Role of Calcium-Mediated CBL–CIPK Network in Plant Mineral Nutrition and Abiotic Stress

  • Indu Tokas
  • Amita Pandey
  • Girdhar K. Pandey


In plants like other organisms, nutrition plays a vital role in biological processes such as growth, development and reproduction. Extensive studies done in the field of plant nutrition signalling using Arabidopsis thaliana as a model system have unravelled the calcium-mediated regulation of various ion transporters and channels involved in mineral nutrient acquisition and assimilation. Unlike animals, the immobile nature of plants makes them more vulnerable to the unavoidable environmental conditions in which they grow and are exposed to numerous biotic as well as abiotic stresses. Nutrition deprivation severely affects soil productivity, crop yield, and quality and stress resistance. So, a rapid and efficient signalling mechanism in response to disturbances in nutrient levels is crucial for the survival of organisms from bacteria to humans. Plants have, therefore, evolved a host of molecular pathways that can sense nutrient concentrations, both intracellular and extracellular, and quickly regulate gene expression and protein modifications to respond to any such changes. Ion channels and transporters present in the plasma membrane aid in acquisition of these nutrients. Nutrient deprivation acts as a trigger for the activation of calcium-mediated CBL–CIPK complex signalling pathways that integrate adaptive responses in plants. Several members of CBL–CIPK family such as CBL1, CBL9, CIPK6, CIPK8, CIPK16 and CIPK23 work in combination in multiple nutrient-sensing pathways to confer specific responses during uptake and transport of minerals especially nitrate and potassium. The regulatory circuit of these ion channels and transporters involves multiple post-translational modifications like phosphorylation by CBL–CIPK complex, which modulates the nutrient uptake properties in response to changes in soil nutrient concentration. This chapter concisely discusses the imperative role of newly identified CBL–CIPK members as crucial components of potassium- and nitrate-sensing mechanisms during nutrition uptake, allocation and signalling.


Xenopus Oocyte Nitrate Uptake Potassium Uptake Nitrate Transporter Calcium Sensor 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Research in GKP’s lab is supported by funding from Department of Biotechnology (DBT), Department of Science and Technology (DST), India. IT acknowledges Council for Scientific and Industrial Research (CSIR), India, for her research fellowship.


  1. Aguera E, Haba P, Fontes AG, Maldonado JM (1990) Nitrate and nitrite uptake and reduction in intact sunflower. Planta 182:149–154CrossRefGoogle Scholar
  2. Ahn SJ, Shin R, Schachtman DP (2004) Expression of KT/KUP genes in Arabidopsis and the role of root hairs in K+ uptake. Plant Physiol 134:1135–1145PubMedCrossRefGoogle Scholar
  3. Anderson JA, Huprikar SS, Kochian LV, Lucas WJ, Gaber RF (1992) Functional expression of a probable Arabidopsis thaliana potassium channel in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 89:3736–3740PubMedCrossRefGoogle Scholar
  4. Armengaud P, Breitling R, Amtmann A (2004) The potassium dependent transcriptome of Arabidopsis reveals a prominent role of jasmonic acid in nutrient signalling. Plant Physiol 136:2556–2576PubMedCrossRefGoogle Scholar
  5. Arnon DI, Stout PR (1939) Molybdenum as an essential element for higher plants. Plant Physiol 14:599–602PubMedCrossRefGoogle Scholar
  6. Ashley MK, Grant M, Grabov A (2006) Plant responses to potassium deficiencies: a role for potassium transport proteins. J Exp Bot 57:425–436PubMedCrossRefGoogle Scholar
  7. Aslam M, HuVaker RC, Rains DW (1984) Early effects of salinity on nitrate assimilation in barley seedlings. Plant Physiol 76:321–325PubMedCrossRefGoogle Scholar
  8. Aslam M, Travis RL, HuVaker RC (1992) Comparative kinetics and reciprocal inhibition of uninduced and induced barley (Hordeum vulgare L.) seedlings. Plant Physiol 99:1124–1133PubMedCrossRefGoogle Scholar
  9. Batistic O, Kudla J (2004) Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK protein kinase network. Planta 219:915–924PubMedCrossRefGoogle Scholar
  10. Batistič O, Kudla J (2012) Analysis of calcium signaling pathways in plants. Biochim Biophys Acta 1820:1283–1293PubMedCrossRefGoogle Scholar
  11. Berger H, Pachlinger R, Morozov I, Goller S, Narendja F, Caddick M, Strauss J (2006) The GATA factor AreA regulates localization and in vivo binding site occupancy of the nitrate activator NirA. Mol Microbiol 59:433–446PubMedCrossRefGoogle Scholar
  12. Burger G, Tilburn J, Scazzocchio C (1991) Molecular cloning and functional characterization of the pathway-specific regulatory gene nirA, which controls nitrate assimilation in Aspergillus nidulans. Mol Cell Biol 11(2):795–802PubMedGoogle Scholar
  13. Bernreiter A, Ramon A, Fernandez-Martinez J, Berger H, Araujo-Bazan L, Espeso EA, Pachlinger R, Gallmetzer A, Anderl I, Scazzocchio C, Strauss J (2007) Nuclear export of the transcription factor NirA is a regulatory checkpoint for nitrate induction in Aspergillus nidulans. Mol Cell Biol 27:791–802PubMedCrossRefGoogle Scholar
  14. Blatt MR (2000) Cellular signaling and volume control in stomatal movements of plants. Annu Rev Cell Dev Biol 16:221–241PubMedCrossRefGoogle Scholar
  15. Cavicchioli R, Chiang RC, Kalman LV, Gunsalus RP (1996) Role of the periplasmic domain of the Escherichia coli NarX sensor-transmitter protein in nitrate-dependent signal transduction and gene regulation. Mol Microbiol 21:901–911PubMedCrossRefGoogle Scholar
  16. Chen YF, Wang Y, Wu WH (2008) Membrane transporters for nitrogen, phosphate and potassium uptake in plants. J Integr Plant Biol 50:835–848PubMedCrossRefGoogle Scholar
  17. Cheong YH, Pandey GK, Grant JJ, Batistic O, Li L, Kim BG, Lee SC, Kudla J, Luan S (2007) Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate. Plant J 52:223–239PubMedCrossRefGoogle Scholar
  18. Cherel I (2004) Regulation of K+ channel activities in plants: from physiological to molecular aspects. J Exp Bot 55:337–351PubMedCrossRefGoogle Scholar
  19. Chiang RC, Cavicchioli R, Gunsalus RP (1997) ‘Locked-on’ and ‘locked-off’ signal transduction mutations in the periplasmic domain of the Escherichia coli NarQ and NarX sensors affect nitrate- and nitrite-dependent regulation by NarL and NarP. Mol Microbiol 24:1049–1060PubMedCrossRefGoogle Scholar
  20. Coruzzi GM, Bush DR (2001) Nitrogen and carbon nutrient and metabolite signaling in plants. Plant Physiol 125:61–64PubMedCrossRefGoogle Scholar
  21. Crawford NM (1995) Nitrate: nutrient and signal for plant growth. Plant Cell 7:859–868PubMedGoogle Scholar
  22. Crawford NM, Glass ADM (1998) Molecular and physiological aspects of nitrate uptake in plants. Trends Plant Sci 3:389–395CrossRefGoogle Scholar
  23. Czempinski K, Gaedeke N, Zimmermann S, MuellerRoeber B (1999) Molecular mechanisms and regulation of plant ion channels. J Exp Bot 50:955–966Google Scholar
  24. Czempinski K, Frachisse JM, Maurel C, Barbier-Brygoo H, Mu¨ller-Ro¨ber B (2002) Vacuolar membrane localization of the Arabidopsis ‘two-pore’ K+channel KCO1. Plant J 29:809–820PubMedCrossRefGoogle Scholar
  25. Dang J, Harvey D, Jobbagy A, Grady C Jr (1989) Evaluation of biodegradation kinetic with respirometric data. Res J Water Pollut Control Federation 61:1711–1721Google Scholar
  26. De Angeli A, Monachello D, Ephritikhine G, Frachisse JM, Thomine S, Gambale F, Barbier-Brygoo H (2006) The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature 442:939–942PubMedCrossRefGoogle Scholar
  27. De Angeli A, Moran O, Wege S, Filleur S, Ephritikhine G, Thomine S, BarbierBrygoo H, Gambale F (2009) ATP binding to the C terminus of the Arabidopsis thaliana nitrate/proton antiporter, AtCLCa, regulates nitrate transport into plant vacuoles. J Biol Chem 284:26526–26532PubMedCrossRefGoogle Scholar
  28. Dechorgnat J, Nguyen CT, Armengaud P, Jossier M, Diatloff E, Filleur S, Daniel-Vedele F (2011) From the soil to the seeds: the long journey of nitrate in plants. J Exp Bot 62:1349–1359PubMedCrossRefGoogle Scholar
  29. Doddema H, Telkamp GP (1979) Uptake of nitrate by mutants of Arabidopsis thaliana disturbed in uptake or reduction of nitrate. II. Kinetics. Physiol Plant 45:332–338CrossRefGoogle Scholar
  30. Epstein E (1972) In: Epstein E (ed) Mineral nutrition of plants: principles and perspectives. Wiley, New York, pp 325–344Google Scholar
  31. Epstein E (1973) Mechanisms of ion transport through plant cell membranes. Int Rev Cytol 34:123–167CrossRefGoogle Scholar
  32. Esser JE, Liao YJ, Schroeder JI (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 mastoparans. J Exp Bot 48:539–550PubMedCrossRefGoogle Scholar
  33. Evans NH, McAinsh MR, Hetherington AM (2001) Calcium oscillations in higher plants. Curr Opin Plant Biol 4:415–420PubMedCrossRefGoogle Scholar
  34. Evans AM, Mustard KJ, Wyatt CN, Peers C, Dipp M, Kumar P, Kinnear NP, Hardie DG (2005) Does AMP-activated protein kinase couple inhibition of mitochondrial oxidative phosphorylation by hypoxia to calcium signaling in O2-sensing cells? J Biol Chem 280:41504–41511PubMedCrossRefGoogle Scholar
  35. Fan L-M, Zhao Z, Assmann SM (2004) Guard cells: a dynamic signalling model. Curr Opin Plant Biol 7:537–546PubMedCrossRefGoogle Scholar
  36. Forde BG (2000) Nitrate transporters in plants: structure, function and regulation. Biochem Biophys Acta 1465:219–235PubMedCrossRefGoogle Scholar
  37. Forde BG, Clarkson DT (1999) Nitrate and ammonium nutrition of plants: physiological and molecular perspectives. Adv Bot Res 30:1–90CrossRefGoogle Scholar
  38. Forde BG, Lorenzo H (2001) The nutritional control of root development. Plant Soil 232:57–68CrossRefGoogle Scholar
  39. Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JDG et al (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446PubMedCrossRefGoogle Scholar
  40. Fu Y-H, Kneesi JY, Marzluf GA (1989) Isolation of ni t -4, the minor nitrogen regulatory gene which mediates nitrate induction in Neurospora crassa. J Bacteriol 171:4067–4070PubMedGoogle Scholar
  41. Gaymard F, Pilot G, Lacombe B, Bouchez D, Bruneau D, Boucherez J, Michaux-Ferriere N, Thibaud JB, Sentenac H (1998) Identification and disruption of a plant shaker-like outward channel involved in K+ release into the xylem sap. Cell 94:647–655PubMedCrossRefGoogle Scholar
  42. Geiger D, Scherzer S, Mumm P, Stange A, Marten I, Bauer H, Ache P, Matschi S, Liese A, Al-Rasheid KA, Romeis T, Hedrich R (2009) Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc Natl Acad Sci USA 106:21425–21430PubMedCrossRefGoogle Scholar
  43. Gierth M, Maser P (2007) Potassium transporters in plants–Involvement in K+ acquisition, redistribution and homeostasis. FEBS Lett 581:2348–2356PubMedCrossRefGoogle Scholar
  44. Gierth M, Maser P, Schroeder JI (2005) 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 137:1105–1114PubMedCrossRefGoogle Scholar
  45. Gowri G, Kenis JD, Ingemarsson B, Redinbaugh MG, Campbell WH (1992) Nitrate reductase transcript is expressed in the primary response of maize to environmental nitrate. Plant Mol Biol 18:55–64PubMedCrossRefGoogle Scholar
  46. Guo FQ et al (2001) The Arabidopsis dual-affinity nitrate transporter gene AtNRT1.1 (CHL1) is activated and functions in nascent organ development during vegetative and reproductive growth. Plant Cell 13:1761–1777PubMedGoogle Scholar
  47. Hamilton DW, Hills A, Kohler B, Blatt MR (2000) Ca2+ channels at the plasma membrane of stomatal guard cells are activated by hyperpolarization and abscisic acid. Proc Natl Acad Sci USA 97:4967–4972PubMedCrossRefGoogle Scholar
  48. Harmon AC, Gribskov M, Harper JF (2000) CDPKs. A kinase for every Ca2+ signal? Trends Plant Sci 5:154–159PubMedCrossRefGoogle Scholar
  49. Hashimoto K, Eckert C, Anschuetz U, Scholz M, Held K, Waadt R, Reyer A et al (2012) Phosphorylation of Calcineurin B-like (CBL) calcium sensor proteins by their CBL-interacting protein kinases (CIPKs) is required for full activity of CBL-CIPK complexes towards their target proteins. J Biol Chem 287:7956–7968PubMedCrossRefGoogle Scholar
  50. Hedrich R, Kudla J (2006) Calcium signaling networks channel plant K+ uptake. Cell 125:1221–1223PubMedCrossRefGoogle Scholar
  51. Held K, Pascaud F, Eckert C, Gajdanowicz P, Hashimoto K, Corratgé-Faillie C, Offenborn JN et al (2011) Calcium-dependent modulation and plasma membrane targeting of the AKT2 potassium channel by the CBL4/CIPK6 calcium sensor/protein kinase complex. Cell Res 21:1116–1130PubMedCrossRefGoogle Scholar
  52. Ho C-H, Tsay YF (2011) Nitrate, ammonium, and potassium sensing and signaling. Curr Opin Plant Biol 13:604–610CrossRefGoogle Scholar
  53. Ho CH, Lin SH, Hu HC, Tsay YF (2009) CHL1 functions as a nitrate sensor in plants. Cell 138:1184–1194PubMedCrossRefGoogle Scholar
  54. Hole DJ, Emran AM, Fares Y, Drew MC (1990) Induction of nitrate transport in maize roots, and kinetics of influx, measured with nitrogen-13. Plant Physiol 93:642–647PubMedCrossRefGoogle Scholar
  55. Hosy E, Vavasseur A, Mouline K, Dreyer I, Gaymard F, Poree F, Boucherez J, Lebaudy A, Bouchez D, Very AA et al (2003) The Arabidopsis outward K+ channel GORK is involved in regulation of stomatal movements and plant transpiration. Proc Natl Acad Sci USA 100:5549–5554PubMedCrossRefGoogle Scholar
  56. Hu HC, Wang YY, Tsay YF (2009) AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. Plant J 57:264–278PubMedCrossRefGoogle Scholar
  57. Huang NC et al (1999) Cloning and functional characterization of an Arabidopsis nitrate transporter gene that encodes a constitutive component of low-affinity uptake. Plant Cell 11:1381–1392PubMedGoogle Scholar
  58. Hundal HS, Taylor PM (2009) Amino acid transceptors: gate keepers of nutrient exchange and regulators of nutrient signalling. Am J Physiol Endocrinol Metab 296:E603–E613PubMedCrossRefGoogle Scholar
  59. Jackson RB, Caldwell MM (1993) The scale of nutrient heterogeneity around individual plants and its qualification with geostatistics. Ecology 74:612–614CrossRefGoogle Scholar
  60. Kim EJ, Kwak JM, Uozumi N, Schroeder JI (1998) AtKUP1: an Arabidopsis gene encoding high-affinity potassium transport activity. Plant Cell 10:51–62PubMedGoogle Scholar
  61. Kim MJ, Ciani S, Schachtman DP (2010) A peroxidase contributes to ROS production during Arabidopsis root response to potassium deficiency. Mol Plant 3:420–427PubMedCrossRefGoogle Scholar
  62. Kim TH, Böhmer M, Hu H, Nishimura N, Schroeder JI (2010) Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu Rev Plant Biol 61:561–591PubMedCrossRefGoogle Scholar
  63. Kwak JM, Mori I, Pei Z-M, Leonhardt N, Torres MA, Dangl JL, Bloom R, Bodde S, Jones JDG, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633PubMedCrossRefGoogle Scholar
  64. Laegreid M, Bockman OC, Kaarstad O (1999) Agriculture, fertilizers and the environment. CABI (CABI Publishing in association with Norsk Hydro ASA), Oxon, UK, 294 ppGoogle Scholar
  65. Lan WZ, Lee SC, Che YF, Jiang YQ, Luan S (2011) Mechanistic analysis of AKT1regulation by the CBL-CIPK-PP2CA interactions. Mol Plant 4:527–536PubMedCrossRefGoogle Scholar
  66. Larsson CM, Ingemarsson B (1989) Molecular aspects of nitrate uptake in higher plants. In: Wray J, Kinghorn J (eds) Molecular and genetic aspects of nitrate assimilation. Oxford University Press, Oxford, pp 3–24Google Scholar
  67. Lebaudy A, Ve’ry AA, Sentenac H (2007) K+ channel activity in plants: genes, regulations and functions. FEBS Lett 581:2357–2366PubMedCrossRefGoogle Scholar
  68. Leckie CP, McAinsh MR, Montgomery L, Priestley AJ, Staxen I, Webb AAR, Hetherington AM (1998) Second messengers in guard cells. J Exp Bot 49:339–349Google Scholar
  69. Lee SC, Lan WZ, Kim BG, 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 104:15959–15964PubMedCrossRefGoogle Scholar
  70. Lee SC, Lan W, Buchanan BB, Luan S (2009) A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. Proc Natl Acad Sci USA 106(50):21419–21424PubMedCrossRefGoogle Scholar
  71. Leigh RA, Jones RGW (1984) A hypothesis relating critical potassium concentrations for growth to the distribution and functions of this ion in the plant-cell. New Phytol 97:1–13CrossRefGoogle Scholar
  72. Lejay L, Tillard P, Lepetit M, Olive F, Filleur S et al (1999) Molecular and functional regulation of two NO3− uptake systems by N- and C-status of Arabidopsis plants. Plant J 18:509–519PubMedCrossRefGoogle Scholar
  73. Li L, Kim BG, Cheong YH, Pandey GK, Luan S (2006) A Ca(2)+ signaling pathway regulates a K(+) channel for low-K response in Arabidopsis. Proc Natl Acad Sci USA 103:12625–12630PubMedCrossRefGoogle Scholar
  74. Li W, Wang Y, Okamoto M, Nigel M, Crawford NM, Siddiqui MY, Glass ADM (2007) Dissection of the AtNRT2.1:AtNRT2.2 inducible high-affinity nitrate transporter gene cluster. Plant Physiol 143:425–433PubMedCrossRefGoogle Scholar
  75. Little DY et al (2005) The putative high-affinity nitrate transporter NRT2.1 represses lateral root initiation in response to nutritional cues. Proc Natl Acad Sci USA 102:13693–13698PubMedCrossRefGoogle Scholar
  76. Liu KH, Tsay YF (2003) Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO J 22:1005–1013PubMedCrossRefGoogle Scholar
  77. Liu KH, Huang CY, Tsay YF (1999) CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell 11:865–874PubMedGoogle Scholar
  78. Luan S (2009) The CBL–CIPK network in plant calcium signaling. Trends Plant Sci 14:37–42PubMedCrossRefGoogle Scholar
  79. 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(Suppl):S389–S400PubMedGoogle Scholar
  80. Luan S, Lan W, Chul Lee S (2009) Potassium nutrition, sodium toxicity, and calcium signaling: connections through the CBL–CIPK network. Curr Opin Plant Biol 12:339–346PubMedCrossRefGoogle Scholar
  81. MacRobbie EAC (1998) Signal transduction and ion channels in guard cells. Philos Trans R Soc Lond B Biol Sci 353:1475–1488PubMedCrossRefGoogle Scholar
  82. Marschner H (1995) Functions of mineral nutrients: macronutirents. In: Mineral nutrition of higher plants, 2nd edn. Academic, New York, pp 299–312Google Scholar
  83. McAinsh MR, Clayton H, Mans®eld TA, Hetherington AM (1996) Changes in stomatal behavior and guard cell cytosolic free calcium in response to oxidative stress. Plant Physiol 111:1031–1042PubMedGoogle Scholar
  84. Miller AJ, Fan X, Orsel M, Smith SJ, Wells DM (2007) Nitrate transport and signalling. J Exp Bot 58:2297–2306PubMedCrossRefGoogle Scholar
  85. Munos S, Cazettes C, Fizames C, Gaymard F, Tillard P, Lepetit M, Lejay L, Gojon A (2004) Transcript profiling in the chl1-5 mutant of Arabidopsis reveals a role of the nitrate transporter NRT1.1 in the regulation of another nitrate transporter, NRT2.1. Plant Cell 16:2433–2447PubMedCrossRefGoogle Scholar
  86. Pandey GK (2008) Emergence of a novel calcium signalling pathway in plants: CBL-CIPK signaling network. Physiol Mol Biol Plants 14:51–68CrossRefGoogle Scholar
  87. Pandey GK, Cheong YH, Kim BG, Grant JJ, Li L, Luan S (2007) CIPK9: a calcium sensor-interacting protein kinase required for low-potassium tolerance in Arabidopsis. Cell Res 17:411–421PubMedCrossRefGoogle Scholar
  88. Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signaling in guard cells. Nature 406:731–734PubMedCrossRefGoogle Scholar
  89. Peiter E, Maathuis FJM, Mills LN, Knight H, Pelloux M, Hetherington AM et al (2005) The vacuolar Ca2+ -activated channel TPC1 regulates germination and stomatal movement. Nature 434:404–408PubMedCrossRefGoogle Scholar
  90. Pilot G, Gaymard F, Mouline K, Cherel I, Sentenac H (2003) Regulated expression of Arabidopsis shaker K1 channel genes involved in K1 uptake and distribution in the plant. Plant Mol Biol 51:773–787PubMedCrossRefGoogle Scholar
  91. Pouteau S, Cherel I, Vaucheret H, Caboche M (1989) Nitrate reductase mRNA regulation in Nicotiana plumbaginifolia nitrate reductase–deficient mutants. Plant Cell 1:1111–1120PubMedGoogle Scholar
  92. Reddy VS, Ali GS, Reddy AS (2002) Genes encoding calmodulin-binding proteins in the Arabidopsis genome. J Biol Chem 277:9840–9852PubMedCrossRefGoogle Scholar
  93. Redinbaugh MG, Campbell WH (1991) Higher plant responses to environmental nitrate. Physiol Plant 82:640–650CrossRefGoogle Scholar
  94. Remans T, Nacry P, Pervent M, Filleur S, Diatloff E, Mounier E, Tillard P, Forde BG, Gojon A (2006) The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proc Natl Acad Sci USA 103:19206–19211PubMedCrossRefGoogle Scholar
  95. Roelfsema MR and Hedrich R (2010) Making sense out of Ca2+ signals: their role in regulating stomatal movements. Plant Cell Environ 33(3):305–21PubMedCrossRefGoogle Scholar
  96. Rubio F, Nieves-Cordones M, Aleman F, Martinez V (2008) Relative contribution of AtHAK5 and AtAKT1 to K+ uptake in the high-affinity range of concentrations. Physiol Plant 134:598–608PubMedCrossRefGoogle Scholar
  97. Santa-Maria GE, Rubio F, Dubcovsky J, Rodriguez-Navarro A (1997) The HAK1 gene of barley is a member of a large gene family and encodes a high-affinity potassium transporter. Plant Cell 9:2281–2289PubMedGoogle Scholar
  98. Schachtman DP (2000) Molecular insights into the structure and function of plant K+ transport mechanisms. Biochim Biophys Acta 1465(1–2):127–139PubMedGoogle Scholar
  99. Schachtman DP, Shin R (2007) Nutrient sensing and signalling: NPKS. Annu Rev Plant Biol 58:47–69PubMedCrossRefGoogle Scholar
  100. Scheible WR, Gonzalez Fontes A, Lauerer M, Muller Rober B, Caboche M, Stitt M (1997a) Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco. Plant Cell 9:783–798PubMedGoogle Scholar
  101. Scheible WR, Lauerer M, Schulze ED, Caboche M, Stitt M (1997b) Accumulation of nitrate in the shoot acts as a signal to regulate shoot root allocation in tobacco. Plant J 11:671–691CrossRefGoogle Scholar
  102. Schroeder JI (1988) K+ transport properties of K+ channels in plasma membrane of Vicia faba guard cells. J Gen Physiol 92:667–683PubMedCrossRefGoogle Scholar
  103. Schroeder JI (1989) Quantitative analysis of outward rectifying K+ channel currents in guard cell protoplasts from Vicia faba. J Membr Biol 7:229–235Google Scholar
  104. Schroeder JI, Raschke K, Neher E (1987) Voltage dependence of K+ channels in guard cell protoplasts. Proc Natl Acad Sci USA 84:4108–4112PubMedCrossRefGoogle Scholar
  105. Schroeder BC, Hechenberger M, Weinreich F, Kubisch C, Jentsch TJ (2000) KCNQ5, a novel potassium channel broadly expressed in brain, mediates M-type currents. J Biol Chem 275:24089–24095PubMedCrossRefGoogle Scholar
  106. Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D (2001a) Guard cell signal transduction. Annu Rev Plant Physiol Plant Mol Biol 52:627–658PubMedCrossRefGoogle Scholar
  107. Schroeder JI, Kwak JM, Allen GJ (2001b) Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410:327–330PubMedCrossRefGoogle Scholar
  108. Shin R, Schachtman DP (2004) Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proc Natl Acad Sci USA 101(23):8827–8832PubMedCrossRefGoogle Scholar
  109. Shin R, Berg RH, Schachtman DP (2005) Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency. Oxford journals. Plant Cell Physiol 46(8):1350–1357PubMedCrossRefGoogle Scholar
  110. Siddiqi MY, Glass ADM, Ruth TJ, Fernando M (1989) Studies of the regulation of nitrate influx by barley seedlings using I3NO3 . Plant Physiol 90:806–813PubMedCrossRefGoogle Scholar
  111. Siddiqi MY, Glass ADM, Ruth TJ, Rufty TW (1990) Studies of the uptake of nitrate in barley. I. Kinetics of 13NO, – influx. Plant Physiol 93:1426–1432PubMedCrossRefGoogle Scholar
  112. Snedden WA, Fromm H (1998) Calmodulin, calmodulin-related proteins and plant responses to the environment. Trends Plant Sci 3:299–304CrossRefGoogle Scholar
  113. Snedden WA, Fromm H (2001) Calmodulin as a versatile calcium signal transducer in plants. New Phytol 151:35–66CrossRefGoogle Scholar
  114. Stitt M (1999) Nitrate regulation of metabolism and growth. Curr Opin Plant Biol 2:178–186PubMedCrossRefGoogle Scholar
  115. Trewavas AJ, Malho R (1997) Signal perception and transduction: the origin of the phenotype. Plant Cell 9(7):1181–1195PubMedCrossRefGoogle Scholar
  116. Tsay YF, Schroeder JI, Feldmann KA, Crawford NM (1993) The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell 72:705–713PubMedCrossRefGoogle Scholar
  117. Tsay YF, Chiu CC, Tsai CB, Ho CH, Hsu PK (2007) Nitrate transporters and peptide transporters. FEBS Lett 581:2290–2300PubMedCrossRefGoogle Scholar
  118. Tsay YF et al (2011) Integration of nitrogen and potassium signaling. Annu Rev Plant Biol 62:207–226PubMedCrossRefGoogle Scholar
  119. Vahisalu T, Puzõrjova I, Brosché M, Valk E, Lepiku M, Moldau H, Pechter P, Wang YS, Lindgren O, Salojärvi J, Loog M, Kangasjärvi J, Kollist H (2008) Ozone-triggered rapid stomatal response involves the production of reactive oxygen species, and is controlled by SLAC1 and OST1. Plant J 62(3):442–453CrossRefGoogle Scholar
  120. Vahisalu T, Kollist H, Wang YF, Nishimura N, Chan WY, Valerio G, Lamminmäki A, Brosché M, Moldau H, Desikan R, Schroeder JI, Kangasjärvi J (2010) SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature 452(7186):487–491CrossRefGoogle Scholar
  121. Vert G, Chory J (2009) A toggle switch in plant nitrate uptake. Cell 138(6):1064–1066PubMedCrossRefGoogle Scholar
  122. Véry AA, Sentenac H (2002) Cation channels in the Arabidopsis plasma membrane. Trends Plant Sci 7(4):168–175PubMedCrossRefGoogle Scholar
  123. Véry AA, Sentenac H (2003) Molecular mechanisms and regulation of K+ transport in higher plants. Annu Rev Plant Biol 54:575–603PubMedCrossRefGoogle Scholar
  124. Von Wirén N, Bergfeld A, Ninnemann O, Frommer WB (1997a) OsAMT1-1: A high-affinity ammonium transporter fromrice (Oryza sativa cv. Nipponbare). Plant Mol Biol 3:681Google Scholar
  125. Von Wirén N, Gazzarrini S, Frommer WB (1997b) Regulation of mineral nitrogen uptake in plants. Plant Soil 196:191–199CrossRefGoogle Scholar
  126. Walch-Liu P, Forde BG (2008) Nitrate signalling mediated by the NRT1.1 nitrate transporter antagonises l-glutamate-induced changes in root architecture. Plant J 54:820–828PubMedCrossRefGoogle Scholar
  127. Walker DJ, Leigh RA, Miller AJ (1996) Potassium homeostasis in vacuolated plant cells. Proc Natl Acad Sci USA 93:10510–10514PubMedCrossRefGoogle Scholar
  128. Wang R, Crawford NM (1996) Genetic identification of a gene involved in constitutive, high-affinity nitrate transport in higher plants. Proc Natl Acad Sci USA 93:9297–9301PubMedCrossRefGoogle Scholar
  129. Wang P, Song CP (2008) Guard-cell signalling for hydrogen peroxide and abscisic acid. New Phytol 178:703–718PubMedCrossRefGoogle Scholar
  130. Wang Y, Wu WH (2010) Plant sensing and signaling in response to K+- deficiency. Mol Plant 3:280–287PubMedCrossRefGoogle Scholar
  131. Wang R et al (1998) The Arabidopsis CHL1 protein plays a major role in high-affinity nitrate uptake. Proc Natl Acad Sci USA 95:15134–15139PubMedCrossRefGoogle Scholar
  132. Wang YY, Hsu PK, Tsay YF (2012) Uptake, allocation and signaling of nitrate. Trends Plant Sci 971:1–10Google Scholar
  133. Xu J, Li HD, Chen LQ, Wang Y, Liu LL, He L, Wu WH (2006) A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125:1347–1360PubMedCrossRefGoogle Scholar
  134. Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279:407–409PubMedCrossRefGoogle Scholar
  135. Zhang YJ, Lynch JP, Brown KM (2003) Ethylene and phosphorus availability have interacting yet distinct effects on root hair development. J Exp Bot 54:2351–2361PubMedCrossRefGoogle Scholar
  136. Zielinski RE (1998) Calmodulin and calmodulin binding proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 49:697–725PubMedCrossRefGoogle Scholar

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© Springer India 2013

Authors and Affiliations

  1. 1.Department of Plant Molecular BiologyUniversity of Delhi South CampusNew DelhiIndia

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