Plant Growth Regulation

, Volume 76, Issue 1, pp 3–12 | Cite as

The role of the CBL–CIPK calcium signalling network in regulating ion transport in response to abiotic stress

  • Emily Laurina Thoday-Kennedy
  • Andrew Keith Jacobs
  • Stuart John Roy
Original paper


Plants are sessile organisms and have multiple tolerance mechanisms which allow them to adapt to the environmental stresses to which they may be exposed. Key to a plant’s tolerance of abiotic stresses is the ability to rapidly detect stress and activate the appropriate stress response mechanism. The calcineurin B-like (CBL) and CBL-interacting protein kinase (CIPK) signalling pathway is a flexible Ca2+ signalling network which allows a plant to fine tune its response to stress, via both pre- and post-translational mechanisms. Genes encoding CBLs and CIPKs have now been identified in a variety of plant species. Plants have been found to have large gene families of CBLs and CIPKs, each encoding proteins with specific upstream and downstream targets, thus providing the flexibility required to allow a plant to adapt to a variety of stresses. Characterisation of CBL and CIPK mutants have shown them to be important for a plant to survive cold, drought, heat, salinity and low nutrient stresses. Many CBLs and CIPKs have been shown to be involved in the transport of ions through a plant, either limiting the supply of toxic ions to certain tissues or maximising the uptake of beneficial nutrients from the soil. This review will provide an update into the current knowledge of CBL and CIPK interactions and their role in ion transport during abiotic stress.


Calcium signalling Calcineurin B-like protein CBL-interacting protein kinase Abiotic stress 


  1. Albrecht V, Ritz O, Linder S, Harter K, Kudla J (2001) The NAF domain defines a novel protein–protein interaction module conserved in Ca2+-regulated kinases. EMBO J 20:1051–1063PubMedCentralPubMedGoogle Scholar
  2. Albrecht V, Weinl S, Blazevic D, D’Angelo C, Batistic O, Kolukisaoglu Ü, Bock R, Schulz B, Harter K, Kudla J (2003) The calcium sensor CBL1 integrates plant responses to abiotic stresses. Plant J 36:457–470PubMedGoogle Scholar
  3. Alemán F, Nieves-Cordones M, Martínez V, Rubio F (2011) Root K+ acquisition in plants: the Arabidopsis thaliana model. Plant Cell Physiol 52:1603–1612PubMedGoogle Scholar
  4. Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1337–1344Google Scholar
  5. Batistič O, Kudla J (2004) Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK protein kinase network. Planta 219:915–924PubMedGoogle Scholar
  6. Batistič O, Kudla J (2012) Analysis of calcium signaling pathways in plants. Biochim Biophys Acta 1820:1283–1293PubMedGoogle Scholar
  7. Batistič O, Sorek N, Schültke S, Yalovsky S, Kudla J (2008) Dual fatty acyl modification determines the localization and plasma membrane targeting of CBL/CIPK Ca2+ signaling complexes in Arabidopsis. Plant Cell 20:1346–1362PubMedCentralPubMedGoogle Scholar
  8. Batistič O, Waadt R, Steinhorst L, Held K, Kudla J (2010) CBL-mediated targeting of CIPKs facilitates the decoding of calcium signals emanating from distinct cellular stores. Plant J 61:211–222PubMedGoogle Scholar
  9. Bose J, Pottosin II, Shabala SS, Palmgren MG, Shabala S (2011) Calcium efflux systems in stress signaling and adaptation in plants. Front Plant Sci 2:1–17Google Scholar
  10. Chakraborty K, Sairam RK, Bhattacharya RC (2012) Differential expression of salt overly sensitive pathway genes determines salinity stress tolerance in Brassica genotypes. Plant Physiol Biochem 51:90–101PubMedGoogle Scholar
  11. Chen J-H, Sun Y, Sun F, Xia X-L, Yin W-L (2011a) Tobacco plants ectopically expressing the Ammopiptanthus mongolicus AmCBL1 gene display enhanced tolerance to multiple abiotic stresses. Plant Growth Regul 63:259–269Google Scholar
  12. Chen X, Gu Z, Liu F, Ma B, Zhang H (2011b) Molecular analysis of rice CIPKs involved in both biotic and abiotic stress responses. Rice Sci 18:1–9Google Scholar
  13. Chen L, Ren F, Zhou L, Wang Q-Q, Zhong H, Li X-B (2012) The Brassica napus calcineurin B-Like 1/CBL-interacting protein kinase 6 (CBL1/CIPK6) component is involved in the plant response to abiotic stress and ABA signalling. J Exp Bot 63:6211–6222PubMedCentralPubMedGoogle Scholar
  14. Chen L, Wang Q-Q, Zhou L, Ren F, Li D-D, Li X-B (2013) Arabidopsis CBL-interacting protein kinase (CIPK6) is involved in plant response to salt/osmotic stress and ABA. Mol Biol Rep 40:4759–4767PubMedGoogle Scholar
  15. Chen X, Huang Q, Zhang F, Wang B, Wang J, Zheng J (2014) ZmCIPK21, a maize CBL-interacting kinase, enhances salt stress tolerance in Arabidopsis thaliana. Int J Mol Sci 15:14819–14834PubMedCentralPubMedGoogle Scholar
  16. Cheong Y, Kim K, Pandey G, Gupta R, Grant J, Luan S (2003) CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis. Plant Cell 15:1833–1845PubMedCentralPubMedGoogle Scholar
  17. Cheong YH, Pandey GK, Grant JJ, Batistic O, Li L, Kim B-G, Lee S-C, Kudla J, 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 52:223–239PubMedGoogle Scholar
  18. Cheong YH, Sung SJ, Kim B-G, Pandey GK, Cho J-S, Kim K-N, Luan S (2010) Constitutive overexpression of the calcium sensor CBL5 confers osmotic or drought stress tolerance in Arabidopsis. Mol Cells 29:159–165PubMedGoogle Scholar
  19. Chérel I, Michard E, Platet N, Mouline K, Alcon C, Sentenac H, Thibaud JB (2002) Physical and functional interaction of the Arabidopsis K+ channel AKT2 and phosphatase AtPP2CA. Plant Cell 14:1133–1146PubMedCentralPubMedGoogle Scholar
  20. Choi W-G, Toyota M, Kim S-H, Hilleary R, Gilroy S (2014) Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. Proc Natl Acad Sci USA 111:6497–6502PubMedCentralPubMedGoogle Scholar
  21. Cuéllar T, Pascaud F, Verdeil J-L, Torregrosa L, Adam-Blondon A-F, Thibaud J-B, Sentenac H, Gaillard I (2010) A grapevine Shaker inward K+ channel activated by the calcineurin B-like calcium sensor 1-protein kinase CIPK23 network is expressed in grape berries under drought stress conditions. Plant J 61:58–69PubMedGoogle Scholar
  22. Cuéllar T, Azeem F, Andrianteranagna M, Pascaud F, Verdeil J-L, Sentenac H, Zimmermann S, Gaillard I (2013) Potassium transport in developing fleshy fruits: the grapevine inward K+ channel VvK1.2 is activated by CIPK–CBL complexes and induced in ripening berry flesh cells. Plant J 73:1006–1018PubMedGoogle Scholar
  23. D’Angelo C, Weinl S, Batistič O, Pandey GK, Cheong YH, Schültke S, Albrecht V, Ehlert B, Schulz B, Harter K, Luan S, Bock R, Kudla J (2006) Alternative complex formation of the Ca2+-regulated protein kinase CIPK1 controls abscisic acid-dependent and independent stress responses in Arabidopsis. Plant J 48:857–872PubMedGoogle Scholar
  24. De la Torre F, Gutiérrez-Beltrán E, Pareja-Jaime Y, Chakravarthy S, Martin GB, del Pozo O (2013) The tomato calcium sensor CBL10 and its interacting protein kinase CIPK6 define a signaling pathway in plant immunity. Plant Cell 25:2748–2764PubMedCentralPubMedGoogle Scholar
  25. Deeken R, Geiger D, Fromm J, Koroleva O, Ache P, Langenfeld-Heyser R, Sauer N, May ST, Hedrich R (2002) Loss of the AKT2/3 potassium channel affects sugar loading into the phloem of Arabidopsis. Planta 216:334–344PubMedGoogle Scholar
  26. Deng X, Hu W, Wei S, Zhou S, Zhang F, Han J, Chen L, Li Y, Feng J, Fang B, Luo Q, Li S, Liu Y, Yang G, He G (2013a) TaCIPK29, a CBL-interacting protein kinase gene from wheat, confers salt stress tolerance in transgenic tobacco. PLoS One 8:e69881PubMedCentralPubMedGoogle Scholar
  27. Deng X, Zhou S, Hu W, Feng J, Zhang F, Chen L, Huang C, Luo Q, He Y, Yang G, He G (2013b) Ectopic expression of wheat TaCIPK14, encoding a calcineurin B-like protein-interacting protein kinase, confers salinity and cold tolerance in tobacco. Physiol Plant 149:367–377PubMedGoogle Scholar
  28. Dennison KL, Robertson WR, Lewis BD, Hirsch RE, Sussman MR, Spalding EP (2001) Functions of AKT1 and AKT2 potassium channels determined by studies of single and double mutants of Arabidopsis. Plant Physiol 127:1012–1019PubMedCentralPubMedGoogle Scholar
  29. Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61:593–620PubMedGoogle Scholar
  30. Drerup MM, Schlücking K, Hashimoto K, Manishankar P, Steinhorst L, Kuchitsu K, Kudla J (2013) The calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF. Mol Plant 6:559–569PubMedGoogle Scholar
  31. Eckert C, Offenborn JN, Heinz T, Armarego-Marriott T, Schültke S, Zhang C, Hillmer S, Heilmann M, Schumacher K, Bock R, Heilmann I, Kudla J (2014) The vacuolar calcium sensors CBL2 and CBL3 affect seed size and embryonic development in Arabidopsis thaliana. Plant J 78:146–156PubMedGoogle Scholar
  32. Elphick CH, Sanders D, Maathuis FJM (2001) Critical role of divalent cations and Na+ efflux in Arabidopsis thaliana salt tolerance. Plant Cell Environ 24:733–740Google Scholar
  33. Forde BG (2002) Local and long-range signaling pathways regulating plant responses to nitrate. Annu Rev Plant Biol 53:203–224PubMedGoogle Scholar
  34. Gajdanowicz P, Michard E, Sandmann M, Rocha M, Corrêa LGG, Ramírez-Aguilar SJ, Gomez-Porras JL, González W, Thibaud J-B, van Dongen JT, Dreyer I (2011) Potassium (K+) gradients serve as a mobile energy source in plant vascular tissues. Proc Natl Acad Sci USA 108:864–869PubMedCentralPubMedGoogle Scholar
  35. Gao S, Yuan L, Zhai H, Liu C, He S, Liu Q (2012) Overexpression of SOS genes enhanced salt tolerance in sweetpotato. J Integr Agric 11:378–386Google Scholar
  36. Gill PK, Sharma AD, Singh P, Bhullar SS (2003) Changes in germination, growth and soluble sugar contents of Sorghum bicolor (L.) Moench seeds under various abiotic stresses. Plant Growth Regul 40:157–162Google Scholar
  37. Gu Z, Ma B, Jiang Y, Chen Z, Su X, Zhang H (2008) Expression analysis of the calcineurin B-like gene family in rice (Oryza sativa L.) under environmental stresses. Gene 415:1–12PubMedGoogle Scholar
  38. Guo Y, Xiong L, Song C-P, Gong D, Halfter U, Zhu J-K (2002) A calcium sensor and its interacting protein kinase are global regulators of abscisic acid signaling in Arabidopsis. Dev Cell 3:233–244PubMedGoogle Scholar
  39. Guo Y, Qiu Q-S, Quintero FJ, Pardo JM, Ohta M, Zhang C, Schumaker KS, Zhu J-K (2004) 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 Arabidopsis thaliana. Plant Cell 16:435–449PubMedCentralPubMedGoogle Scholar
  40. Halfter U, Ishitani M, Zhu JK (2000) The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc Natl Acad Sci USA 97:3735–3740PubMedCentralPubMedGoogle Scholar
  41. He L, Yang X, Wang L, Zhu L, Zhou T, Deng J, Zhang X (2013) Molecular cloning and functional characterization of a novel cotton CBL-interacting protein kinase gene (GhCIPK6) reveals its involvement in multiple abiotic stress tolerance in transgenic plants. Biochem Biophys Res Commun 435:209–215PubMedGoogle Scholar
  42. Held K, Pascaud F, Eckert C, Gajdanowicz P, Hashimoto K, Corratgé-Faillie C, Offenborn JN, Lacombe B, Dreyer I, Thibaud J-B, Kudla J (2011) Calcium-dependent modulation and plasma membrane targeting of the AKT2 potassium channel by the CBL4/CIPK6 calcium sensor/protein kinase complex. Cell Res 21:1116–1130PubMedCentralPubMedGoogle Scholar
  43. Ho C-H, Lin S-H, Hu H-C, Tsay Y-F (2009) CHL1 functions as a nitrate sensor in plants. Cell 138:1184–1194PubMedGoogle Scholar
  44. Hu H-C, Wang Y-Y, Tsay Y-F (2009) AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. Plant J 57:264–278PubMedGoogle Scholar
  45. Hu D-G, Li M, Luo H, Dong Q-L, Yao Y-X, You C-X, Hao Y-J (2012) Molecular cloning and functional characterization of MdSOS2 reveals its involvement in salt tolerance in apple callus and Arabidopsis. Plant Cell Rep 31:713–722PubMedGoogle Scholar
  46. Huang N, Chiang C, Crawford NM, Tsay Y-F (1996) CHL1 encodes a component of the low-affinity nitrate uptake system in Arabidopsis and shows cell type-specific expression in roots. Plant Cell 8:2183–2191PubMedCentralPubMedGoogle Scholar
  47. Huertas R, Olías R, Eljakaoui Z, Gálvez FJ, Li J, De Morales PA, Belver A, Rodríguez-Rosales MP (2012) Overexpression of SlSOS2 (SlCIPK24) confers salt tolerance to transgenic tomato. Plant Cell Environ 35:1467–1482PubMedGoogle Scholar
  48. Jacobs B, Pearson C (1999) Growth, development and yield of rice in response to cold temperature. J Agron Crop Sci 182:79–88Google Scholar
  49. Jannesar M, Razavi K, Saboora A (2014) Effects of salinity on expression of the salt overly sensitive genes in Aeluropus lagopoides. Aust J Crop Sci 8:1–8Google Scholar
  50. Kim B-G, Waadt R, Cheong YH, Pandey GK, Dominguez-Solis JR, Schültke S, Lee SC, Kudla J, Luan S (2007) The calcium sensor CBL10 mediates salt tolerance by regulating ion homeostasis in Arabidopsis. Plant J 52:473–484PubMedGoogle Scholar
  51. Kleist TJ, Spencley AL, Luan S (2014) Comparative phylogenomics of the CBL–CIPK calcium-decoding network in the moss Physcomitrella, Arabidopsis, and other green lineages. Front Plant Sci 5:1–17Google Scholar
  52. Kolukisaoglu Ü, Weinl S, Blazevic D, Batistic O, Kudla J (2004) Calcium sensors and their interacting protein kinases: genomics of the Arabidopsis and rice CBL–CIPK signaling networks. Plant Physiol 134:43–58PubMedCentralPubMedGoogle Scholar
  53. Krouk G, Crawford NM, Coruzzi GM, Tsay Y-F (2010) Nitrate signaling: adaptation to fluctuating environments. Curr Opin Plant Biol 13:266–273PubMedGoogle Scholar
  54. Kushwaha HR, Kumar G, Verma PK, Singla-Pareek SL, Pareek A (2011) Analysis of a salinity induced BjSOS3 protein from Brassica indicate it to be structurally and functionally related to its ortholog from Arabidopsis. Plant Physiol Biochem 49:996–1004PubMedGoogle Scholar
  55. Lacombe B, Pilot G, Michard E, Gaymard F, Sentenac H, Thibaud JB (2000) A shaker-like K+ channel with weak rectification is expressed in both source and sink phloem tissues of Arabidopsis. Plant Cell 12:837–851PubMedCentralPubMedGoogle Scholar
  56. Lagarde D, Basset M, Lepetit M, Conejero G, Gaymard F, Astruc S, Grignon C (1996) Tissue-specific expression of Arabidopsis AKT1 gene is consistent with a role in K+ nutrition. Plant J 9:195–203PubMedGoogle Scholar
  57. Lee SC, Lan W-Z, Kim B-G, Li L, Cheong YH, Pandey GK, Lu G, Buchanan BB, Luan S (2007) A protein phosphorylation/dephosphorylation network regulates a plant potassium channel. Proc Natl Acad Sci USA 104:15959–15964PubMedCentralPubMedGoogle Scholar
  58. Li L, Kim B-G, Cheong YH, Pandey GK, Luan S (2006) A Ca2+ signaling pathway regulates a K+ channel for low-K response in Arabidopsis. Proc Natl Acad Sci USA 103:12625–12630PubMedCentralPubMedGoogle Scholar
  59. Li D, Song S, Xia X, Yin W (2012a) Two CBL genes from Populus euphratica confer multiple stress tolerance in transgenic triploid white poplar. Plant Cell Tissue Organ Cult 109:477–489Google Scholar
  60. Li R, Zhang J, Wu G, Wang H, Chen Y, Wei J (2012b) HbCIPK2, a novel CBL-interacting protein kinase from halophyte Hordeum brevisubulatum, confers salt and osmotic stress tolerance. Plant Cell Environ 35:1582–1600PubMedGoogle Scholar
  61. Li Z-Y, Xu Z-S, He G-Y, Yang G-X, Chen M, Li L-C, Ma Y-Z (2012c) Overexpression of soybean GmCBL1 enhances abiotic stress tolerance and promotes hypocotyl elongation in Arabidopsis. Biochem Biophys Res Commun 427:731–736PubMedGoogle Scholar
  62. Li D-D, Xia X-L, Yin W-L, Zhang H-C (2013) Two poplar calcineurin B-like proteins confer enhanced tolerance to abiotic stresses in transgenic Arabidopsis thaliana. Biol Plant 57:70–78Google Scholar
  63. Li J, Long Y, Qi GN, Xu ZJ, Wu WH, Wang Y (2014a) The Os-AKT1 channel is critical for K+ uptake in rice roots and is modulated by the rice CBL1–CIPK23 complex. Plant Cell 26:3387–3402Google Scholar
  64. Li Q, Fan L, Luo Q, He H, Zhang J, Zeng Q, Li Y, Zhou W, Huang Z, Deng H, Qi Y (2014b) Co-overexpression of AtCBL9, AtCIPK23 and AtAKT1 enhances K+ uptake of sugarcane under low-K+ stress. Plant Omics 7:188–194Google Scholar
  65. Liu J, Zhu J (1997) An Arabidopsis mutant that requires increased calcium for potassium nutrition and salt tolerance. Proc Natl Acad Sci USA 94:14960–14964PubMedCentralPubMedGoogle Scholar
  66. Liu K, Huang C, Tsay Y (1999) CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell 11:865–874PubMedCentralPubMedGoogle Scholar
  67. Liu L-L, Ren H-M, Chen L-Q, Wang Y, Wu W-H (2013) A protein kinase, calcineurin B-like protein-interacting protein Kinase9, interacts with calcium sensor calcineurin B-like Protein3 and regulates potassium homeostasis under low-potassium stress in Arabidopsis. Plant Physiol 161:266–277PubMedCentralPubMedGoogle Scholar
  68. Luan S, Kudla J, Rodriguez-Concepcion M, Yalovsky S, Gruissem W (2002) Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. Plant Cell 14:S389–S400PubMedCentralPubMedGoogle Scholar
  69. Lv F, Zhang H, Xia X, Yin W (2014) Expression profiling and functional characterization of a CBL-interacting protein kinase gene from Populus euphratica. Plant Cell Rep 33:807–818PubMedGoogle Scholar
  70. Lyzenga WJ, Liu H, Schofield A, Muise-Hennessey A, Stone SL (2013) Arabidopsis CIPK26 interacts with KEG, components of the ABA signalling network and is degraded by the ubiquitin-proteasome system. J Exp Bot 64:2779–2791PubMedCentralPubMedGoogle Scholar
  71. Ma D-M, Xu W-R, Li H-W, Jin F-X, Guo L-N, Wang J, Dai H-J, Xu X (2014) Co-expression of the Arabidopsis SOS genes enhances salt tolerance in transgenic tall fescue (Festuca arundinacea Schreb.). Protoplasma 251:219–231PubMedCentralPubMedGoogle Scholar
  72. Maierhofer T, Diekmann M, Offenborn JN, Lind C, Bauer H, Hashimoto K, Al-Rasheid KAS, Luan S, Kudla J, Geiger D, Hedrich R (2014) Site-and kinase-specific phosphorylation-mediated activation of SLAC1, a guard cell anion channel stimulated by abscisic acid. Sci Signal 7:1–12Google Scholar
  73. Martínez-Atienza J, Jiang X, Garciadeblas B, Mendoza I, Zhu J-K, Pardo JM, Quintero FJ (2007) Conservation of the salt overly sensitive pathway in rice. Plant Physiol 143:1001–1012PubMedCentralPubMedGoogle Scholar
  74. Munns R, Schachtman D, Condon A (1995) The significance of a two-phase growth response to salinity in wheat and barley. Funct Plant Biol 22:561–569Google Scholar
  75. Nieves-Cordones M, Caballero F, Martínez V, Rubio F (2012) Disruption of the Arabidopsis thaliana inward-rectifier K+ channel AKT1 improves plant responses to water stress. Plant Cell Physiol 53:423–432PubMedGoogle Scholar
  76. Ohta M, Guo Y, Halfter U, Zhu J-K (2003) A novel domain in the protein kinase SOS2 mediates interaction with the protein phosphatase 2C ABI2. Proc Natl Acad Sci USA 100:11771–11776PubMedCentralPubMedGoogle Scholar
  77. Olías R, Eljakaoui Z, Li J, De Morales PA, Marín-Manzano MC, Pardo JM, Belver A (2009) The plasma membrane Na+/H+ antiporter SOS1 is essential for salt tolerance in tomato and affects the partitioning of Na+ between plant organs. Plant Cell Environ 32:904–916PubMedGoogle Scholar
  78. Pandey GK, Cheong H, Kim K, Grant JJ, Li L, Hung W, Angelo CD, Weinl S, Kudla J, Luan S (2004) The calcium sensor calcineurin B-like 9 modulates abscisic acid sensitivity and biosynthesis in Arabidopsis. Plant Cell 16:1912–1924PubMedCentralPubMedGoogle Scholar
  79. Pandey GK, Cheong YH, Kim B-G, Grant JJ, Li L, Luan S (2007) CIPK9: a calcium sensor-interacting protein kinase required for low-potassium tolerance in Arabidopsis. Cell Res 17:411–421PubMedGoogle Scholar
  80. Pandey GK, Grant JJ, Cheong YH, Kim B-G, Li LG, Luan S (2008) Calcineurin B-like protein CBL9 interacts with target kinase CIPK3 in the regulation of ABA response in seed germination. Mol Plant 1:238–248PubMedGoogle Scholar
  81. Pilot G, Gaymard F, Mouline K, Chérel I, Sentenac H (2003) Regulated expression of Arabidopsis shaker K+ channel genes involved in K+ uptake and distribution in the plant. Plant Mol Biol 51:773–787PubMedGoogle Scholar
  82. Qiu Q-S, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci USA 99:8436–8441PubMedCentralPubMedGoogle Scholar
  83. Qiu Q-S, Guo Y, Quintero FJ, Pardo JM, Schumaker KS, Zhu J-K (2004) Regulation of vacuolar Na+/H+ exchange in Arabidopsis thaliana by the salt-overly-sensitive (SOS) pathway. J Biol Chem 279:207–215PubMedGoogle Scholar
  84. Quan R, Lin H, Mendoza I, Zhang Y, Cao W, Yang Y, Shang M, Chen S, Pardo JM, Guo Y (2007) SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant Cell 19:1415–1431PubMedCentralPubMedGoogle Scholar
  85. Quintero FJ, Ohta M, Shi H, Zhu J-K, Pardo JM (2002) Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis. Proc Natl Acad Sci USA 99:9061–9066PubMedCentralPubMedGoogle Scholar
  86. Rao X-L, Zhang X-H, Li R-J, Shi H-T, Lu Y-T (2011) A calcium sensor-interacting protein kinase negatively regulates salt stress tolerance in rice (Oryza sativa). Funct Plant Biol 38:441–450Google Scholar
  87. Reddy AR, Chaitanya KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161:1189–1202Google Scholar
  88. Ren X-L, Qi G-N, Feng H-Q, Zhao S, Zhao S-S, Wang Y, Wu W-H (2013) Calcineurin B-like protein CBL10 directly interacts with AKT1 and modulates K+ homeostasis in Arabidopsis. Plant J 74:258–266PubMedGoogle Scholar
  89. Rivandi J, Miyazaki J, Hrmova M, Pallotta M, Tester M, Collins NC (2011) A SOS3 homologue maps to HvNax4, a barley locus controlling an environmentally sensitive Na+ exclusion trait. J Exp Bot 62:1201–1216PubMedCentralPubMedGoogle Scholar
  90. Roy SJ, Huang W, Wang XJ, Evrard A, Schmöckel SM, Zafar ZU, Tester M (2013) A novel protein kinase involved in Na+ exclusion revealed from positional cloning. Plant Cell Environ 36:553–568PubMedGoogle Scholar
  91. Rudd J, Franklin-Tong V (2001) Unravelling response-specificity in Ca2+ signalling pathways in plant cells. New Phytol 151:7–33Google Scholar
  92. Saadia M, Jamil A, Ashraf M, Akram NA (2013) Comparative study of SOS2 and a novel PMP3-1 gene expression in two sunflower (Helianthus annuus L.) lines differing in salt tolerance. Appl Biochem Biotechnol 170:980–987PubMedGoogle Scholar
  93. Sairam R, Rao K, Srivastava G (2002) Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Sci 163:1037–1046Google Scholar
  94. Sanders D, Brownlee C, Harper J (1999) Communicating with calcium. Plant Cell 11:691–706PubMedCentralPubMedGoogle Scholar
  95. Sanders D, Pelloux J, Brownlee C, Harper JH (2002) Calcium at the crossroads of signaling. Plant Cell 14:401–418Google Scholar
  96. Sandmann M, Skłodowski K, Gajdanowicz P, Michard E, Rocha M, Gomez-Porras JL, González W, Corrêa LGG, Ramírez-Aguilar SJ, Cuin TA, van Dongen JT, Thibaud J-B, Dreyer I (2011) The K+ battery-regulating Arabidopsis K+ channel AKT2 is under the control of multiple post-translational steps. Plant Signal Behav 6:558–562PubMedCentralPubMedGoogle Scholar
  97. Schroeder JI, Ward JM, Gassmann W (1994) Perspectives on the physiology and structure of inward-rectifying K+ channels in higher plants: biophysical implications for K+ uptake. Annu Rev Biophys Biomol Struct 23:441–471PubMedGoogle Scholar
  98. Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA 97:6896–6901PubMedCentralPubMedGoogle Scholar
  99. Shi H, Lee B, Wu S, Zhu J (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol 21:81–87PubMedGoogle Scholar
  100. Sun Z, Qi X, Li P, Wu C, Zhao Y, Zhang H, Wang Z (2008) Overexpression of a Thellungiella halophila CBL9 homolog, ThCBL9, confers salt and osmotic tolerances in transgenic Arabidopsis thaliana. J Plant Biol 51:25–34Google Scholar
  101. Szyroki A, Ivashikina N, Dietrich P, Roelfsema M, Ache P, Reintanz B, Deeken R, Godde M, Felle H, Steinmeyer R, Palme K, Hedrich R (2001) KAT1 is not essential for stomatal opening. Proc Natl Acad Sci USA 98:2917–2921PubMedCentralPubMedGoogle Scholar
  102. Tang R-J, Liu H, Bao Y, Lv Q-D, Yang L, Zhang H-X (2010) The woody plant poplar has a functionally conserved salt overly sensitive pathway in response to salinity stress. Plant Mol Biol 74:367–380PubMedGoogle Scholar
  103. Tang R-J, Liu H, Yang Y, Yang L, Gao X-S, Garcia VJ, Luan S, Zhang H-X (2012) Tonoplast calcium sensors CBL2 and CBL3 control plant growth and ion homeostasis through regulating V-ATPase activity in Arabidopsis. Cell Res 22:1650–1665PubMedCentralPubMedGoogle Scholar
  104. Tang R-J, Yang Y, Yang L, Liu H, Wang C-T, Yu M-M, Gao X-S, Zhang H-X (2014) Poplar calcineurin B-like proteins PtCBL10A and PtCBL10B regulate shoot salt tolerance through interaction with PtSOS2 in the vacuolar membrane. Plant Cell Environ 37:573–588PubMedGoogle Scholar
  105. Tripathi V, Parasuraman B, Laxmi A, Chattopadhyay D (2009) CIPK6: a CBL-interacting protein kinase is required for development and salt tolerance in plants. Plant J 58:778–790PubMedGoogle Scholar
  106. Wang M, Gu D, Liu T, Wang Z, Guo X, Hou W, Bai Y, Chen X, Wang G (2007) Overexpression of a putative maize calcineurin B-like protein in Arabidopsis confers salt tolerance. Plant Mol Biol 65:733–746PubMedGoogle Scholar
  107. Wang X, Li J, Zou X, Lu L, Li L, Ni S, Liu F (2010) Ectopic expression of AtCIPK23 enhances tolerance against low-K+ stress in transgenic potato. Am J Potato Res 88:153–159Google Scholar
  108. Wang R-K, Li L-L, Cao Z-H, Zhao Q, Li M, Zhang L-Y, Hao Y-J (2012) Molecular cloning and functional characterization of a novel apple MdCIPK6L gene reveals its involvement in multiple abiotic stress tolerance in transgenic plants. Plant Mol Biol 79:123–135PubMedGoogle Scholar
  109. Weinl S, Kudla J (2009) The CBL–CIPK Ca2+-decoding signaling network: function and perspectives. New Phytol 184:517–528PubMedGoogle Scholar
  110. Wu SJ, Ding L, Zhu JK (1996) SOS1: a genetic locus essential for salt tolerance and potassium acquisition. Plant Cell 8:617–627PubMedCentralPubMedGoogle Scholar
  111. Wu Y, Ding N, Zhao X, Zhao M, Chang Z, Liu J, Zhang L (2007) Molecular characterization of PeSOS1: the putative Na+/H+ antiporter of Populus euphratica. Plant Mol Biol 65:1–11PubMedGoogle Scholar
  112. Xiang Y, Huang Y, Xiong L (2007) Characterization of stress-responsive CIPK genes in rice for stress tolerance improvement. Plant Physiol 144:1416–1428PubMedCentralPubMedGoogle Scholar
  113. Xiao B-Z, Chen X, Xiang C-B, Tang N, Zhang Q-F, Xiong L-Z (2009) Evaluation of seven function-known candidate genes for their effects on improving drought resistance of transgenic rice under field conditions. Mol Plant 2:73–83PubMedCentralPubMedGoogle Scholar
  114. Xu J, Li H-D, Chen L-Q, Wang Y, Liu L-L, He L, Wu W-H (2006) A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125:1347–1360PubMedGoogle Scholar
  115. Yang Q, Chen Z-Z, Zhou X-F, Yin H-B, Li X, Xin X-F, Hong X-H, Zhu J-K, Gong Z (2009) Overexpression of SOS (Salt Overly Sensitive) genes increases salt tolerance in transgenic Arabidopsis. Mol Plant 2:22–31PubMedCentralPubMedGoogle Scholar
  116. Ye C-Y, Xia X, Yin W (2013a) Evolutionary analysis of CBL-interacting protein kinase gene family in plants. Plant Growth Regul 71:49–56Google Scholar
  117. Ye J, Zhang W, Guo Y (2013b) Arabidopsis SOS3 plays an important role in salt tolerance by mediating calcium-dependent microfilament reorganization. Plant Cell Rep 32:139–148PubMedGoogle Scholar
  118. Zeng L, Shannon M (2000) Salinity effects on seedling growth and yield components of rice. Crop Sci 40:996–1003Google Scholar
  119. Zhang H, Yin W, Xia X (2008) Calcineurin B-Like family in Populus: comparative genome analysis and expression pattern under cold, drought and salt stress treatment. Plant Growth Regul 56:129–140Google Scholar
  120. Zhang H, Lv F, Han X, Xia X, Yin W (2013) The calcium sensor PeCBL1, interacting with PeCIPK24/25 and PeCIPK26, regulates Na+/K+ homeostasis in Populus euphratica. Plant Cell Rep 32:611–621PubMedGoogle Scholar
  121. Zhang H, Yang B, Liu W-Z, Li H, Wang L, Wang B, Deng M, Liang W, Deyholos MK, Jiang Y-Q (2014) Identification and characterization of CBL and CIPK gene families in canola (Brassica napus L.). BMC Plant Biol 14:8Google Scholar
  122. Zhao D, Oosterhuis D, Bednarz C (2001) Influence of potassium deficiency on photosynthesis, chlorophyll content and chloroplast ultrastructure of cotton plants. Photosynthetica 39:103–109Google Scholar
  123. Zhao J, Sun Z, Zheng J, Guo X, Dong Z, Huai J, Gou M, He J, Jin Y, Wang J, Wang G (2009) Cloning and characterization of a novel CBL-interacting protein kinase from maize. Plant Mol Biol 69:661–674PubMedGoogle Scholar
  124. Zhou J, Wang J, Bi Y, Wang L, Tang L, Yu X, Ohtani M, Demura T, Zhuge Q (2014) Overexpression of PtSOS2 enhances salt tolerance in transgenic poplars. Plant Mol Biol Report 32:185–197PubMedCentralPubMedGoogle Scholar
  125. Zhu JK, Liu J, Xiong L (1998) Genetic analysis of salt tolerance in Arabidopsis: evidence for a critical role of potassium nutrition. Plant Cell 10:1181–1191PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Emily Laurina Thoday-Kennedy
    • 1
    • 2
  • Andrew Keith Jacobs
    • 1
    • 3
  • Stuart John Roy
    • 1
    • 2
  1. 1.Australian Centre for Plant Functional GenomicsUniversity of AdelaideGlen OsmondAustralia
  2. 2.The School of Agriculture Food and WineUniversity of AdelaideGlen OsmondAustralia
  3. 3.ITEK Ventures Pty LtdUniversity of South AustraliaMawson LakesAustralia

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