Advertisement

Potassium Uptake and Homeostasis in Plants Grown Under Hostile Environmental Conditions, and Its Regulation by CBL-Interacting Protein Kinases

  • Mohammad Alnayef
  • Jayakumar Bose
  • Sergey Shabala
Chapter

Abstract

Abiotic stresses impose major penalties on plant growth and agricultural crop production. Understanding the mechanisms by which plants perceive these abiotic stresses, and the subsequent signal transduction that activates their adaptive responses, is therefore of vital importance for improving plant stress tolerance in breeding programs. Among the plethora of second messengers employed by plant cells, calcineurin B–like proteins (CBLs) and CBL-interacting protein kinases (CIPKs) have emerged as critical components of the signal transduction pathways and regulators of plant ionic homeostasis under stress conditions. This chapter summarizes the current knowledge on interaction between CIPKs and K+ transport systems, and the role of the former in regulating cell ionic relations and K+ homeostasis in plants grown under adverse environmental conditions.

Keywords

Potassium channels Transporters Homeostasis Stress tolerance Signal transduction Calcineurin B–like proteins (CBL) CBL-interacting protein kinases (CIPKs) Calcium signature Membrane depolarization Gene expression Abiotic stress 

Abbreviations

ABA

Abscisic acid

AKT

Arabidopsis potassium transporter

[Ca2+]cyt

Cytosolic concentration of calcium

CaM

Calmodulin

CBL

Calcineurin B–like protein

CIPK

CBL-interacting protein kinase

CDPK

Ca2+-dependent protein kinase

CML

CaM-like protein

CPDK

Calcium-dependent protein kinase

Ek

Equilibrium potential

GORK

Guard cells outward-rectifying potassium channel

HAK

High-affinity potassium transporter

KAT

Inward-rectifying Shaker-like potassium channel

KC1

Silent Shaker-like potassium channel

KUP

K+ uptake permease

mRNA

Messenger RNA

NADPH

Reduced nicotinamide adenine dinucleotide phosphate

NO

Nitric oxide

PCD

Programmed cell death

PEG

Polyethylene glycol

PLP

Pyridoxal-5'-phosphate

PP2C

2C-Type protein phosphatase

RBOH

Respiratory burst oxidase homologue

ROS

Reactive oxygen species

SKOR

Stelar outward-rectifying potassium channel

SNO1

Sensitive to nitric oxide 1

SPIK

Shaker pollen inward K+ channel

TPK

Tandem-pore potassium channel

V-ATPase

Vacuolar adenosine triphosphate

Notes

Acknowledgements

This work was supported by the Australian Research Council and Australia–India Strategic Research Funding grants to Sergey Shabala.

References

  1. Adams E, Diaz C, Matsui M, Shin R (2014) Overexpression of a novel component induces HAK5 and enhances growth in Arabidopsis. ISRN Bot 2014:9. https://doi.org/10.1155/2014/490252 Google Scholar
  2. Anschütz U, Becker D, Shabala S (2014) Going beyond nutrition: regulation of potassium homoeostasis as a common denominator of plant adaptive responses to environment. J Plant Physiol 171(9):670–687Google Scholar
  3. Bañuelos MA, Klein RD, Alexander-Bowman SJ, Rodriguez-Navarro A (1995) A potassium transporter of the yeast Schwanniomyces occidentalis homologous to the Kup system of Escherichia coli has a high concentrative capacity. EMBO J 14:3021–3027PubMedCentralPubMedGoogle Scholar
  4. Bañuelos MA, Garciadeblas B, Cubero B, Rodríguez-Navarro A (2002) Inventory and functional characterization of the HAK potassium transporters of rice. Plant Physiol Biochem 130:784–795. https://doi.org/10.1104/pp.007781 Google Scholar
  5. Britto DT, Kronzucker HJ (2002) NH4 + toxicity in higher plants: a critical review. J Plant Physiol 159:567–584. https://doi.org/10.1078/0176-1617-0774 CrossRefGoogle Scholar
  6. Bush DS (1995) Calcium regulation in plant cells and its role in signaling. Annu Rev Plant Biol 46:95–122CrossRefGoogle Scholar
  7. Chen G et al (2015) Rice potassium transporter OsHAK1 is essential for maintaining potassium-mediated growth and functions in salt tolerance over low and high potassium concentration ranges. Plant Cell Environ 38:2747–2765. https://doi.org/10.1111/pce.12585 CrossRefPubMedGoogle Scholar
  8. Cheong YH et al (2007) Two calcineurin B–like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. Plant J 52:223–239. https://doi.org/10.1111/j.1365-313X.2007.03236.x CrossRefPubMedGoogle Scholar
  9. Chérel I (2004) Regulation of K+ channel activities in plants: from physiological to molecular aspects. J Exp Bot 55:337–351. https://doi.org/10.1093/jxb/erh028 CrossRefPubMedGoogle Scholar
  10. DeFalco TA, Bender KW, Snedden WA (2010) Breaking the code: Ca2+ sensors in plant signalling. Biochem J 425:27–40CrossRefGoogle Scholar
  11. Demidchik V, Shabala SN, Coutts KB, Tester MA, Davies JM (2003) Free oxygen radicals regulate plasma membrane Ca2+- and K+-permeable channels in plant root cells. J Cell Sci 116:81–88CrossRefPubMedGoogle Scholar
  12. Demidchik V (2014) Mechanisms and physiological roles of K+ efflux from root cells. J Plant Physiol 171(9):696–707. https://doi.org/10.1016/j.jplph.2014.01.015
  13. 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 127:1012–1019CrossRefPubMedCentralPubMedGoogle Scholar
  14. Desbrosses G, Josefsson C, Rigas S, Hatzopoulos P, Dolan L (2003) AKT1 and TRH1 are required during root hair elongation in Arabidopsis. J Exp Bot 54:781–788CrossRefPubMedGoogle Scholar
  15. Dinneny JR (2010) Analysis of the salt-stress response at cell-type resolution. Plant Cell Environ 33(4):543–551. https://doi.org/10.1111/j.1365-3040.2009.02055.x
  16. Eckert C, Offenborn JN, Heinz T, Armarego-Marriott T, Schultke S, Zhang C (2014) The vacuolar calcium sensors CBL2 and CBL3 affect seed size and embryonic development in Arabidopsis thaliana. Plant J 78:146–156. https://doi.org/10.1111/tpj.12456 CrossRefPubMedGoogle Scholar
  17. Epstein E, Rains DW, Elzam OE (1963) Resolution of dual mechanisms of potassium absorption by barley roots. Proc Natl Acad Sci 49:684–692. https://doi.org/10.1073/pnas.49.5.684 CrossRefPubMedCentralPubMedGoogle Scholar
  18. Fulgenzi FR, Peralta ML, Mangano S, Danna CH, Vallejo AJ, Puigdomenech P, Santa-María GE (2008) The ionic environment controls the contribution of the barley HvHAK1 transporter to potassium acquisition. Plant Physiol 147:252–262. https://doi.org/10.1104/pp.107.114546 CrossRefPubMedCentralPubMedGoogle Scholar
  19. Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. Bioessays 28:1091–1101. https://doi.org/10.1002/bies.20493 CrossRefPubMedGoogle Scholar
  20. Geiger D et al (2009) Heteromeric AtKC1. AKT1 channels in Arabidopsis roots facilitate growth under K+-limiting conditions. J Biol Chem 284:21288–21295. https://doi.org/10.1074/jbc.M109.017574 CrossRefPubMedCentralPubMedGoogle Scholar
  21. 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 137:1105–1114. https://doi.org/10.1104/pp.104.057216 CrossRefPubMedCentralPubMedGoogle Scholar
  22. Golldack D, Quigley F, Michalowski CB, Kamasani UR, Bohnert HJ (2003) Salinity stress–tolerant and –sensitive rice (Oryza sativa L.) regulate AKT1-type potassium channel transcripts differently. Plant Mol Biol 51:71–81CrossRefPubMedGoogle Scholar
  23. Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front Plant Sci 5:151. https://doi.org/10.3389/fpls.2014.00151 CrossRefPubMedCentralPubMedGoogle Scholar
  24. Grabov A (2007) Plant KT/KUP/HAK potassium transporters: single family—multiple functions. Ann Bot 99:1035–1041. https://doi.org/10.1093/aob/mcm066 CrossRefPubMedCentralPubMedGoogle Scholar
  25. Gupta M et al (2008) KT/HAK/KUP potassium transporters gene family and their whole-life cycle expression profile in rice (Oryza sativa). Mol Genet Genomics 280:437–452. https://doi.org/10.1007/s00438-008-0377-7 CrossRefPubMedGoogle Scholar
  26. Hakerlerler H, Oktay M, Eryüce N, Yagmur B (1997) Effect of potassium sources on the chilling tolerance of some vegetable seedlings grown in hotbeds. In: Johnston AE (ed) Food security in the WANA region, the essential need for balanced fertilization. International Potash Institute, Horgen, pp 317–327Google Scholar
  27. He C, Cui K, Duan A, Zeng Y, Zhang J (2012) Genome-wide and molecular evolution analysis of the poplar KT/HAK/KUP potassium transporter gene family. Ecol Evol 2:1996–2004CrossRefPubMedCentralPubMedGoogle Scholar
  28. Hedrich R, Anschütz U, Becker D (2011) Biology of plant potassium channels. In: Murphy SA, Schulz B, Peer W (eds) The plant plasma membrane. Springer Berlin Heidelberg, Berlin, pp 253–274. https://doi.org/10.1007/978-3-642-13431-9_11 CrossRefGoogle Scholar
  29. Held K 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 21:1116–1130. http://www.nature.com/cr/journal/v21/n7/suppinfo/cr201150s1.html CrossRefPubMedCentralPubMedGoogle Scholar
  30. Hirsch RE, Lewis BD, Spalding EP, Sussman MR (1998) A role for the AKT1 potassium channel in plant nutrition. Science 280:918–921CrossRefPubMedGoogle Scholar
  31. Kader MA, Lindberg S (2010) Cytosolic calcium and pH signaling in plants under salinity stress. Plant Signal Behav 5:233–238CrossRefPubMedCentralPubMedGoogle Scholar
  32. 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 134:43–58. https://doi.org/10.1104/pp.103.033068 CrossRefPubMedCentralPubMedGoogle Scholar
  33. 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 9:195–203. https://doi.org/10.1046/j.1365-313X.1996.09020195.x CrossRefPubMedGoogle Scholar
  34. Lan W-Z, Lee S-C, Che Y-F, Jiang Y-Q, Luan S (2011) Mechanistic analysis of AKT1 regulation by the CBL–CIPK–PP2CA interactions. Mol Plant 4:527–536. https://doi.org/10.1093/mp/ssr031 CrossRefPubMedGoogle Scholar
  35. Lebaudy A, Very AA, Sentenac H (2007) K+ channel activity in plants: genes, regulations and functions. FEBS Lett 581:2357–2366. https://doi.org/10.1016/j.febslet.2007.03.058 CrossRefPubMedGoogle Scholar
  36. Lee SC et al (2007) A protein phosphorylation/dephosphorylation network regulates a plant potassium channel. Proc Natl Acad Sci U S A 104:15959–15964. https://doi.org/10.1073/pnas.0707912104 CrossRefPubMedCentralPubMedGoogle Scholar
  37. Leigh RA, Wyn Jones RG (1984) A hypothesis relating critical potassium concentrations for growth to the distribution and function of this ion in the plant cell. New Phytol 97:1–13. https://doi.org/10.1111/j.1469-8137.1984.tb04103.x CrossRefGoogle Scholar
  38. 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 103:12625–12630. https://doi.org/10.1073/pnas.0605129103 CrossRefPubMedCentralPubMedGoogle Scholar
  39. Li R, Zhang J, Wei J, Wang H, Wang Y, Ma R (2009) Functions and mechanisms of the CBL–CIPK signaling system in plant response to abiotic stress. Prog Nat Sci 19:667–676. https://doi.org/10.1016/j.pnsc.2008.06.030 CrossRefGoogle Scholar
  40. Li J, Long Y, Qi GN, Xu ZJ, Wu WH (2014) The Os-AKT1 channel is critical for K+ uptake in rice roots and is modulated by the rice CBL1–CIPK23 complex. Plant Cell 26:3387–3402. https://doi.org/10.1105/tpc.114.123455 CrossRefPubMedCentralPubMedGoogle Scholar
  41. 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 161:266–277. https://doi.org/10.1104/pp.112.206896 CrossRefPubMedGoogle Scholar
  42. Ma L, Zhang H, Sun L, Jiao Y, Zhang G, Miao C, Hao F (2012a) NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Na+/K+ homeostasis in Arabidopsis under salt stress. J Exp Bot 63:305–317. https://doi.org/10.1093/jxb/err280 CrossRefPubMedGoogle Scholar
  43. Ma T-L, Wu W-H, Wang Y (2012b) Transcriptome analysis of rice root responses to potassium deficiency BMC. Plant Biol 12:1–13. https://doi.org/10.1186/1471-2229-12-161 Google Scholar
  44. Maathuis FJ, Sanders D (1994) Mechanism of high-affinity potassium uptake in roots of Arabidopsis thaliana. Proc Natl Acad Sci U S A 91:9272–9276CrossRefPubMedCentralPubMedGoogle Scholar
  45. Maathuis FJ, Ichida AM, Sanders D, Schroeder JI (1997) Roles of higher plant K+ channels. Plant Physiol 114:1141–1149CrossRefPubMedCentralPubMedGoogle Scholar
  46. Mangano S, Silberstein S, Santa-María GE (2008) Point mutations in the barley HvHAK1 potassium transporter lead to improved K+-nutrition and enhanced resistance to salt stress. FEBS Lett 582:3922–3928. https://doi.org/10.1016/j.febslet.2008.10.036 CrossRefPubMedGoogle Scholar
  47. Manik SMN, Shi S, Mao J, Dong L, Su Y, Wang Q, Liu H (2015) The calcium sensor CBL–CIPK is involved in plant’s response to abiotic stresses. Int J Genomics 2015:10. https://doi.org/10.1155/2015/493191 CrossRefGoogle Scholar
  48. Maser P et al (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667CrossRefPubMedCentralPubMedGoogle Scholar
  49. Neumann PM (2011) Recent advances in understanding the regulation of whole-plant growth inhibition by salinity, drought and colloid stress. Adv Bot Res 57:33–48CrossRefGoogle Scholar
  50. Nieves-Cordones M, Miller AJ, Aleman F, Martinez V, Rubio F (2008) A putative role for the plasma membrane potential in the control of the expression of the gene encoding the tomato high-affinity potassium transporter HAK5. Plant Mol Biol 68:521–532. https://doi.org/10.1007/s11103-008-9388-3 CrossRefPubMedGoogle Scholar
  51. Nieves-Cordones M, Aleman F, Martinez V, Rubio F (2010) The Arabidopsis thaliana HAK5 K+ transporter is required for plant growth and K+ acquisition from low K+ solutions under saline conditions. Mol Plant 3:326–333. https://doi.org/10.1093/mp/ssp102 CrossRefPubMedGoogle Scholar
  52. 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 53:423–432. https://doi.org/10.1093/pcp/pcr194 CrossRefPubMedGoogle Scholar
  53. Ogasawara Y et al (2008) Synergistic activation of the Arabidopsis NADPH oxidase AtrbohD by Ca2+ and phosphorylation. J Biol Chem 283:8885–8892. https://doi.org/10.1074/jbc.M708106200 CrossRefPubMedGoogle Scholar
  54. 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 17:411–421CrossRefPubMedGoogle Scholar
  55. Perochon A, Aldon D, Galaud J-P, Ranty B (2011) Calmodulin and calmodulin-like proteins in plant calcium signaling. Biochimie 93:2048–2053. https://doi.org/10.1016/j.biochi.2011.07.012 CrossRefPubMedGoogle Scholar
  56. Pilot G, Pratelli R, Gaymard F, Meyer Y, Sentenac H (2003) Five-group distribution of the shaker-like K+ channel family in higher plants. J Mol Evol 56:418–434. https://doi.org/10.1007/s00239-002-2413-2 CrossRefPubMedGoogle Scholar
  57. Pyo YJ, Gierth M, Schroeder JI, Cho MH (2010) High-affinity K+ transport in Arabidopsis: AtHAK5 and AKT1 are vital for seedling establishment and postgermination growth under low-potassium conditions. Plant Physiol 153:863–875. https://doi.org/10.1104/pp.110.154369 CrossRefPubMedCentralPubMedGoogle Scholar
  58. Ragel P et al (2015) The CBL-interacting protein kinase CIPK23 regulates HAK5-mediated high-affinity K+ uptake in Arabidopsis roots. Plant Physiol 169:2863–2873. https://doi.org/10.1104/pp.15.01401 PubMedCentralPubMedGoogle Scholar
  59. Reddy VS, Reddy ASN (2004) Proteomics of calcium-signaling components in plants. Phytochemistry 65:1745–1776. https://doi.org/10.1016/j.phytochem.2004.04.033 CrossRefPubMedGoogle Scholar
  60. Rodriguez-Navarro A (2000) Potassium transport in fungi and plants. Biochim Biophys Acta (BBA) Rev Biomembr 1469:1–30CrossRefGoogle Scholar
  61. Rodríguez-Navarro A, Rubio F (2006) High-affinity potassium and sodium transport systems in plants. J Exp Bot 57:1149–1160. https://doi.org/10.1093/jxb/erj068 CrossRefPubMedGoogle Scholar
  62. Santa-María 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 9:2281–2289CrossRefPubMedCentralPubMedGoogle Scholar
  63. Schachtman DP, Schroeder JI, Lucas WJ, Anderson JA, Gaber RF (1992) Expression of an inward-rectifying potassium channel by the Arabidopsis KAT1 cDNA. Science 258:1654–1658CrossRefPubMedGoogle Scholar
  64. Schleyer M, Bakker EP (1993) Nucleotide sequence and 3′-end deletion studies indicate that the K+-uptake protein kup from Escherichia coli is composed of a hydrophobic core linked to a large and partially essential hydrophilic C terminus. J Bacteriol 175:6925–6931CrossRefPubMedCentralPubMedGoogle Scholar
  65. Schmöckel SM, Garcia AF, Berger B, Tester M, Webb AA, Roy SJ (2015) Different NaCl-induced calcium signatures in the Arabidopsis thaliana ecotypes Col-0 and C24. PloS One 10:e0117564CrossRefPubMedCentralPubMedGoogle Scholar
  66. Schulz P, Herde M, Romeis T (2013) Calcium-dependent protein kinases: hubs in plant stress signaling and development. Plant Physiol 163:523–530. https://doi.org/10.1104/pp.113.222539 CrossRefPubMedCentralPubMedGoogle Scholar
  67. Sentenac H, Bonneaud N, Minet M, Lacroute F, Salmon JM, Gaymard F, Grignon C (1992) Cloning and expression in yeast of a plant potassium ion transport system. Science 256:663–665CrossRefPubMedGoogle Scholar
  68. Shabala S, Pottosin I (2014) Regulation of potassium transport in plants under hostile conditions: implications for abiotic and biotic stress tolerance. Physiol Plant 151:257–279. https://doi.org/10.1111/ppl.12165 CrossRefPubMedGoogle Scholar
  69. Shabala L, Zhang JY, Pottosin I, Bose J, Zhu M, Fuglsang AT, Velarde-Buendia A, Massart A, Hill CB, Roessner U, Bacic A, Wu HH, Azzarello E, Pandolfi C, Zhou MX, Poschenrieder C, Mancuso S, Shabala S (2016) Cell-Type-Specific H+-ATPase Activity in Root Tissues Enables K+ Retention and Mediates Acclimation of Barley (Hordeum vulgare) to Salinity Stress. Plant Physiol 172(4):2445–2458. https://doi.org/10.1104/pp.16.01347
  70. Shabala S (2017) Signalling by potassium: another second messenger to add to the list? J Exp Bot 68(15):4003–4007. https://doi.org/10.1093/jxb/erx238
  71. Spalding EP, Hirsch RE, Lewis DR, Qi Z, Sussman MR, Lewis BD (1999) Potassium uptake supporting plant growth in the absence of AKT1 channel activity: inhibition by ammonium and stimulation by sodium. J Gen Physiol 113:909–918. https://doi.org/10.1085/jgp.113.6.909 CrossRefPubMedCentralPubMedGoogle Scholar
  72. Szczerba MW, Britto DT, Ali SA, Balkos KD, Kronzucker HJ (2008) NH4 +-stimulated and -inhibited components of K+ transport in rice (Oryza sativa L.) J Exp Bot 59:3415–3423. https://doi.org/10.1093/jxb/ern190 CrossRefPubMedCentralPubMedGoogle Scholar
  73. Szyroki A et al (2001) KAT1 is not essential for stomatal opening. Proc Natl Acad Sci U S A 98:2917–2921. https://doi.org/10.1073/pnas.051616698 CrossRefPubMedCentralPubMedGoogle Scholar
  74. Tai F, Wang Q, Yuan Z, Yuan Z, Li H, Wang W (2013) Characterization of five CIPK genes expressions in maize under water stress. Acta Physiol Plant 35:1555–1564. https://doi.org/10.1007/s11738-012-1197-2 CrossRefGoogle Scholar
  75. Tang RJ, Liu H, Yang Y, Yang L, Gao XS, Garcia VJ (2012) Tonoplast calcium sensors CBL2 and CBL3 control plant growth and ion homeostasis through regulating V-ATPase activity in Arabidopsis. Cell Res 22:1650–1665. https://doi.org/10.1038/cr.2012.161 CrossRefPubMedCentralPubMedGoogle Scholar
  76. Tuteja N, Mahajan S (2007) Calcium signaling network in plants: an overview. Plant Signal Behav 2:79–85CrossRefPubMedCentralPubMedGoogle Scholar
  77. Very AA, Sentenac H (2002) Cation channels in the Arabidopsis plasma membrane. Trends Plant Sci 7:168–175CrossRefPubMedGoogle Scholar
  78. Véry AA, Sentenac H (2003) Molecular mechanisms and regulation of K+ transport in higher plants. Annu Rev Plant Biol 54:575–603. https://doi.org/10.1146/annurev.arplant.54.031902.134831 CrossRefPubMedGoogle Scholar
  79. Walker DJ, Leigh RA, Miller AJ (1996) Potassium homeostasis in vacuolate plant cells. Proc Natl Acad Sci 93:10510–10514CrossRefPubMedCentralPubMedGoogle Scholar
  80. Walker DJ, Black CR, Miller AJ (1998) The role of cytosolic potassium and pH in the growth of barley roots. Plant Physiol 118:957–964CrossRefPubMedCentralPubMedGoogle Scholar
  81. Wang M, Zheng Q, Shen Q, Guo S (2013) The critical role of potassium in plant stress response. Int J Mol Sci 14:7370–7390CrossRefPubMedCentralPubMedGoogle Scholar
  82. Wang X-P et al (2016) AtKC1 and CIPK23 synergistically modulate AKT1-mediated low potassium stress responses in Arabidopsis. Plant Physiol 170:2264–2277. https://doi.org/10.1104/pp.15.01493 CrossRefPubMedCentralPubMedGoogle Scholar
  83. Whalley HJ, Knight MR (2013) Calcium signatures are decoded by plants to give specific gene responses. New Phytologist 197:690–693. https://doi.org/10.1111/nph.12087 CrossRefPubMedGoogle Scholar
  84. Xia J et al (2014) Nitric oxide negatively regulates AKT1-mediated potassium uptake through modulating vitamin B6 homeostasis in Arabidopsis. Proc Natl Acad Sci 111:16196–16201. https://doi.org/10.1073/pnas.1417473111 CrossRefPubMedCentralPubMedGoogle Scholar
  85. Xiang Y, Huang Y, Xiong L (2007) Characterization of stress-responsive CIPK genes in rice for stress tolerance improvement. Plant Physiol 144:1416–1428. https://doi.org/10.1104/pp.107.101295 CrossRefPubMedCentralPubMedGoogle Scholar
  86. Xu J, Li HD, Chen LQ, Wang Y, Liu LL, He L (2006) A protein kinase, interacting with two calcineurin B–like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125:1347–1360. https://doi.org/10.1016/j.cell.2006.06.011 CrossRefPubMedGoogle Scholar
  87. Yang W, Kong Z, Omo-Ikerodah E, Xu W, Li Q, Xue Y (2008) Calcineurin B–like interacting protein kinase OsCIPK23 functions in pollination and drought stress responses in rice (Oryza sativa L.). J Genet Genomics 35:531–543, s531–532. https://doi.org/10.1016/s1673-8527(08)60073-9
  88. Yang Z, Gao Q, Sun C, Li W, Gu S, Xu C (2009) Molecular evolution and functional divergence of HAK potassium transporter gene family in rice (Oryza sativa L.) J Genet Genomics 36:161–172. https://doi.org/10.1016/s1673-8527(08)60103-4 CrossRefPubMedGoogle Scholar
  89. Yang T et al (2014) The role of a potassium transporter OsHAK5 in potassium acquisition and transport from roots to shoots in rice at low potassium supply levels. Plant Physiol 166:945–959. https://doi.org/10.1104/pp.114.246520 CrossRefPubMedCentralPubMedGoogle Scholar
  90. Zhang Z, Zhang J, Chen Y, Li R, Wang H, Wei J (2012) Genome-wide analysis and identification of HAK potassium transporter gene family in maize (Zea mays L.) Plant Mol Biol Report 39:8465–8473. https://doi.org/10.1007/s11033-012-1700-2 CrossRefGoogle Scholar
  91. Zhu S, Zhou X, Wu X, Jiang Z (2013) Structure and function of the CBL–CIPK Ca2+-decoding system in plant calcium signaling. Plant Mol Biol Report 31:1193–1202. https://doi.org/10.1007/s11105-013-0631-y CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Mohammad Alnayef
    • 1
  • Jayakumar Bose
    • 2
  • Sergey Shabala
    • 1
  1. 1.School of Land and Food, University of TasmaniaHobartAustralia
  2. 2.ARC Centre of Excellence in Plant Energy Biology, School of Agriculture, Food and Wine, Waite Research InstituteThe University of AdelaideGlen OsmondAustralia

Personalised recommendations