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. 2008 Jun 15;14(1-2):51–68. doi: 10.1007/s12298-008-0005-3

Emergence of a novel calcium signaling pathway in plants: CBL-CIPK signaling network

Girdhar K Pandey 1,✉
PMCID: PMC3550666  PMID: 23572873

Abstract

In the environment, plants are exposed to plethora of adverse stimuli such as abiotic and biotic stresses. Abiotic stresses including dehydration, salinity and low temperature poses a major threat for crop productivity. Plant responds to these stresses by activating a number of signaling pathways which enable them to defend or adjust against these stresses. To understand the mechanisms by which plants perceive environmental signals and transmit these signals to cellular machinery to activate adaptive responses is of fundamental importance to biology. Calcium plays a pivotal role in plant responses to a number of stimuli including pathogens, abiotic stresses, and hormones. However, the molecular mechanisms underlying calcium functions are poorly understood. It is hypothesized that calcium serves as second messenger and, in many cases, requires intracellular protein sensors to transduce the signal further downstream in the pathways. Recently a novel calcium signaling pathway which consist of calcineurin B-like protein (CBL) calcium sensor and CBL-interacting protein kinase (CIPK) network as a newly emerging signaling system mediating a complex array of environmental stimuli. This review focuses on the overview of functional aspects of CBL and CIPK in plants. In addition, an attempt has also been made to categorize the functions of this CBL-CIPK pair in major signaling pathways in plants.

Key words: Abiotic stress, ABA, Calcium, CBL, CIPK, Signal transduction

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References

  1. Adams F. Soil solution. In: Carson E.W., editor. The plant root and its environment. Charlottesville, VA: University Press of Virginia; 1971. pp. 441–481. [Google Scholar]
  2. Albrecht V., Ritz O., Linder S., Harter K., Kudla J. The NAF domain defines a novel protein-protein interaction module conserved in Ca2+-regulated kinases. EMBO J. 2001;20:1051–1063. doi: 10.1093/emboj/20.5.1051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Albrecht V., Weinl S., Blazevic D., D’Angelo C., Batistic O., Kolukisaoglu U., Bock R., Schulz B., Harter K., Kudla J. The calcium sensor CBL1 integrates plant responses to abiotic stresses. Plant J. 2003;36:457–470. doi: 10.1046/j.1365-313X.2003.01892.x. [DOI] [PubMed] [Google Scholar]
  4. Allen G.J., Chu S.P., Harrington C.L., Schumacher K., Hoffmann T., Tang Y.Y., Grill E., Schroeder J.I. A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature. 2001;411:1053–1057. doi: 10.1038/35082575. [DOI] [PubMed] [Google Scholar]
  5. Amtmann A., Armengaud P., Volkov V. Potassium nutrition and salt stress. In: Blatt M.R., editor. Membrane Transport in Plants. Oxford: Blackwell Publishing; 2004. [Google Scholar]
  6. Amtmann A., Armengaud P. The role of calcium sensor-interacting protein kinases in plant adaptation to potassium-deficiency: new answers to old questions. Cell Res. 2007;17:483–485. doi: 10.1038/cr.2007.49. [DOI] [PubMed] [Google Scholar]
  7. Amtmann A., Jelitto T.C., Sanders D. K+-Selective inward-rectifying channels and apoplastic pH in barley roots. Plant Physiol. 1999;120:331–338. doi: 10.1104/pp.120.1.331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Apse M.P., Blumwald E. Engineering salt tolerance in plants. Curr. Opin. Biotechnol. 2002;13:146–150. doi: 10.1016/S0958-1669(02)00298-7. [DOI] [PubMed] [Google Scholar]
  9. Apse M.P., Aharon G.S., Snedden W.A., Blumwald E. Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science. 1999;285:1256–1258. doi: 10.1126/science.285.5431.1256. [DOI] [PubMed] [Google Scholar]
  10. Apse M.P., Sottosanto J.B., Blumwald E. Vacuolar cation/H+ exchange, ion homeostasis, and leaf development are altered in a T-DNA insertional mutant of AtNHX1, the Arabidopsis vacuolar Na+/H+ antiporter. Plant J. 2003;36:229–239. doi: 10.1046/j.1365-313X.2003.01871.x. [DOI] [PubMed] [Google Scholar]
  11. Ashley M.K., Grant M., Grabov A. Plant responses to potassium deficiencies: a role for potassium transport proteins. J. Exp. Bot. 2006;57:425–436. doi: 10.1093/jxb/erj034. [DOI] [PubMed] [Google Scholar]
  12. Batistic O., Kudla J. Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK protein kinase network. Planta. 2004;219:915–924. doi: 10.1007/s00425-004-1333-3. [DOI] [PubMed] [Google Scholar]
  13. Barabasi A.L., Oltvai Z.N. Network biology: understanding the cells functional organization. Nat. Rev. Genet. 2004;5:101–113. doi: 10.1038/nrg1272. [DOI] [PubMed] [Google Scholar]
  14. Berthomieu P., Conejero G., Nublat A., Brackenbury W.J., Lambert C., Savio C., Uozumi N., Oiki S., Yamada K., Cellier F., Gosti F., Simonneau T., Essah P.A., Tester M., Very A.A., Sentenac H., Casse F. Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance. EMBO J. 2003;22:2004–2014. doi: 10.1093/emboj/cdg207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Bijlmakers M.J., Marsh M. The on-off story of protein palmitoylation. Trends Cell Biol. 2003;13:32–42. doi: 10.1016/S0962-8924(02)00008-9. [DOI] [PubMed] [Google Scholar]
  16. Blumwald E. Sodium transport and salt tolerance in plants. Curr. Opin. Cell Biol. 2000;12:431–434. doi: 10.1016/S0955-0674(00)00112-5. [DOI] [PubMed] [Google Scholar]
  17. Bressan R.A., Hasegawa P.M. AtHKT1 facilitates Na+ homeostasis and K+ nutrition in planta. Plant Physiol. 2004;136:2500–2511. doi: 10.1104/pp.104.042234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Bruggemann, L., Dietrich, P., Becker, D., Dreyer, I. I., Palme, K. and Hedrich, R. Channel-mediated high-affinity K+ uptake into guard cells from Arabidopsis. Proc. Natl. Acad. Sci. U S A., 96:3298–3302. [DOI] [PMC free article] [PubMed]
  19. Burgoyne R.D., Weiss J.L. The neuronal calcium sensor family of Ca2+-binding proteins. Biochem J. 2001;353:1–12. doi: 10.1042/0264-6021:3530001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Berthomieu P., Conejero G., Nublat A., Brackenbury W.J., Lambert C., Savio C., Uozumi N., Oiki S., Yamada K., Cellier F., Gosti F., Simonneau T., Essah P.A., Tester M., Very A.A., Sentenac H., Casse F. Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance. EMBO J. 2003;22:2004–2014. doi: 10.1093/emboj/cdg207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Cheng S.-H., Willmann M.R., Chen H.-C., Sheen J. Calcium signaling through protein kinases: the Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol. 2002;129:469–485. doi: 10.1104/pp.005645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Cheong Y.H., Kim K.N., Pandey G.K., Gupta R., Grant J.J., Luan S. CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis. Plant Cell. 2003;15:1833–1845. doi: 10.1105/tpc.012393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Cheong, Y.H., Pandey, G.K., Grant, J.J., Batistic, O., Li, L., Kim, B.G., Lee, S.L., Kudla, J. and Luan, S. (2007) Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. Plant J, doi: 10.1111/j.1365-313X.2007.03236.x [DOI] [PubMed]
  24. Cherel I. Regulation of K+ channel activities in plants: from physiological to molecular aspects. J Exp Bot. 2004;55:337–351. doi: 10.1093/jxb/erh028. [DOI] [PubMed] [Google Scholar]
  25. Chinnusamy V., Jagendorf A., Zhu J.K. Understanding and improving salt tolerance in plants. Crop Sci. 2005;45:437–448. [Google Scholar]
  26. D’Angelo C., Weinl S., Batistic O., Pandey G.K., Cheong Y.H., Schultke S., Albrecht V., Ehlert B., Schulz B., Harter K., Luan S., Bock R., Kudla J. Alternative complex formation of the Ca2+-regulated protein kinase CIPK1 controls abscisic acid-dependent and independent stress responses in Arabidopsis. Plant J. 2006;48:857–872. doi: 10.1111/j.1365-313X.2006.02921.x. [DOI] [PubMed] [Google Scholar]
  27. Dennison K.L., Robertson W.R., Lewis B.D., Hirsch R.E., Sussman M.R., Spalding E.P. Functions of AKT1 and AKT2 potassium channels determined by studies of single and double mutants of Arabidopsis. Plant Physiol. 2001;127:1012–1019. doi: 10.1104/pp.127.3.1012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Epstein E., Rains D.W., Elzam O. E. Resolution of dual mechanisms of potassium absorption by barley roots. Proc. Natl. Acad. Sci. USA. 1963;49:684–692. doi: 10.1073/pnas.49.5.684. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Epstein E. Dual pattern of ion absorption by plant cells and by plants. Nature. 1966;212:1324–1327. doi: 10.1038/2121324a0. [DOI] [Google Scholar]
  30. Farazi T.A., Waksman G., Gordon J.I. The biology and enzymology of protein N-myristoylation. J. Biol. Chem. 2001;276:39501–39504. doi: 10.1074/jbc.R100042200. [DOI] [PubMed] [Google Scholar]
  31. Fedoroff, N.V. (2002) Cross-talk in abscisic acid signaling. Science’s STKE, RE10. [DOI] [PubMed]
  32. Finkelstein R.R., Gampala S.S.L., Rock C.D. Abscisic acid signaling in seeds and seedlings. Plant Cell. 2002;14:S15–S45. doi: 10.1105/tpc.010441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Flowers T.J., Koyama M.L., Flowers S.A., Sudhakar C., Singh K.P., Yeo A.R. QTL: their place in engineering tolerance of rice to salinity. J. Exp. Bot. 2000;51:99–106. doi: 10.1093/jexbot/51.342.99. [DOI] [PubMed] [Google Scholar]
  34. Foreman J., Demidchik V., Bothwell J.H., Mylona P., Miedema H., Torres M.A., Linstead P., Costa S., Brownlee C., Jones J.D., Davies J.M., Dolan L. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature. 2003;422:442–446. doi: 10.1038/nature01485. [DOI] [PubMed] [Google Scholar]
  35. Fu H.H., Luan S. AtKuP1: a dual-affinity K+ transporter from Arabidopsis. Plant Cell. 1998;10:63–73. doi: 10.1105/tpc.10.1.63. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Garcia A., Rizzo C.A., Ud-Din J., Bartos S.L., Senadhira D., Flowers T.J., Yeo A.R. Sodium and potassium transport to the xylem are inherited independently in rice and the mechanism of sodium:potassium selectivity differs from rice and wheat. Plant Cell Environ. 1997;20:1167–1174. doi: 10.1046/j.1365-3040.1997.d01-146.x. [DOI] [Google Scholar]
  37. Gierth M., Maser P., Schroeder J.I. The potassium transporter AtHAK5 functions in K+-deprivation-induced high-affinity K+-uptake and AKT1 K+ channel contribution to K+ uptake kinetics in Arabidopsis roots. Plant Physiol. 2005;137:1105–1114. doi: 10.1104/pp.104.057216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Giraudat J. Abscisic acid signaling. Curr. Opin. Cell Biol. 1995;7:232–238. doi: 10.1016/0955-0674(95)80033-6. [DOI] [PubMed] [Google Scholar]
  39. Glass A.D.M. Plant Nutrition: An introduction to current concepts. Boston, MA: Jones and Bartlett; 1989. [Google Scholar]
  40. Gong D., Guo Y., Schumaker K.S., Zhu J.K. The SOS3 family of calcium sensors and SOS2 family of protein kinases in Arabidopsis. Plant Physiol. 2004;134:919–926. doi: 10.1104/pp.103.037440. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Gong D., Zhang C., Chen X., Gong Z., Zhu J.K. Constitutive activation and transgenic evaluation of the function of an Arabidopsis PKS protein kinase. J. Biol. Chem. 2002;277:42088–42096. doi: 10.1074/jbc.M205504200. [DOI] [PubMed] [Google Scholar]
  42. Gorham J., Bridges J., Dubcovsky J., Dvorak J., Hollington P.A., Luo M.C., Khan J.A. Genetic analysis and physiology of a trait for enhanced K+/Na+ discrimination in wheat. New Phytol. 1997;137:109–116. doi: 10.1046/j.1469-8137.1997.00825.x. [DOI] [Google Scholar]
  43. Guo Y., Halfter U., Ishitani M., Zhu J.K. Molecular characterization of functional domains in the protein kinase SOS2 that is required for plant salt tolerance. Plant Cell. 2001;13:1383–1400. doi: 10.1105/tpc.13.6.1383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Guo Y., Qiu Q., Quintero F.J., Pardo J.M., Ohta M., Zhang C., Schumaker K.S., Zhu J.-K. Transgenic evaluation of activated mutant alleles of SOS2 reveals a critical requirement for its kinase activity and C-terminal regulatory domain for salt tolerance in Arabidopis thaliana. Plant Cell. 2004;16:435–449. doi: 10.1105/tpc.019174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Guo Y., Xiong L., Song C.P., Gong D., Halfter U., Zhu J.-K. A calcium sensor and its interacting protein kinase are global regulators of abscisic acid signaling in Arabidopsis. Dev. Cell. 2002;3:233–244. doi: 10.1016/S1534-5807(02)00229-0. [DOI] [PubMed] [Google Scholar]
  46. Halfter U., Ishitani M., Zhu J.K. The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc. Natl. Acad. Sci. USA. 2000;97:3735–3740. doi: 10.1073/pnas.040577697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Harmon A.C., Gribskov M., Harper J.F. CDPKs: A kinase for every Ca2+ signal? Trends Plant Sci. 2000;5:154–159. doi: 10.1016/S1360-1385(00)01577-6. [DOI] [PubMed] [Google Scholar]
  48. Harper J.F. Dissecting calcium oscillators in plant cells. Trends Plant Sci. 2001;6:395–397. doi: 10.1016/S1360-1385(01)02023-4. [DOI] [PubMed] [Google Scholar]
  49. Harper J.F., Breton G., Harmon A. Decoding Ca2+ signals through plant protein kinases. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2004;55:263–288. doi: 10.1146/annurev.arplant.55.031903.141627. [DOI] [PubMed] [Google Scholar]
  50. Hasegawa, P.M., Bressan, R.A., Zhu, J.K. and Bohnert, H.J. (2000) Plant Cellular [DOI] [PubMed]
  51. Hedrich R, Kudla J. Calcium signaling networks channel plant K+ uptake. Cell, 125:1221–1223. [DOI] [PubMed]
  52. Hetherington A.M., Brownlee C. The generation of Ca2+ signals in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2004;55:401–427. doi: 10.1146/annurev.arplant.55.031903.141624. [DOI] [PubMed] [Google Scholar]
  53. Hetherington A.M., Woodward F.I. The role of stomata in sensing and driving environmental change. Nature. 2003;424:901–908. doi: 10.1038/nature01843. [DOI] [PubMed] [Google Scholar]
  54. Himmelbach A., Yang Y., Grill E. Relay and control of abscisic acid signaling. Curr. Opin. Plant Biol. 2003;6:470–479. doi: 10.1016/S1369-5266(03)00090-6. [DOI] [PubMed] [Google Scholar]
  55. Hirsch R.E., Lewis B.D., Spalding E.P., Sussman M.R. A role for the AKT1 potassium channel in plant nutrition. Science. 1998;280:918–921. doi: 10.1126/science.280.5365.918. [DOI] [PubMed] [Google Scholar]
  56. Hrabak E.M., Chan C.W., Gribskov M., Harper J.F., Choi J.H., Halford N., Kudla J., Luan S., Nimmo H.G., Sussman M.R., et al. The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol. 2003;132:666–680. doi: 10.1104/pp.102.011999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Ishitani M., Liu J., Halfter U., Kim C.S./., Shi W., Zhu J.K. SOS3 function in plant salt tolerance requires N-myristoylation and calcium binding. Plant Cell. 2000;12:1667–1678. doi: 10.1105/tpc.12.9.1667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Kim, B-G, Waadt, R., Cheong, Y.H., Pandey, G.K., Dominguez-Solis, J.R., Schültke, S., Lee, S.C., Kudla, J. and Luan, S. (2007) The calcium sensor CBL10 mediates salt tolerance by regulating ion homeostasis in Arabidopsis. Plant J., Published article online: 6-Sep-2007 doi: 10.1111/j.1365-313X.2007.03249.x [DOI] [PubMed]
  59. Kim K.N., Cheong Y.H., Grant J.J., Pandey G.K., Luan S. CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis. Plant Cell. 2003;15:411–423. doi: 10.1105/tpc.006858. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Kim K.N., Cheong Y.H., Gupta R., Luan S. Interaction specificity of Arabidopsis calcineurin B-like calcium sensors and their target kinases. Plant Physiol. 2000;124:1844–1853. doi: 10.1104/pp.124.4.1844. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Knight H., Knight M.R. Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci. 2001;6:262–267. doi: 10.1016/S1360-1385(01)01946-X. [DOI] [PubMed] [Google Scholar]
  62. Knight H. Calcium sinaling during abiotic stress in plants. Int. Rev. Cytol. 2000;195:269–324. doi: 10.1016/s0074-7696(08)62707-2. [DOI] [PubMed] [Google Scholar]
  63. Knight H., Knight M.R. Abiotic stress signaling pathways: Specificity and cross-talk. Trends Plant Sci. 2001;6:262–267. doi: 10.1016/S1360-1385(01)01946-X. [DOI] [PubMed] [Google Scholar]
  64. Kochian L.V., Lucas W.J. Potassium transport in roots. Adv. Bot. Research. 1988;15:93–178. [Google Scholar]
  65. Kolukisaoglu U., Weinl S., Blazevic D., Batistic O., Kudla J. Calcium sensors and their interacting protein kinases: genomics of the Arabidopsis and rice CBL-CIPK signaling networks. Plant Physiol. 2004;134:43–58. doi: 10.1104/pp.103.033068. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Kudla J., Xu Q., Harter K., Gruissem W., Luan S. Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals. Proc. Natl. Acad. Sci. USA. 1999;96:4718–4723. doi: 10.1073/pnas.96.8.4718. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Laegreid M., Bockman O.C., Kaarstad O. Agriculture, Fertilizers and the Environment. Oxon, UK: CABI; 1999. [Google Scholar]
  68. Lagarde D., Basset M., Lepetit M., Conejero G., Gaymard F., Astruc S., Grignon C. Tissue-specific expression of Arabidopsis AKT1 gene is consistent with a role in K+ nutrition. Plant J. 1996;9:195–203. doi: 10.1046/j.1365-313X.1996.09020195.x. [DOI] [PubMed] [Google Scholar]
  69. LaHaye P.A., Epstein E. Science. 1969;166:395–396. doi: 10.1126/science.166.3903.395. [DOI] [PubMed] [Google Scholar]
  70. Lauchli, A. (1990) In Calcium in Plant growth and Development, ed. R.T. Leonard and P. K. Hepler, The American Society of Plant Physiologists Symposium Series. American Society Plant Physiol. Rockville, MD, 4: 26–35.
  71. Lee S.C., Lan W.Z., Kim B.G., Li L., Choeng Y.H., Pandey G.K., Lu G., Buchanan B., Luan S. A protein phosphorylation/dephosphorylation network regulates a plant potassium channel. Proc. Natl. Acad. Sci. USA. 2007;104:15959–15964. doi: 10.1073/pnas.0707912104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Leigh R.A., Jones R.G.W. A hypothesis relating critical potassium concentrations for growth to the distribution and functions of this ion in the plant-cell. New Phytol. 1984;97:1–13. doi: 10.1111/j.1469-8137.1984.tb04103.x. [DOI] [Google Scholar]
  73. Li L., Kim B.G., Cheong Y.H., Pandey G.K., Luan S. A Ca2+ signaling pathway regulates a K+ channel for low-K response in Arabidopsis. Proc. Natl. Acad. Sci. U S A. 2006;103:12625–12630. doi: 10.1073/pnas.0605129103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Liu J., Zhu J.K. An Arabidopsis mutant that requires increased calcium for potassium nutrition and salt tolerance. Proc. Natl. Acad. Sci. U S A. 1997;94:14960–14964. doi: 10.1073/pnas.94.26.14960. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Liu J., Ishitani M., Halfter U., Kim C.-S., Zhu J.-K. The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc. Natl. Acad. Sci. U S A. 2000;97:3730–3734. doi: 10.1073/pnas.060034197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Liu J., Zhu J.K. A calcium sensor homolog required for plant salt tolerance. Science. 1998;280:1943–1945. doi: 10.1126/science.280.5371.1943. [DOI] [PubMed] [Google Scholar]
  77. Luan S., Kudla J., Rodriguez-Concepcion M., Yalovsky S., Gruissem W. Calmodulins and calcineurin B-like proteins: Calcium sensors for specific signal response coupling in plants. Plant Cell. 2002;14:S389–S400. doi: 10.1105/tpc.001115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Maathuis F.J.M., Sanders D. Mechanisms of potassium absorption by higher plant roots. Physiol. Plant. 1996;96:158–168. doi: 10.1111/j.1399-3054.1996.tb00197.x. [DOI] [Google Scholar]
  79. Mahajan S., Sopory S.K., Tuteja N. Cloning and characterization of CBL-CIPK signalling components from a legume (Pisum sativum) FEBS J. 2006;273:907–925. doi: 10.1111/j.1742-4658.2006.05111.x. [DOI] [PubMed] [Google Scholar]
  80. Marschner H. Mineral Nutrition of Higher Plants. Ed 2. London: Academic Press; 1995. [Google Scholar]
  81. Martinez-Atienza J., Jiang X., Garciadeblas B., Mendoza I., Zhu J.K., Pardo J.M., Quintero F.J. Conservation of the salt overly sensitive pathway in rice. Plant Physiol. 2007;143:1001–1012. doi: 10.1104/pp.106.092635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Maser P., Thomine S., Schroeder J.I., Ward J.M., Hirschi K., Sze H., Talke I.N., Amtmann A., Maathuis F.J., Sanders D., Harper J.F., Tchieu J., Gribskov M., Persans M.W., Salt D.E., Kim S.A., Guerinot M.L. Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol. 2001;126:1646–1667. doi: 10.1104/pp.126.4.1646. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. McAinsh M.R., Hetherington A.M. Encoding specificity in Ca2+ signaling systems. Trends Plant Sci. 1998;3:32–36. doi: 10.1016/S1360-1385(97)01150-3. [DOI] [Google Scholar]
  84. McCarty D.R., Chory J. Conservation and innovation in plant signaling pathways. Cell. 2000;103:201–209. doi: 10.1016/S0092-8674(00)00113-6. [DOI] [PubMed] [Google Scholar]
  85. Munns R., James R.A., Lauchli A. Approaches to increasing the salt tolerance of wheat and other cereals. J. Exp. Bot. 2006;57:1025–1043. doi: 10.1093/jxb/erj100. [DOI] [PubMed] [Google Scholar]
  86. Nagae M., Nozawa A., Koizumi N., Sano H., Hashimoto H., Sato M., Shimizu T. The crystal structure of the novel calcium binding protein AtCBL2 from Arabidopsis thaliana. J. Biol. Chem. 2003;278:42240–42246. doi: 10.1074/jbc.M303630200. [DOI] [PubMed] [Google Scholar]
  87. Niu X., Narasimhan M.L., Salzman R.A., Bressan R.A., Hasegawa P.M., Nozawa A., Koizumi N., Sano H. An Arabidopsis SNF1-related protein kinase, AtSR1, interacts with a calcium-binding protein, AtCBL2, of which transcripts respond to light. Plant Cell Physiol. 2001;42:976–981. doi: 10.1093/pcp/pce126. [DOI] [PubMed] [Google Scholar]
  88. Ohta M., Guo Y., Halfter U., Zhu J.-K. A novel domain in the protein kinase SOS2 mediates interaction with the protein phosphatase 2C ABI2. Proc. Natl. Acad. Sci. USA. 2003;100:11771–11776. doi: 10.1073/pnas.2034853100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Pandey, G.K., Grant, J.J., Cheong, Y.H., Kim, B.G., Li, L. and Luan, S. (2008) Calcineurin-B-like protein CBL9 interacts with target kinase CIPK3 in the regulation of ABA response in seed germination. In press (Molecular Plants) [DOI] [PubMed]
  90. Pandey G.K., Cheong Y.H., Kim B.G., Grant J.J., Li L., Luan S. CIPK9: a calcium sensor-interacting protein kinase required for low-potassium tolerance in Arabidopsis. Cell Res. 2007;17:411–421. doi: 10.1038/cr.2007.39. [DOI] [PubMed] [Google Scholar]
  91. Pandey G.K., Cheong Y.H., Kim K.N., Grant J.J., Li L., Hung W., D’Angelo C., Weinl S., Kudla J., Luan S. The calcium sensor Calcineurin B-Like 9 modulates ABA sensitivity and biosynthesis in Arabidopsis. Plant Cell. 2004;16:1912–1924. doi: 10.1105/tpc.021311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. Pandey G.K., Grant J.J., Cheong Y.H., Kim B.G., Li L., Luan S. ABR1, an APETALA2-domain transcription factor that functions as a repressor of ABA response in Arabidopsis. Plant Physiol. 2005;139:1185–1193. doi: 10.1104/pp.105.066324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  93. Perrenoud S. Potassium and Plant Health. Basel: International Potash Institute; 1990. [Google Scholar]
  94. Qiu Q.-S., Guo Y., Dietrich M., Schumaker K.S., Zhu J.-K. Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc. Natl. Acad. Sci. U S A. 2002;99:8436–8441. doi: 10.1073/pnas.122224699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  95. Qiu Q.S., Guo Y., Dietrich M.A., Schumaker K.S., Zhu J.K. Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc. Natl. Acad. Sci. U S A. 2002;99:8436–8441. doi: 10.1073/pnas.122224699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. Qiu Q.-S., Guo Y., Quintero F.J., Pardo J.M., Schumaker K.S., Zhu J.-K. Regulation of vacuolar Na+/H+ exchange in Arabidopsis thaliana by the salt-overly sensitive (SOS) pathway. J. Biol. Chem. 2004;279:207–215. doi: 10.1074/jbc.M307982200. [DOI] [PubMed] [Google Scholar]
  97. Qiu Q.S., Barkla B.J., Vera-Estrella R., Zhu J.K., Schumaker K.S. Na+/H+ exchange activity in the plasma membrane of Arabidopsis. Plant Physiol. 2003;132:1041–1052. doi: 10.1104/pp.102.010421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  98. Quan R., Lin H., Mendoza I., Zhang Y., Cao W., Yang Y., Shang M., Chen S., Pardo J.M., Guo Y. SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant Cell. 2007;19:1415–1431. doi: 10.1105/tpc.106.042291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  99. Quintero F.J., Ohta M., Shi H., Zhu J.K., Pardo J.M. Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis. Proc. Natl. Acad. Sci. USA. 2002;99:9061–9066. doi: 10.1073/pnas.132092099. [DOI] [PMC free article] [PubMed] [Google Scholar]
  100. Reddy A.S.N. Calcium: silver bullet in signaling. Plant Sci. 2001;160:381–404. doi: 10.1016/S0168-9452(00)00386-1. [DOI] [PubMed] [Google Scholar]
  101. Ren Z.H., Gao J.P., Li L.G., Cai X.L., Huang W., Chao D.Y., Zhu M.Z., Wang Z.Y., Luan S., Lin H.X. A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat. Genet. 2005;37:1141–1146. doi: 10.1038/ng1643. [DOI] [PubMed] [Google Scholar]
  102. Rubio F., Gassmann W., Schroeder J.I. Sodium driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science. 1995;270:1660–1663. doi: 10.1126/science.270.5242.1660. [DOI] [PubMed] [Google Scholar]
  103. Rudd J.J., Franklin-Tong V.E. Unraveling response-specificity in Ca2+ signaling pathways in plant cells. New Phytol. 2001;151:7–33. doi: 10.1046/j.1469-8137.2001.00173.x. [DOI] [PubMed] [Google Scholar]
  104. Rus A., Lee B.H., Munoz-Mayor A., Sharkhuu A., Miura K., Zhu J.K., Bressan R.A., Hasegawa P.M. AtHKT1 facilitates Na+ homeostasis and K+ nutrition in planta. Plant Physiol. 2004;136:2500–2511. doi: 10.1104/pp.104.042234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  105. Rus A., Yokoi S., Sharkhuu A., Reddy M., Lee B.-H., Matsumoto T.K., Koiwa H., Zhu J.-K., Bressan R.A., Hasegawa P.M. AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots. Proc. Natl. Acad. Sci. USA. 2001;98:14150–14155. doi: 10.1073/pnas.241501798. [DOI] [PMC free article] [PubMed] [Google Scholar]
  106. Sanders D., Brownlee C., Harper J.F. Communicating with calcium. Plant Cell. 1999;11:691–706. doi: 10.1105/tpc.11.4.691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  107. Sanders D., Pelloux J., Brownlee C., Harper J.F. Calcium at the crossroads of signaling. Plant Cell Suppl. 2002;14:S401–S417. doi: 10.1105/tpc.002899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  108. Scrase-Field S.A., Knight M.R. Calcium: just a chemical switch? Curr. Opin. Plant Biol. 2003;6:500–506. doi: 10.1016/S1369-5266(03)00091-8. [DOI] [PubMed] [Google Scholar]
  109. Seamon K.B., Kreetsinger R.H. Calcium-modulated proteins. Met. Ions Biol. 1983;6:1–51. [Google Scholar]
  110. Shi H., Ishitani M., Kim C., Zhu J.-K. The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc. Natl. Acad. Sci. USA. 2000;97:6896–6901. doi: 10.1073/pnas.120170197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  111. Shi H., Wu S.-J., Zhu J.-K. Overexpression of a plasma membrane Na+/H+ antiporter improves salt tolerance in Arabidopsis. Nat. Biotechnol. 2003;21:81–85. doi: 10.1038/nbt766. [DOI] [PubMed] [Google Scholar]
  112. Shi J., Kim K.N., Ritz O., Albrecht V., Gupta R., Harter K., Luan S., Kudla J. Novel protein kinases associated with calcineurin B-like calcium sensors in Arabidopsis. Plant Cell. 1999;11:2393–2405. doi: 10.1105/tpc.11.12.2393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  113. Shi H., Quintero F.J., Pardo J.M., Zhu J.K. The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell. 2002;14:465–477. doi: 10.1105/tpc.010371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  114. Shin R., Schachtman D.P. Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proc. Natl. Acad. Sci. USA. 2004;101:8827–8832. doi: 10.1073/pnas.0401707101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  115. Shinozaki K., Yamaguchi-Shinozaki K. Gene expression and signal transduction in water stress response. Plant Physiol. 1997;115:327–334. doi: 10.1104/pp.115.2.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  116. Shinozaki K., Yamaguchi-Shinozaki K. Molecular responses to dehydration and low temperature: Differences and cross-talk between two stress signaling pathways. Curr. Opin. Plant Biol. 2000;3:217–223. [PubMed] [Google Scholar]
  117. Shinozaki K., Yamaguchi-Shinozaki K., Mizoguchi T., Urao T., Katagiri T., Nakashima K., Abe H., Ichimura K., Liu Q., Nanjyo T., Uno Y., Iuchi S., Seki M., Ito T., Hirayama T., Mikami K.M. Molecular responses to water stress in Arabidopsis thaliana. J. Plant Res. 1998;111:345–351. doi: 10.1007/BF02512195. [DOI] [Google Scholar]
  118. Siddiqi M.Y., Glass A.D.M. Studies of the growth and mineral nutrition of barley varieties2. Potassium uptake and its regulation. Can. J. Bot. 1983;61:1551–1558. [Google Scholar]
  119. Snedden W., Fromm H. Calmodulin, calmodulin-related proteins and plant responses to the environment. Trends Plant Sci. 1998;3:299–304. doi: 10.1016/S1360-1385(98)01284-9. [DOI] [Google Scholar]
  120. Song C.P., Agarwal M., Ohta M., Guo Y., Halfter U., Wang P., Zhu J.K. Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. Plant Cell. 2005;17:2384–2396. doi: 10.1105/tpc.105.033043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  121. Spalding E.P., Hirsch R.E., Lewis D.R., Qi Z., Sussman M.R., Lewis B.D. Potassium uptake supporting plant growth in the absence of AKT1 channel activity: Inhibition by ammonium and stimulation by sodium. J. Gen. Physiol. 1999;113:909–918. doi: 10.1085/jgp.113.6.909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  122. Tester M., Blatt M.R. Direct measurement of K+ channels in thylakoid membranes by incorporation of vesicles into planar lipid bilayers. Plant Physiol. 1989;91:249–252. doi: 10.1104/pp.91.1.249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  123. Very A.A., Sentenac H. Molecular mechanisms and regulation of K+ transport in higher plants. Annu. Rev. Plant Biol. 2003;54:575–603. doi: 10.1146/annurev.arplant.54.031902.134831. [DOI] [PubMed] [Google Scholar]
  124. Wu W., Peters J., Berkowitz G.A. Surface charge-mediated effects of Mg2+ and K+ flux across the chloroplast envelope are associated with regulation of stroma pH and photosynthesis. Plant Physiol. 1991;97:580–587. doi: 10.1104/pp.97.2.580. [DOI] [PMC free article] [PubMed] [Google Scholar]
  125. Xiang Y., Huang Y., Xiong L. Characterization of stress-responsive CIPK genes in rice for stress tolerance improvement. Plant Physiol. 2007;144:1416–1428. doi: 10.1104/pp.107.101295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  126. Xiong L., Zhu J.K. Regulation of abscisic acid biosynthesis. Plant Physiol. 2003;133:29–36. doi: 10.1104/pp.103.025395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  127. Xiong L., Schumaker K.S., Zhu J.-K. Cell signaling during cold, drought, and salt stress. Plant Cell. 2002;14:S165–S183. doi: 10.1105/tpc.010278. [DOI] [PMC free article] [PubMed] [Google Scholar]
  128. Xiong L., Schumaker K.S., Zhu J.-K. Cell signaling during cold, drought, and salt stress. Plant Cell. 2002;14:S165–S183. doi: 10.1105/tpc.010278. [DOI] [PMC free article] [PubMed] [Google Scholar]
  129. Xu J., Li H.D., Chen L.Q., Wang Y., Liu L.L., He L., Wu W.H. A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell. 2006;125:1347–1360. doi: 10.1016/j.cell.2006.06.011. [DOI] [PubMed] [Google Scholar]
  130. Yadav R., Flowers T.J., Yeo A.R. The involvement of the transpirational bypass flow in sodium uptake by high-and low-sodium-transporting lines of rice developed through intra-varietal selection. Plant Cell Environ. 1996;22:329–336. doi: 10.1111/j.1365-3040.1996.tb00255.x. [DOI] [Google Scholar]
  131. Yang T., Poovaiah B.W. Calcium/calmodulin-mediated signal network in plants. Trends Plant Sci. 2003;8:505–512. doi: 10.1016/j.tplants.2003.09.004. [DOI] [PubMed] [Google Scholar]
  132. Yokoi S., Quintero F.J., Cubero B., Ruiz M.T., Bressan R.A., Hasegawa P.M., Pardo J.M. Differential expression and function of Arabidopsis thaliana NHX Na+/H+ antiporters in the salt stress response. Plant J. 2002;30:529–539. doi: 10.1046/j.1365-313X.2002.01309.x. [DOI] [PubMed] [Google Scholar]
  133. Zhu J.-K. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 2002;53:247–273. doi: 10.1146/annurev.arplant.53.091401.143329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  134. Zhu J.K. Regulation of ion homeostasis under salt stress. Curr. Opin. Plant Biol. 2003;6:441–445. doi: 10.1016/S1369-5266(03)00085-2. [DOI] [PubMed] [Google Scholar]
  135. Zielinski R.E. Calmodulin and calmodulin-binding proteins in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1998;49:697–725. doi: 10.1146/annurev.arplant.49.1.697. [DOI] [PubMed] [Google Scholar]

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