Molecular mechanisms involved in plant adaptation to low K+ availability

Journal of Experimental Botany

Volumn 65, Issue 3, 2014, Pages 833-848

  Chérel, Isabelle ^a   Lefoulon, Cécile ^a,b   Boeglin, Martin ^a   Sentenac, Hervé ^a  

^a INRA   (France)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Auxin; ethylene; K+ membrane transport; K+ starvation; plant K+ nutrition; reactive oxygen species (ROS); root

Indexed keywords

AUXIN; ETHYLENE; POTASSIUM; POTASSIUM CHANNEL;

ADAPTATION; BIOLOGICAL MODEL; CHEMISTRY; GENE EXPRESSION REGULATION; K+ MEMBRANE TRANSPORT; K+ STARVATION; METABOLISM; PHYSIOLOGY; PLANT; PLANT K+ NUTRITION; PLANT LEAF; PLANT ROOT; PLANT STEM; POTASSIUM DEFICIENCY; REACTIVE OXYGEN SPECIES (ROS); REVIEW; ROOT.; SIGNAL TRANSDUCTION; SOIL;

AUXIN; ETHYLENE; K+ MEMBRANE TRANSPORT; K+ STARVATION; PLANT K+ NUTRITION; REACTIVE OXYGEN SPECIES (ROS); ROOT.;

ADAPTATION, PHYSIOLOGICAL; GENE EXPRESSION REGULATION, PLANT; MODELS, BIOLOGICAL; PLANT LEAVES; PLANT ROOTS; PLANT STEMS; PLANTS; POTASSIUM; POTASSIUM CHANNELS; POTASSIUM DEFICIENCY; SIGNAL TRANSDUCTION; SOIL;

EID: 84894227340     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert402     Document Type: Review

References (118)

1. Ache P, Becker D, Ivashikina N, Dietrich P, Roelfsema MRG, Hedrich R. 2000. GORK, a delayed outward rectifier expressed in guard cells of Arabidopsis thaliana, is a K+-selective, K+-sensing ion channel. FEBS Letters 486, 93-98.
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 Physiology 134, 1135-1145.
3. Amtmann A, Armengaud P. 2007. The role of calcium sensorinteracting protein kinases in plant adaptation to potassium-deficiency: new answers to old questions. Cell Research 17, 483-485.
4. Armengaud P, Breitling R, Amtmann A. 2004. The potassiumdependent transcriptome of Arabidopsis reveals a prominent role of jasmonic acid in nutrient signaling. Plant Physiology 136, 2556-2576.
5. Armengaud P, Breitling R, Amtmann A. 2010. Coronatineinsensitive 1 (COI1) mediates transcriptional responses of Arabidopsis thaliana to external potassium supply. Molecular Plant 3, 390-405.
6. Armengaud P, Sulpice R, Miller AJ, Stitt M, Amtmann A, Gibon Y. 2009. Multilevel analysis of primary metabolism provides new insights into the role of potassium nutrition for glycolysis and nitrogen assimilation in Arabidopsis roots. Plant Physiology 150, 772-785.
7. Armstrong MJ, Kirkby EA. 1979. Estimation of potassium recirculation in tomato plants by comparison of the rates of potassium and calcium accumulation in the tops with their fluxes in the xylem stream. Plant Physiology 63, 1143-1148.
8. Ashley MK, Grabov A. 2006. Plant responses to potassium deficiencies: a role for potassium transport proteins. Journal of Experimental Botany 57, 425-436.
9. Benlloch-González M, Arquero O, Fournier JM, Barranco D, Benlloch M. 2008. K+ starvation inhibits water-stress-induced stomatal closure. Journal of Plant Physiology 165, 623-630.
10. Billou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heldstra R, Alda M, Palme K, Scheres B. 2005. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433, 39-44.
11. Buch-Pedersen MJ, Rudashevskaya EL, Berner TS, Venema K, Palmgren MG. 2006. Potassium as an intrinsic uncoupler of the plasma membrane H+-ATPase. Journal of Biological Chemistry 281, 38285-38292.
12. Buschmann PH, Vaidyanathan R, Gassmann W, Schroeder JI. 2000. Enhancement of Na+ uptake currents, time-dependent inwardrectifying K+ channel currents, and K+ channel transcripts by K+ starvation in wheat root cells. Plant Physiology 122, 1387-1397.
13. Cakmak I, Hengeler CC, Marschner H. 1994. Partitioning of shoot and root dry matter and carbohydrates in bean plants suffering from phosphorus, potassium and magnesium deficiency. Journal of Experimental Botany 45, 1245-1250.
14. Cao Y, Glass ADM, Crawford N. 1993. Ammonium inhibition of Arabidopsis root growth can be reversed by potassium and by auxin resistance mutations aux1, axr1, and axr2. Plant Physiology 102, 983-989.
15. Cheong YH, Pandey GK, Grant JJ, Batistic O, Li L, Kim BG, Lee SC, Kudla J, Luan S. 2007. Two calcineurin B-like sensors, interacting with protein kinase CIPK23, regulate root transpiration and potassium uptake in Arabidopsis. The Plant Journal 52, 223-239.
16. 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. The Plant Cell 14, 1133-1146.
17. Clarkson DT, Hanson JB. 1980. The mineral nutrition of higher plants. Annual Review of Plant Physiology 31, 239-298.
18. Cochrane TT, Cochrane TA. 2009. The vital role of potassium in the osmotic mechanism of stomata aperture modulation and its link with potassium deficiency. Plant Signaling and Behavior 4, 240-243.
19. Corratgé-Faillie C, Jabnoune M, Zimmermann S, Véry A-A, Fizames C, Sentenac H. 2010. Potassium and sodium transport in non-animal cells: the Trk/Ktr/HKT transporter family. Cellular and Molecular Life Sciences 67, 2511-2532.
20. Czempinski K, Frachisse J-M, Maurel C, Barbier-Brygoo H, Mueller-Roeber B. 2002. Vacuolar membrane localization of the Arabidopsis 'two-pore' K+ channel KCO1. The Plant Journal 29, 809-820.
21. 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, 334-344.
22. Desbrosses G, Josefsson C, Rigas S, Hatzopoulos P, Dolan L. 2003. AKT1 and TRH1 are required during root hair elongation in Arabidopsis. Journal of Experimental Botany 54, 781-788.
23. 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. Molecular Plant 6, 559-569.
24. Drew MC. 1975. Comparison of the effects of a localized supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytologist 75, 479-490.
25. Drew MC, Saker LR, Barber SA, Jenkins W. 1984. Changes in kinetics of phosphate and potassium absorption in nutrient-deficient barley roots measured by a solution-depletion technique. Planta 160, 490-499.
26. Dreyer I, Antunes S, Hoshi T, Müller-Röber B, Palme K, Pongs O, Reintanz B, Hedrich R. 1997. Plant K+ channel alpha-subunits assemble indiscriminately. Biophysical Journal 72, 2143-2150.
27. Duby G, Hosy E, Fizames C, Alcon C, Costa A, Sentenac H, Thibaud J-B. 2008. AtKC1, a conditionally targeted Shaker-type subunit, regulates the activity of plant K+ channels. The Plant Journal 53, 115-123.
28. Epstein E, Rains DW, Elzam OE. 1963. Resolution of dual mechanisms of potassium absorption by barley roots. Proceedings of the National Academy of Sciences, USA 49, 684-692.
29. Fu HH, Luan S. 1998. AtKUP1: a dual-affinity K+ transporter from Arabidopsis. The Plant Cell 10, 63-73.
30. 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 Physiology 147, 252-262.
31. Gajdanowicz P, Michard E, Sandmann M, et al. 2011. Potassium (K+) gradients serve as a mobile energy source in plant vascular tissues. Proceedings of the National Academy of Sciences, USA 108, 864-869.
32. Garcia-Mata C, Wang J, Gajdanowicz P, Gonzalez W, Hills A, Donald N, Riedelsberger J, Amtmann A, Dreyer I, Blatt MR. 2010. A minimal cysteine motif required to activate the SKOR K+ channel of Arabidopsis by the reactive oxygen species H2O2. Journal of Biological Chemistry 285, 29286-29294.
33. Gaymard F, Pilot G, Lacombe B, Bouchez D, Bruneau D, Boucherez J, Michaux-Ferrière N, Thibaud J-B, Sentenac H. 1998. Identification and disruption of a plant Shaker-like outward channel involved in K+ release into the xylem sap. Cell 94, 647-655.
34. Geiger D, Becker D, Vosloh D, Gambale F, Palme K, Rehers M, Anschuetz U, Dreyer I, Kudla J, Hedrich R. 2009. Heteromeric AtKC1-AKT1 channels in Arabidopsis roots facilitate growth under K+-limiting conditions. Journal of Biological Chemistry 284, 21288-21295.
35. Gierth M, Mäser P. 2007. Potassium transport in plants-involvement in K+ acquisition, redistribution and homeostasis. FEBS Letters 581, 2348-2356.
36. Gierth M, Mäser 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 Physiology 137, 1105-1114.
37. Grabov A. 2007. Plant KT/KUP/HAK potassium transporters: single family-multiple functions. Annals of Botany 99, 1035-1041.
38. Grefen C, Blatt MR. 2012. Do calcineurin B-like proteins interact independently of the serine threonine kinase CIPK23 with the K+ channel AKT1? Lessons learned from a ménage à trois. Plant Physiology 159, 915-919.
39. Haro R, Bañuelos MA, Senn ME, Barrero-Gil J, Rodríguez- Navarro A. 2005. HKT1 mediates sodium uniport in roots. Pitfalls in the expression of HKT1 in yeast. Plant Physiology 139, 1495-1506.
40. Held K, Pascaud F, Eckert C, 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 Research 21, 1116-1130.
41. Hernandez M, Fernandez-Garcia N, Garcia-Garma J, Rubio-Asensio JS, Rubio F, Olmos E. 2012. Potassium starvation induces oxidative stress in Solanum lycopersicum L. roots. Journal of Plant Physiology 169, 1366-1374.
42. Hirsch RE, Lewis BD, Spalding EP, Sussman MR. 1998. A role for the AKT1 potassium channel in plant nutrition. Science 280, 918-921.
43. Ho CH, Lin SH, Hu HC, Tsay YF. 2009. CHL1 functions as a nitrate sensor in plants. Cell 138, 1184-1194.
44. Hong JP, Takeshi Y, Kondou Y, Schachtman DP, Matsui M, Shin R. 2013. Identification and characterization of transcription factors regulating Arabidopsis HAK5. Plant and Cell Physiology 54, 1478-1490.
45. Honsbein A, Sokolovski S, Grefen C, Campanoni P, Pratelli R, Paneque M, Chen Z, Johansson I, Blatt MR. 2009. A tripartite SNARE-K+ channel complex mediates in channel-dependent K+ nutrition in Arabidopsis. The Plant Cell 21, 2859-2877.
46. Horie T, Brodsky DE, Costa A, Kaneko T, Lo Schiavo F, Katsuhara M, Schroeder JI. 2011. K+ transport by the OsHKT2;4 transporter from rice with atypical Na+ transport properties and competition in permeation of K+ over Mg2+ and Ca2+ ions. Plant Physiology 156, 1493-1507.
47. Horie T, Costa A, Kim TH, Han MJ, Horie R, Leung H-Y, Miyao A, Hirochika H, An G, Schroeder JI. 2007. Rice OsHKT2;1 transporter mediates large Na+ influx component into K+-starved roots for growth. EMBO Journal 26, 3003-3014.
48. Hosy E, Vavasseur A, Mouline K, et al. 2003. The Arabidopsis outward K+ channel GORK is involved in regulation of stomatal movements and plant transpiration. Proceedings of the National Academy of Sciences, USA 100, 5549-5554.
49. Ivashikina N, Becker D, Ache P, Meyerhoff O, Felle HH, Hedrich R. 2001. K+ channel profile and electrical properties of Arabidopsis root hairs. FEBS Letters 508, 463-469.
50. Jeanguenin L, Alcon C, Duby G, Boeglin M, Chérel I, Gaillard I, Zimmermann S, Sentenac H, Véry A-A. 2011. AtKC1 is a general modulator of Arabidopsis inward Shaker channel activity. The Plant Journal 67, 570-582.
51. Johansson I, Wulfetange K, Poree F, et al. 2006. External K+ modulates the activity of the Arabidopsis potassium channel SKOR via an unusual mechanism. The Plant Journal 46, 269-281.
52. Jung J-Y, Shin R, Schachtman DP. 2009. Ethylene mediates response and tolerance to potassium deprivation in Arabidopsis. The Plant Cell 21, 607-621.
53. Jungk A, Claassen N. 1986. Availability of phosphate and potassium as a result of interactions between root and soil in the rhizosphere. Zeitschrift für Pflanzenernährung und Bodenkunde 149, 411-427.
54. Kellermeier F, Chardon F, Amtmann A. 2013. Natural variation of Arabidopsis root architecture reveals complementing adaptive strategies to potassium starvation. Plant Physiology 161, 1421-1432.
55. Kim MJ, Ciani S, Schachtman DP. 2010. A peroxidase contributes to ROS production during Arabidopsis root response to potassium deficiency. Molecular Plant 3, 420-427.
56. Kim EJ, Kwak JM, Uozumi N, Schroeder JI. 1998. AtKUP1: an Arabidopsis gene encoding high-affinity potassium transport activity. The Plant Cell 10, 51-62.
57. Kim MJ, Ruzika D, Shin R, Schachtman DP. 2012. The Arabidopsis AP2/ERF transcription factor RAP2.11 modulates plant response to low-potassium conditions. Molecular Plant 5, 1042-1057.
58. Kochian LV, Lucas WJ. 1983. Potassium transport in corn roots. II. The significance of the root periphery. Plant Physiology 73, 208-215.
59. Lacombe B, Pilot G, Michard E, Gaymard F, Sentenac H, Thibaud J-B. 2000. A Shaker-like K+ channel with weak rectification is expressed in both source and sink phloem tissues of Arabidopsis. The Plant Cell 12, 837-851.
60. Lan WZ, Lee SC, Che YF, Jiang YQ, Luan S. 2011. Mechanistic analysis of AKT1 regulation by the CBL-CIPK-PP2CA interactions. Molecular Plant 4, 527-536.
61. Lan WZ, Wang W, Wang SM, Li LG, Buchanan BB, Lin HX, Gao JP, Luan S. 2010. A rice high-affinity transporter (HKT) conceals a calcium-permeable cation channel. Proceedings of the National Academy of Sciences, USA 107, 7089-7094.
62. Laohavisit A, Shang Z, Rubio L, et al. 2012. Arabidopsis annexin1 mediates the radical-activated plasma membrane Ca2+-and K+-permeable conductance in root cells. The Plant Cell 24, 1522-1533.
63. 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. Proceedings of the National Academy of Sciences, USA 104, 15959-15964.
64. Leigh RA, Wyn Jones RG. 1984. A hypothesis relating critical potassium concentrations for growth to the distribution and functions of this ion in the plant cell. New Phytologist 97, 1-13.
65. Lewis DR, Negi S, Sukumar P, Muday GK. 2011. Ethylene inhibits lateral root development, increases IAA transport and expression of PIN3 and PIN7 auxin efflux carriers. Development 138, 3485-3495.
66. 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. Proceedings of the National Academy of Sciences, USA 103, 12625-12630.
67. 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. Progress in Natural Science 19, 667-676.
68. Liu J, Zhu J-K. 1997. An Arabidopsis mutant with increased calcium requirement for potassium nutrition and salt tolerance. Proceedings of the National Academy of Sciences, USA 94, 14960-14964.
69. 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 Physiology 161, 266-277.
70. Ma TL, Wu WH, Wang Y. 2012. Transcriptome analysis of rice root responses to potassium deficiency. BMC Plant Biology 12, 161.
71. Maathuis FJ. 2006. The role of monovalent cations in plant response to salinity. Journal of Experimental Botany 57, 1137-1147.
72. Maathuis FJ, Filatov V, Herzyk P, et al. 2003. Transcriptome analysis of root transporters reveals participation of multiple gene families in the response to cation stress. The Plant Journal 35, 675-692.
73. Maathuis FJ, Ichida AM, Sanders D, Schroeder JI. 1997. Roles of higher plant K+ channels. Plant Physiology 114, 1141-1149.
74. Maathuis F, Sanders D. 1992. Plant membrane transport. Current Opinion in Cell Biology 4, 661-669.
75. Maathuis F, Sanders D. 1993. Energization of potassium uptake in Arabidopsis thaliana. Planta 191, 302-307.
76. Martínez-Cordero MA, Martínez V, Rubio F. 2005. High-affinity K+ uptake in pepper plants. Journal of Experimental Botany 56, 1553-1562.
77. Mäser P, Thomine S, Schroeder JI, et al. 2001. Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiology 126, 1646-1667.
78. Mazars C, Thuleau P, Lamotte O, Bourque S. 2010. Cross-talk between ROS and calcium in regulation of nuclear activities. Molecular Plant 3, 706-718.
79. Nam YJ, Tran LSP, Kojima M, Sakakibara H, Nishiyama R, Shin R. 2012. Regulatory roles of cytokinins and cytokinin signaling in response to potassium deficiency in Arabidopsis. PLoS One 7, e47797.
80. 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. Molecular Plant 3, 326-333.
81. Nieves-Cordones M, Martinez-Cordero MA, Martinez V, Rubio F. 2007. An NH4 +-sensitive component dominates high-affinity K+ uptake in tomato plants. Plant Science 172, 273-280.
82. Nieves-Cordones M, Miller AJ, Alemán F, Martínez V, Rubio F. 2008. A putative role for the plasma membrane potential in the control of the expression of the gene encoding the tomato highaffinity potassium transporter HAK5. Plant Molecular Biology 68, 521-532.
83. Pandey GK, Cheong YH, Kim B-G, Grant JJ, Li L, Luan S. 2007. CIPK9: a calcium sensor-interacting protein kinase required for lowpotassium tolerance in Arabidopsis. Cell Research 17, 411-421.
84. 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 Molecular Biology 51, 773-787.
85. Pritchard J, Wyn Jones, RG, Tomos, AD. 1991. Turgor, growth and rheological gradients of wheat roots following osmotic stress. Journal of Experimental Botany 42, 1043-1049.
86. Qi Z, Hampton CR, Shin R, Barkla BJ, White PJ, Schachtman DP. 2008. The high affinity K+ transporter AtHAK5 plays a physiological role in planta at very low K+ concentrations and provides a caesium uptake pathway in Arabidopsis. Journal of Experimental Botany 59, 595-607.
87. Reintanz B, Szyroki A, Ivashikina N, Ache P, Godde M, Becker D, Palme K, Hedrich R. 2002. AtKC1, a silent Arabidopsis potassium channel alpha-subunit modulates root hair K+ influx. Proceedings of the National Academy of Sciences, USA 99, 4079-4084.
88. Ren X-L, Qi G-N, Feng H-Q, Zhao S, Zhao S-S, Wang Y, Wu WH. 2013. Calcineurin B-like protein CBL10 directly interacts with AKT1 and modulates K+ homeostasis in Arabidopsis. The Plant Journal 74, 258-266.
89. Rigas S, Ditengou FA, Ljung K, Daras G, Tietz O, Palme K, Hatzopoulos P. 2013. Root gravitropism and root hair development constitute coupled developmental responses regulated by auxin homeostasis in the Arabidopsis root apex. New Phytologist 197, 1130-1141.
90. Rubio F, Nieves-Cordones M, Alemán F, Martínez V. 2008. Relative contribution of AtHAK5 and AtAKT1 to K+ uptake in the highaffinity range of concentrations. Physiologia Plantarum 134, 598-608.
91. Rubio F, Santa-Maria GE, Rodriguez-Navarro A. 2000. Cloning of Arabidopsis and barley cDNAs encoding HAK potassium transporters in root and shoot cells. Physiologia Plantarum 109, 34-43.
92. R?zicka K, Ljung K, Vanneste S, Podhorská R, Beeckman T, Friml J, Benková E. 2007. Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. The Plant Cell 19, 2197-2212.
93. Santa-Maria GE, Rubio F, Dubcovsky J, Rodriguez-Navarro A. 1997. The HAK1 gene of barley is a member of a large family and encodes a high-affinity potassium transporter. The Plant Cell 9, 2281-2289.
94. Sassi A, Mieulet D, Khan I, Moreau B, Gaillard I, Sentenac H, Véry AA. 2012. The rice monovalent cation transporter OsHKT2;4: revisited ionic selectivity. Plant Physiology 160, 498-510.
95. Shabala S, Cuin TA. 2007. Potassium transport and plant salt tolerance. Physiologia Plantarum 133, 651-669.
96. Sharma T, Dreyer I, Riedelsberger J. 2013. The role of K+ channels in uptake and redistribution of potassium in the model plant Arabidopsis thaliana. Frontiers in Plant Science 4, 224.
97. Sharp RE, Hsiao TC, Silk WK. 1990. Growth of the maize primary root at low water potentials, II. Role of growth and deposition of hexose and potassium in osmotic adjustement. Plant Physiology 93, 1337-1346.
98. Shi H, Quintero FJ, Pardo JM, Zhu JK. 2002. The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. The Plant Cell 14, 465-477.
99. Shin R, Berg RH, Schachtman DP. 2005. Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency. Plant and Cell Physiology 46, 1350-1357.
100. Shin R, Schachtman DP. 2004. Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proceedings of the National Academy of Sciences, USA 101, 8827-8832.
101. 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. Journal of General Physiology 113, 909-918.
102. Sugiyama T, Goto Y, Akazawa T. 1968. Pyruvate kinase activity of wheat plants grown under potassium deficient conditions. Plant Physiology 43, 730-734.
103. Szczerba MW, Britto DT, Kronzucker HJ. 2009. K+ transport in plants: physiology and molecular biology. Journal of Plant Physiology 166, 447-466.
104. Takehisa H, Sato Y, Antonio BA, Nagamura Y. 2013. Global transcriptome profile of rice root in response to essential macronutrient deficiency. Plant Signaling and Behavior 8, e24409.
105. Teale WD, Paponov IA, Ditengou F, Palme K. 2005. Auxin and the developing root of Arabidopsis thaliana. Physiologia Plantarum 123, 130-138.
106. ten Hoopen F, Cuin TA, Pedas P, Hegelund JN, Shabala S, Schjoerring JK, Jahn TP. 2010. Competition between uptake of ammonium and potassium in barley and Arabidopsis roots: molecular mechanisms and physiological consequences. Journal of Experimental Botany 61, 2303-2315.
107. Touraine B, Grignon N, Grignon C. 1988. Charge balance in NO3-fed soybean: estimation of K+ and carboxylate recirculation. Plant Physiology 88, 605-612.
108. Tsay YF, Ho CH, Chen HY, Lin SH. 2011. Integration of nitrogen and potassium signaling. Annual Review of Plant Biology 62, 207-226.
109. Véry A-A, Sentenac H. 2003. Molecular mechanisms and regulation of K+ transport in higher plants. Annual Review of Plant Biology 54, 575-603.
110. Vicente-Agullo F, Rigas S, Desbrosses G, Dolan L, Hatzopoulos P, Grabov A. 2004. Potassium carrier TRH1 is required for auxin transport in Arabidopsis roots. The Plant Journal 40, 523-535.
111. Walker DJ, Leigh RA, Miller AJ. 1996. Potassium homeostasis in vacuolated plant cells. Proceedings of the National Academy of Sciences, USA 93, 10510-10514.
112. Wang T-B, Gassmann W, Rubio F, Schroeder JI, Glass ADM. 1998. Rapid up-regulation of HKT1, a high-affinity potassium transporter gene, in roots of barley and wheat following withdrawal of potassium. Plant Physiology 118, 651-659.
113. Wang Y, He L, Li H-D, Xu J, Wu W-H. 2010. Potassium channel alpha-subunit AtKC1 negatively regulates AKT1-mediated K+ uptake in Arabidopsis roots under low-K+ stress. Cell Research 20, 826-837.
114. Wang Y, Li B, Du M, Eneji AE, Wang B, Duan L, Li Z, Tian X. 2012. Mechanism of phytohormone involvement in feedback regulation of cotton leaf senescence induced by potassium deficiency. Journal of Experimental Botany 63, 5887-5901.
115. Wang Y, Wu W-H. 2013. Potassium transport and signaling in higher plants. Annual Review of Plant Biology 64, 451-76.
116. Wu S-J, Ding, L, Zhu, J-K. 1996. SOS1, a genetic locus essential for salt tolerance and potassium acquisition. The Plant Cell 8, 617-627.
117. Xu J, Li HD, Chen LQ, Wang Y, Liu LL, He L, Wu W-H. 2006. A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125, 1347-1360.
118. Zhu J-K, Liu J, Xiong L. 1998. Genetic analysis of salt tolerance in Arabidopsis: evidence for a critical role of potassium nutrition. The Plant Cell 10, 1181-1191.