrient and cell cyclesignalling and between nutrient and ABA signalling.

ABA Assimilate partitioning Cell cycle Crosstalk Cytokinin Ethylene Nutrient signalling Phosphorylation Plant growth regulators Plant hormones Signalling SnRK Stress responses Sugar sensing 


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  1. Anderberg R.J. and Walker-Simmons M.K. 1992. Isolation of a wheat cDNA clone for an abscisic acid-inducible transcript with homology to protein kinases. Proc. Natl. Acad. Sci. USA. 89: 10183–10187.Google Scholar
  2. Bach T.J. 1995. Some new aspects of isoprenoid biosynthesis in plants - a review. Lipids. 30: 191–202.Google Scholar
  3. Ball K.L., Barker J.H.A., Halford N.C. and Hardie D.G. 1995. Immunological evidence that HMG-CoA reductase kinasc-A is the cauliflower homologue of the RKIN1 subfamily of plant protein kinases. FEBS. Lett. 377: 189–192.Google Scholar
  4. Barker J.H.A., Slocombe S.P., Ball K.L., Hardie D.G., Shewry P.R. and Halford N.C. 1996. Evidence that barley 3-hydroxy-3-methylglutaryl-Coenzyme A reductase kinase is a member of the sucrose nonfermenting-1-related protein kinase family. Plant Physiology. 112: 1141–1149.Google Scholar
  5. Bell M.H., Halford N.C., Ormrod J.C. and Francis D. 1993. Tobacco plants transformed with cdc25, a mitotic inducer gene from fission yeast. Plant Molec. Biol. 23: 445–451.Google Scholar
  6. Busk P.G. and Pages M. 1998. Regulation of abscisic acid-induced transcription. Plant Molec. Biol. 37: 425–435.Google Scholar
  7. Celenza J.L. and Carlson M. 1986. A yeast gene that is essential for release from glucose repression encodes a protein kinase. Science. 233: 1175–1180.Google Scholar
  8. Davies J.P., Yildiz F.H. and Grossman A.R. 1999. Sac3, an Snf1-like serine threonine kinase that positively and negatively regulates the responses of Chlamydomonas to sulfur limitation. Plant Cell. 11: 1179–1190.Google Scholar
  9. Dickinson J.R., Cole D. and Halford N.G. 1999. A cell cycle role for a plant sucrose nonfermenting-1-related protein kinase (Sn-RK1) is indicated by experiments in yeast.Plant Growth Regulation. 28: 169–174.Google Scholar
  10. Douglas P., Pigaglio E., Ferrer A., Halford N.G. and MacKintosh C. 1997. Three spinach leaf nitrate reductase/3-hydroxy-3-methylglutaryl-CoA reductase kinases that are regulated by reversible phosphorylation and/or Ca2+ ions. Biochem. J. 325: 101–109.Google Scholar
  11. Dunphy W.G. and Kumagai A. 1991. The CDC25 protein contains an intrinsic phosphatase activity. Cell. 67: 189–196.Google Scholar
  12. Eisenreich W., Menhard B., Hylands P.J., Zenk M.H. and Bacher A. 1996. Studies on the biosynthesis of taxol: The taxane carbon skeleton is not of mevalonoid origin. Proc. Natl. Acad. Sci. USA. 93: 6431–6436.Google Scholar
  13. Esser J.F., Liao Y.J. and Schroeder J.I. 1997. Characterization of ion channel modulator effects on ABA-and malate-induced stomatal movements: Strong regulation by kinase and phosphatase inhibitors, and relative insensitivity to mastoporans. J. Exp. Bot. 48: 539–550.Google Scholar
  14. Felix G., Regenass M., Spanu P. and Boller T. 1994. The protein phosphatase inhibitor calyculinA mimics elicitor action in plant cells and induces rapid hyperphosphorylation of specific proteins as revealed by pulse labelling with [P-33] phosphate. Proc. Natl. Acad. Sci. USA. 91: 952–956.Google Scholar
  15. Fesquet D., Labbe J.C., Derancourt J., Capony J.P., Galas S., Girard F. et al. 1993. The MOI5 gene encodes the catalytic subunit of a protein kinase that activates CDC2 and other cyclindependent kinases (CDKS) through phosphorylation of Thr161 and its homologs. EMBO. J. 12: 3111–3121.Google Scholar
  16. Francis D. and Halford N.G. 1995. The Plant Cell Cycle. Physiologia Plantarum. 93: 365–374.Google Scholar
  17. Francis D. and Sorrell D.A. 2001. The interface between the cell cycle and plant growth. Plant Growth Regulation. (in press).Google Scholar
  18. Gancedo J.M. 1998. Yeast carbon catabolite repression. Microbiol. Molec. Biol. Rev. 62: 334–361.Google Scholar
  19. Gómez-Cadenas A., Verhey S.D., Holappa L.D., Shen Q., Ho T.-H.D. and Walker-Simmons M.K. 1999. An abscisic acid-induced protein kinase, PKABA1, mediates abscic acid-suppressed gene expression in barley aleurone layers. Proc. Natl. Acad. Sci. USA. 96: 1767–1772.Google Scholar
  20. Halford N.G. 1999. Metabolic signalling and the partitioning of resources in plant storage organs. Journal of Agricultural Science, Cambridge. 133: 243–249.Google Scholar
  21. Halford N.G. and Hardie D.C. 1998. SNF1-related protein kinases: global regulators of carbon metabolism in plants?. Plant Molec. Biol. 37: 735–748.Google Scholar
  22. Halford N.G., Purcell P.C. and Hardie D.G. 1999. Is hexokinase really a sugar sensor in plants?. Trends in Plant Science. 4: 117–120.Google Scholar
  23. Hanks S.K. and Hunter T. 1995. The eukaryotic protein kinase superfamily. In: Hardie D.G. and Hanks S. (eds), The Protein Kinase Factsbook. vol. I Academic Press, London, pp. 7–47.Google Scholar
  24. Hardie D.G. 1995. Cellular functions of protein kinases. In: Hardie D.G. and Hanks S. (eds), The Protein Kinase Factsbook. vol. I Academic Press, London, pp. 48–56.Google Scholar
  25. Hardie D.G. 1999. Plant protein serine/threonine kinases. Ann. Rev. Plant Pbysioal. Plant Molec. Biol. 50: 97–131.Google Scholar
  26. Hare P.D., Cress W.A. and van Staden J. 1997. The involvement of cytokinins in plant responses to environmental stress. Plant Growth Regulation. 23: 79–103.Google Scholar
  27. Hey S.J., Bacon A., Burnett E. and Neill S.J. 1997. Abscisic acid signal transduction in epidermal cells of Pisum sativun L. Argenteum: Both dehydrin mRNA accumulation and stomatal responses require protein phosphorylation and dephosphorylation. Planta. 202: 85–92.Google Scholar
  28. Himmelbach A., Iten M. and Grill E. 1998. Signalling of abscisic acid to regulate plant growth. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences. 353: 1439–1444.Google Scholar
  29. Hinnebusch A.G. 1994. Translational control of GCN4 — an in vivo barometer of initiation factor activity. Trends. Biochem. Sci. 19: 409–414.Google Scholar
  30. Hirt H. 1997. Multiple roles of MAP kinases in plant signal transduction. Trends. Plant Sci. 2: 11–15.Google Scholar
  31. Holappa L.D. and Walker-Simmons M.K. 1997. The wheat protein kinase gene, TaPK3, of the PKABA1 subfamily is differentially regulated in greening wheat seedlings. Plant Molec. Biol. 33: 935–941.Google Scholar
  32. Hong S.W., Jon J.H., Kwak J.M. and Nam H.G. 1997. Identification of a receptor-like protein kinase gene rapidly induced by abscisic acid, dehydration, high salt, and cold treatments in Arabidopsis thaliana. Plant Physiology. 113: 1203–1212.Google Scholar
  33. Hwang T.W. and Goodman H.M. 1995. An Arabidopsis thaliana root-specific kinase homolog is induced by dehydration, ABA and NaCl. Plant J. 8: 37–43.Google Scholar
  34. Imamura A., Hanaki N., Nakamura A., Suzuki T., Taniguchi M., Kiba T. et al. 1999. Compilation and characterization of Arabidopsis thaliana response regulators implicated in His-Asp phosphorelay signal transduction. Plant Cell Physiol. 40: 733–742.Google Scholar
  35. Kakimoto T. 1996. CKI1, a histidine kinase homolog impicated in cytokinin signal transduction. Science. 254: 982–985.Google Scholar
  36. Knetsch M.L.W., Wang M., Snaar-Jagalska B.E. and Heimovaara-Dijkstra S. 1996. Abscisic acid induces mitogen-activated protein kinase activation in barley aleurone protoplasts. Plant Cell. 8: 1061–1067.Google Scholar
  37. Labbe J.C., Capony J.P., Caput D., Cavadore J.C., Derancourt J., Kaghad M. et al. 1989. MPF from starfish oocytes at 1st meiotic metaphase is a heterodimer containing 1 molecule of CDC2 and 1 molecule of cyclin-B. EMBO. J. 8: 3053–3058.Google Scholar
  38. Lee M.G. and Nurse P. 1987. Cell cycle genes of the fission yeast. Science Progress. 71: 1–14.Google Scholar
  39. Lee S.H., Lee M.H., Chung W.I. and Liu J.R. 1998. WAPK, a Ser/ Thr protein kinase gene of Nicotiana tabacum, is uniquely regulated by wounding, abscisic acid and methyl jasmonate. Molecular and General Genetics. 259: 516–522.Google Scholar
  40. Li J.X. and Assmann S.M. 1996. An abscisic acid-activated and calcium-independent protein kinase from guard cells of fava bean. Plant Cell. 8: 2359–2368.Google Scholar
  41. Mathooko F.M., Inaba A. and Nakamura R. 1998. Characterization of carbon dioxidc stress-induced ethylene biosynthesis in cucuruber (Cucumis sativus L.) fruit. Plant and Cell Physiology. 39: 285–293.Google Scholar
  42. McKibbin R.S., Halford N.G. and Francis D. 1998. Expression of fission yeast cdc25 alters the pattern of lateral root formation in transgenic tobacco. Plant Molecular Biology. 36: 601–612.Google Scholar
  43. Mikami K., Katagiri T., Iuchi S., Yamaguchishinozaki K. and Shinozaki K. 1998. A gene encoding phosphatidylinositol-4-phosphate 5-kinase is induced by water stress and abscisic acid in Arabidopsis thaliana. Plant Journal. 15: 563–568.Google Scholar
  44. Mizoguchi T., Irie K., Hirayama T., Hayashida N., Yamaguchi-Shinozaki K., Matsurnoto K. et al. 1996. A gene encoding a mitogen-activated protein kinase kinase kinase is induced simultaneously with genes for a mitogen-activated protein kinase and an S6 ribosomal protein kinase by touch, cold, and water stress in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA. 93: 765–769.Google Scholar
  45. Morrell S. and ap Rees T. 1986. Sugar metabolism in developing tubers of Solanum tuberosum. Phytochem. 25: 1579–1585.Google Scholar
  46. Muller M. and Knudsen S. 1993. The nitrogen response of a barley C-hordein promoter is controlled by positive and negative regulation of the GCN4 and endosperm box. Plant Journal. 4: 343–355.Google Scholar
  47. Murray J.A.H., Freeman D., Greenwood J., Huntley R., Makkerh J., Riou-Khamlichi C. et al. 1998. Plant D cyclins and retinoblastoma protein homologues. In: Francis D., Dudits and Inze D. (eds), Plant Cell Division. Portland Press, London, pp. 99–127.Google Scholar
  48. Neill S.J. and Burnett E.C. 1999. Regulation of gene expression during water deficit stress. Plant Growth Regulation. 29: 23–33.Google Scholar
  49. Nurse P. 1990. Universal control mechanism regulating onset of M-phase. Nature. 344: 503–508.Google Scholar
  50. Pan Z.Q. and Chang C.R. 1999. Functional complementanon of the Schizosaccharomyces pombe wis1 mutant by Arabidopsis MEK1 and non-catalytic enhancement by jCTR1. FEBS. Lett. 459: 405–410.Google Scholar
  51. Pei Z.M., Kuchitsu K., Ward J.M., Schwarz M. and Schroede J.I. 1997. Differential abscisic acid regulation of guard cell slow anion channels in Arabidopsis wild-type and abi1 and abi2 mutants. Plant Cell. 9: 409–423.Google Scholar
  52. Pestenacz A. and Erdei L. 1996. Calcium-dependent protein kinase in maize and sorghum induced by polyethylene glycol. Physiologia Plantarum. 97: 360–364.Google Scholar
  53. Piao H.L., Pib K.T., Lirn J.H., Kang S.G., Jin J.B., Kim S.H. et al. 1999. An Arabidopsis GSK3/shaggy-like gene that complements yeast salt stress-sensitive mutants is induced by NaCl and abscisic acid. Plant Physiology. 119: 1527–1534.Google Scholar
  54. Poon R.Y.C., Yamashita K., Adamczewski J.P., Hunt T. and Shuttleworth J. 1993. The CDC2-related protein P40(MO15) is the catalytic subunit of a protein kinase that can activate P33(CDK2) and P34(CDC2). EMBO. J. 12: 3123–3132.Google Scholar
  55. Purcell P.C., Smith A.M. and Halford N.G. 1998. Antisense expression of a sucrose nonfermenting-l-reiated protein kinase sequence in potato results in decreased expression of sucrose synthase in tubers and loss of sucrose-inducibility of sucrose synthase transcripts in leaves. Plant Journal. 14: 195–202.Google Scholar
  56. Raz V. and Fluhr R. 1993. Ethylene signal is transduced via protein phosphorylation events in plants. Plant Cell. 5: 523–530.Google Scholar
  57. 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.Google Scholar
  58. Roitsch T. 1999. Source-sink regulation by sugar and stress. Current Opinion Plant Biol. 2: 198–206.Google Scholar
  59. Russell P. and Nurse P. 1987. Negative regulation of mitosis by WEE1+, a gene encoding a protein kinase homolog. Cell. 49: 559–567.Google Scholar
  60. Russell P. and Nurse P. 1987. The mitotic inducer NIM1+ functions in a regulatory network of protein kinase homologs controlling the initiation of mitosis. Cell. 49: 569–576.Google Scholar
  61. Sakakibara H., Hayakawa A., Deji A., Gawronski S.W. and Sugiyama T. 1999. His-Asp phosphotransfer possibly involved in the nitrogen signal transduction mediated by cytokinin in maize: molecular cloning of cDNAs for two-component regulatory factors and demonstration of phosphotransfer activity in vitro. Plant Molec. Biol. 41: 563–573.Google Scholar
  62. Sauter M., Mekhedov S.L. and Kender 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. Plant J. 7: 623–632.Google Scholar
  63. Schmidt C., Schelle I., Liao Y.J. and Schroeder J.I. 1995. Strong regulation of slow anion channels and abscisic acid signalling in guard cells by phosphorylation and dephosphorylation events. Proc. Natl. Acad. Sci. USA. 92: 9535–9539.Google Scholar
  64. Schwarz M. and Schroede J.I. 1998. Abscisic acid maintains S-type anion channel activity in ATP-depleted Vicia faba guard cells. FEBS. lett. 428: 177–182.Google Scholar
  65. Sheen J. 1996. Ca2+-dependent protein kinases and stress signal transduction in plants. Science. 274: 1900–1902.Google Scholar
  66. Solano R. and Ecker J.R. 1998. Ethylene gas: perception, signalling and response. Current Opinion Plant Biol. 1: 393–398.Google Scholar
  67. Sugden C., Donaghy P., Halford N.G. and Hardie D.G. 1999. Two SNF1-related protein kinases from spinach leaf phosphorylate and inactivate HMC-CoA reductase, nitrate reductase and sucrose phosphate synthase in vitro. Plant Physiology. 120: 257–274.Google Scholar
  68. Sun Y.J., Dilkes B.P., Zhang C.S., Dante R.A., Carneiro N.P., Lowe K.S. et al. 1999. Characterization of maize (Zen mays L.) Weel and its activity in developing endosperm. Proc. Natl. Acad. Sci. USA. 96: 4180–4185.Google Scholar
  69. Sung S.-J.S., Xu D.-P. and Black C.C. 1989. Identification of actively-filling sucrose sinks. Plant Physiol. 89: 1117–1121.Google Scholar
  70. Tanaka S. and Nojima H. 1996. Nik1: a Nim1-like protein kinase of S. cerevisicie interacts with the Cdc28 complex and regulates cell cycle progression. Genes to Cells. 1: 905–921.Google Scholar
  71. Thompson-Jaeger S., Francois J., Gaughran J.P. and Tatchell K. 1991. Deletion of SNF1 affects the nutrient response of yeast and resembles mutations which activate the adenylate cyclase pathway. Genetics. 129: 697–706.Google Scholar
  72. Tuomainen J., Betz C., Kangasjarvi J., Ernst D., Yin Z.H., Langebartels C. et al. 1997. Ozone induction of ethylene emission in tomato plants: regulation by differential accumulation of transcripts for the biosynthetic enzymes. Plant J. 12: 1151–1162.Google Scholar
  73. Urao T., Katagiri T., Mizoguchi T., Yamaguchishinozaki K., Hiayashida N. and Shinozaki K. 1994. Genes that encode Ca2+-dependent protein-kinases are induced by drought and high-salt stresses in Arabidopsis thaliana. Molec. Gen. Genet. 244: 331–340.Google Scholar
  74. Wang H., Fowke L.C. and Crosby W.L. 1997. A plant cyclin-dependent kinase inhibitor gene. Nature. 386: 451.Google Scholar
  75. Wek R.C., Jackson B.M. and Hinnebusch A.G. 1989. Juxtaposition of domains homologous to protein kinases and histidyl transfer RNA synthetases in GCN2 protein suggests a mechanism for coupling GCN4 expression to amino acid availability. Proc. Natl. Acad. Sci. USA. 86: 4579–4583.Google Scholar
  76. Woodgett J.R. 1991. A common denominator linking glycogen metabolism, nuclear oncogenes and development. Trends. Biochem. Sci. 16: 177–181.Google Scholar
  77. Zhang K., Diederich L., Sek F.J., Larkin P.J. 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. Planta. 200: 2–12.Google Scholar
  78. Zhou L., Jang J.C., Jones T.L. and Sheen J. 1998. Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucose-insensitive mutant. Proc. Natl. Acad. Sci. USA. 95: 10294–10299.Google Scholar
  79. Zrenner R., Salanoubat M., Wilimitzer L. and Sonnewald U. 1995. Evidence of the crucial role of sucrose synthase for sink strength using transgenic potato plants (Solanum tuberosum L.). Plant J. 7: 97–107.Google Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • Sophie Laurie
    • 1
  • Nigel G. Halford
    • 1
  1. 1.Department of Agricultural SciencesUniversity of Bristol, IACR-Long Ashton Research StationBristolUK

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