Abstract
In plant cells, potassium (K+) is abundantly present and is dominant cation plays a vital role in maintaining physiological and morphological characteristics of plants. Many membrane integrated channels and transporters specific to K+ are involved in maintaining the potassium concentration within plants via membrane electrical activities. Elemental homologues to K+ compete with it for entry inside plants; among those, cesium is very common radionuclide. Once cesium enters into the plant cell, it can cause phytotoxicity. Therefore, it is desirable to understand complete pathway and mechanisms of cesium uptake in the plants, in order to assess consequences from accidental release of radioactive substance. This review focuses on mechanism of K+ ion uptake through channels/transporter and involvement of these channels/transporter in cesium uptake in plant cells.
Similar content being viewed by others
References
Ache P, Becker D, Ivashikina N, Dietrich P, Roelfsema MR, Hedrich R (2000) GORK, a delayed outward rectifier expressed in guard cells of Arabidopsis thaliana, is a K+-selective, K+-sensing ion channel. FEBS Lett 486:93–98. https://doi.org/10.1016/S0014-5793(00)02248-1
Aleman F, Nieves-Cordones M, Martinez Rubio F (2009) Differential regulation of the HAK5 genes encoding the high-affinity K+ transporters of Thellungiella halophila and Arabidopsis thaliana. Environ Exp Bot 65:263–269. https://doi.org/10.1016/j.envexpbot.2008.09.011
Aleman F, Nieves-Cordones M, Martinez V, Rubio F (2011) Root K+ acquisition in plants: the Arabidopsis thaliana model. Plant Cell Physiol 52:1603–1612. https://doi.org/10.1093/pcp/pcr096
Almeida DM, Oliveira MM, Saibo NJM (2017) Regulation of Na+ and K+ homeostasis in plants: towards improved salt stress tolerance in crop plants. Genet Mol Biol 40:326–345. https://doi.org/10.1590/1678-4685-GMB-2016-0106
Anderson JA, Huprikar SS, Kochian LV, Lucas WJ, Gaber RF (1992) Functional expression of a probable Arabidopsis thaliana potassium channel in Saccharomyces cerevisiae. Pro Natl Acad Sci USA 89:3736–3740
Assaha DVM, Ueda A, Saneoka H, Al-Yahyai R, Yaish MW (2017) The role of Na<sup>+</sup> and K<sup>+</sup> transporters in salt stress adaptation in glycophytes. Front Physiol 8:509. https://doi.org/10.3389/fphys.2017.00509
Ayub J, Juri L, Valverde R, Garcia-Sanchez MJ, Fernández JA, Velasco RH (2008) Kinetics of caesium and potassium absorption by roots of three grass pastures and competitive effects of potassium on caesium uptake in Cynodon sp. In: The Natural Radiation Environment: 8th International Symposium (NRE VIII). AIP Publishing 1034:269–272. https://doi.org/10.1063/1.2991224
Basu D, Haswell ES (2017) Plant mechanosensitive ion channels: an ocean of possibilities. Curr Opin Plant Biol 40:43–48. https://doi.org/10.1016/j.pbi.2017.07.002
Benito B, Haro R, Amtmann A, Cuin TA, Dreyer I (2014) The twins K+ and Na+ in plants. J Plant Physiol 171:723–731. https://doi.org/10.1016/j.jplph.2013.10.014
Blatt MR, Grabov A, Brearley J, Kosack KH, Jones JDG (1999) K+ channels of Cf-9 transgenic tobacco guard cells as targets for Cladosporium fulvum Avr9 elicitor-dependent signal transduction. Plant J 19:453–462
Broadley MR, Escobar-Guttierrez AJ, Bowen HC, Willey NJ, White PJ (2001) Influx and accumulation of Cs+ by the akt1 mutant of Arabidopsis thaliana (L.) Heynh. lacking a dominant K+ transport system. J Exp Bot 52:839–844
Burger A, Lichtscheidl I (2018) Stable and radioactive cesium: a review about distribution in the environment, uptake and translocation in plants, plant reactions and plants' potential for bioremediation. Sci Total Environ 618:1459–1485. https://doi.org/10.1016/j.scitotenv.2017.09.298
Buschmann PH, Vaidyanathan R, Gassmann W, Schroeder JI (2000) Enhancement of Na+ uptake currents, time-dependent inward-rectifying K+ channel currents, and K+ channel transcripts by K+ starvation in wheat root cells. Plant Physiol 122:1387–1398. https://doi.org/10.1104/pp.122.4.1387
Cao Y, Jin X, Huang H, Derebe MG, Levin EJ, Kabaleeswaran V, Pan Y, Punta M, Love J, Weng J, Quick M, Ye S, Kloss B, Bruni R, Martinez-Hackert E, Hendrickson WA, Rost B, Javitch JA, Rajashankar KR, Jiang Y, Zhou M (2011) Crystal structure of a potassium ion transporter, TrkH. Nature 471:336–340. https://doi.org/10.1038/nature09731
Carraretto L, Teardo E, Checchetto V, Finazzi G, Uozumi N, Szabo I (2016) Ion channels in plant bioenergetic organelles, chloroplasts and mitochondria: from molecular identification to function. Mol Plant 9:371–395. https://doi.org/10.1016/j.molp.2015.12.004
Chanroj S, Lu Y, Padmanaban S, Nanatani K, Uozumi N, Rao R, Sze H (2011) Plant-specific cation/H+ exchanger 17 and its homologs are endomembrane K+ transporters with roles in protein sorting. J Biol Chem 286:33931–33941. https://doi.org/10.1074/jbc.M111.252650
Chatterjee S, Sarma MK, Deb U, Steinhauser G, Walther C, Gupta DK (2017) Mushrooms: from nutrition to mycoremediation. Environ Sci Pollut Res 24:19480–19493. https://doi.org/10.1007/s11356-017-9826-3
Chen SB, Zhu YG, Hu QH (2005a) Soil to plant transfer of 238U, 226Ra and 232Th on a uranium mining-impacted soil from south eastern China. J Environ Radioact 82:223–236. https://doi.org/10.1016/j.jenvrad.2005.01.009
Chen Z, Newman I, Zhou M, Mendham N, Zhang G, Shabala S (2005b) Screening plants for salt tolerance by measuring K+ flux: a case study for barley. Plant Cell Environ 28:1230–1246. https://doi.org/10.1111/j.1365-3040.2005.01364.x
Chen J, Rennie MD, Sadi B, Zhang W, St-Amant N (2016) A study on the levels of radioactivity in fish samples from the experimental lakes area in Ontario, Canada. J Environ Radioact 153:222–230. https://doi.org/10.1016/j.jenvrad.2016.01.005
Cherel 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
Chrispeels MJ, Crawford NM, Schroeder JI (1999) Proteins for transport of water and mineral nutrients across the membranes of plant cells. Plant Cell 11:661–675. https://doi.org/10.1105/tpc.11.4.661
Collander R (1941) Selective absorption of cations by higher plants. Plant Physiol 16:691
Corratge-Faillie C, Jabnoune M, Zimmermann S, Very AA, Fizames C, Sentenac H (2010) Potassium and sodium transport in non-animal cells: the Trk/Ktr/HKT transporter family. Cell Mol Life Sci 67:2511–2532. https://doi.org/10.1007/s00018-010-0317-7
Cuin TA, Dreyer I, Michard E (2018) The role of potassium channels in Arabidopsis thaliana long distance electrical signalling: AKT2 modulates tissue excitability while GORK shapes action potentials. Int J Mol Sci 19:926. https://doi.org/10.3390/ijms19040926
Czempinski K, Gaedeke N, Zimmermann S, Muller RB (1999) Molecular mechanisms and regulation of plant ion channels. J Exp Bot 50:955–966. https://doi.org/10.1093/jxb/50.Special_Issue.955
Davis JJ (1963) Cesium and its relationship to potassium in ecology. In: Schultz V, Klement AW (eds) Radioecology. Reinhold, New York, pp 539–556
Draxl S, Muller J, Li WB, Michalke B, Scherb H, Hense BA, Tschiersch J, Kanter U, Schäffner AR (2013) Caesium accumulation in yeast and plants is selectively repressed by loss of the SNARE Sec22p/SEC22. Nat Commun 4:2092. https://doi.org/10.1038/ncomms3092
Dreyer I, Blatt MR (2009) What makes a gate? The ins and outs of Kv-like K+ channels in plants. Trend Plant Sci 14:383–390. https://doi.org/10.1016/j.tplants.2009.04.001
Dreyer I, Uozumi N (2011) Potassium channels in plant cells. FEBS Lett 278:4293–4303. https://doi.org/10.1111/j.1742-4658.2011.08371.x
Dreyer I, Antunes S, Hoshi T, Müller RB, Palme K, Pongs O, Reintanz B, Hedrich R (1997) Plant K+ channel alpha-subunits assemble indiscriminately. Biophys J 72:2143. https://doi.org/10.1016/S0006-3495(97)78857-X
Dreyer I, Gomez-Porras JL, Riedelsberger J (2017) The potassium battery: a mobile energy source for transport processes in plant vascular tissues. New Phytol 216:1049–1053. https://doi.org/10.1111/nph.14667
Epstein E, Rains DW, Elzam OE (1963) Resolution of dual mechanisms of potassium absorption by barley roots. Proc Natl Acad Sci U S A 49:684–692
Foulkes M, Millward G, Henderson S, Blake W (2017) Bioaccessibility of U, Th and Pb in solid wastes and soils from an abandoned uranium mine. J Environ Radioact 173:85–96. https://doi.org/10.1016/j.jenvrad.2016.11.030
Fu HH, Luan S (1998) AtKUP1: a dual-affinity K+ transporter from Arabidopsis. Plant Cell 10:63–73
Gajdanowicz P, Garcia-Mata C, Gonzalez W, Morales-Navarro SE, Sharma T, Gonzalez-Nilo FD, Gutowicz J, Mueller-Roeber B, Blatt MR, Dreyer I (2009) Distinct roles of the last transmembrane domain in controlling Arabidopsis K+ channel activity. New Phytol 182:380–391. https://doi.org/10.1111/j.1469-8137.2008.02749.x
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. J Biol Chem 284:21288–21295. https://doi.org/10.1074/jbc.M109.017574
Genies L, Orjollet D, Carasco L, Camilleri V, Frelon S, Vavasseur A, Leonhardt N, Henner P (2017) Uptake and translocation of cesium by Arabidopsis thaliana in hydroponics conditions: links between kinetics and molecular mechanisms. Environ Exp Bot 138:164–172. https://doi.org/10.1016/j.envexpbot.2017.03.013
Gierth M, Maser P (2007) Potassium transporters in plants involvement in K+ acquisition, redistribution and homeostasis. FEBS Lett 581:2348–2356. https://doi.org/10.1016/j.febslet.2007.03.035
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
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
Gupta DK, Walther C (2014) Radionuclide contamination and remediation through plants. Springer, Cham. https://doi.org/10.1007/978-3-319-07665-2
Gupta DK, Walther C (2016) Impact of cesium on plants and the environment. Springer, Cham. https://doi.org/10.1007/978-3-319-41525-3
Gupta DK, Chatterjee S, Dutta S, Voronina AV, Walther C (2016) Radionuclides: accumulation and transport in plants. Rev Environ Contam Toxicol 398:1–22. https://doi.org/10.1007/398_2016_7
Gupta DK, Tawussi F, Hölzer A, Hamann L, Walther C (2017) Investigation of low level 242Pu contamination on nutrition disturbance and oxidative stress in Solanum tuberosum L. Environ Sci Pollut Res 24:16050–15061. https://doi.org/10.1007/s11356-017-9071-9
Hafsi C, Falleh H, Saada M, Ksouri R, Abdelly C (2017) Potassium deficiency alters growth, photosynthetic performance, secondary metabolites content, and related antioxidant capacity in Sulla carnosa grown under moderate salinity. Plant Physiol Biochem 118:609–617. https://doi.org/10.1016/j.plaphy.2017.08.002
Han M, Wu W, Wu WH, Wang Y (2016) Potassium transporter KUP7 is involved in K+ acquisition and translocation in Arabidopsis root under K+-limited conditions. Mol Plant 9:437–446. https://doi.org/10.1016/j.molp.2016.01.012
Hanelt I, Wunnicke D, Muller-Trimbusch M, Vor der BM, Kraus I, Bakker EP, Steinhoff HJ (2010) Membrane region M2C2 in subunit KtrB of the K+ uptake system KtrAB from Vibrio alginolyticus forms a flexible gate controlling K+ flux: an electron paramagnetic resonance study. J Biol Chem 285:28210–28219. https://doi.org/10.1074/jbc.M110.139311
Hedrich R (2012) Ion channels in plants. Physiol Rev 92:1777–1811. https://doi.org/10.1152/physrev.00038.2011
Hedrich R, Becker D (1994) Green circuits-the potential of plant specific ion channels. Plant Mol Biol 26:1637–1650
Hedrich R, Becker D, Geiger D, Marten I, Roelfsema M (2012) Role of ion channels in plants. In: Okada Y (ed) Patch clamp techniques. From beginning to advanced protocols. Springer, Cham, pp 295–232. https://doi.org/10.1007/978-4-431-53993-3
Hille B (2001) Ionic channels of excitable membranes. Sinauer, Sunderland
Hirsch RE, Lewis BD, Spalding EP, Sussman MR (1998) A role for the AKT1 potassium channel in plant nutrition. Science 280:918–921
Horie T, Costa A, Kim TH, Han MJ, Horie R, Leung HY, 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 J 26:3003–3014. https://doi.org/10.1038/sj.emboj.7601732
Hosy E, Vavasseur A, Mouline K, Dreyer I, Gaymard F, Poree F, Boucherez J, Lebaudy A, Bouchez D, Very AA, Simonneau T, Thibaud JB, Sentenac H (2003) The Arabidopsis outward K- channel GORK is involved in regulation of stomatal movements and plant transpiration. Pro Natl Acad Sci USA 100:5549–5554. https://doi.org/10.1073/pnas.0733970100
Hu QH, Weng JQ, Wang JS (2010) Sources of anthropogenic radionuclides in the environment: a review. J Environ Radioact 101:426–437. https://doi.org/10.1016/j.jenvrad.2008.08.004
Ishikawa S, Hayashi S, Abe T, Igura M, Kuramata M, Tanikawa H, Iino M, Saito T, Ono Y, Ishikawa T, Fujimura S, Goto A, Takagi H (2017) Low-cesium rice: mutation in OsSOS2 reduces radiocesium in rice grains. Sci Report 7:2432. https://doi.org/10.1038/s41598-017-02243-9
Ivashikina N, Becker D, Ache P, Meyerhoff O, Felle HH, Hedrich R (2001) K channel profile and electrical properties of Arabidopsis root hairs. FEBS Lett 508:463–469. https://doi.org/10.1016/S0014-5793(01)03114-3
Jan LY, Jan YN (1997) Receptor-regulated ion channels. Curr Opin Cell Biol 9:155–160. https://doi.org/10.1016/S0955-0674(97)80057-9
Kanter U, Hauser A, Michalke B, Draxl S, Schaffner AR (2010) Cesium and strontium accumulation in shoots of Arabidopsis thaliana: genetic and physiological aspects. J Exp Bot 61:3995–4009. https://doi.org/10.1093/jxb/erq213
Kim EJ, Kwak JM, Uozumi N, Schroeder JI (1998) AtKUP1: an Arabidopsis gene encoding high-affinity potassium transport activity. Plant Cell 10:51–62
Kim TH, Bohmer 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 61:561–591. https://doi.org/10.1146/annurev-arplant-042809-112226
Kobayashi D, Uozumi N, Hisamatsu S, Yamagami M (2010) AtKUP/HAK/KT9, a K1 transporter from Arabidopsis thaliana, mediates Cs1 uptake in Escherichia coli. Biosci Biotechnol Biochem 74:203–205. https://doi.org/10.1271/bbb.90638
Kochian LV, Lucas WJ (1993) Can K+ channels do it all? Plant Cell 5:720
Kovler K (2017) The national survey of natural radioactivity in concrete produced in Israel. J Environ Radioact 168:46–53. https://doi.org/10.1016/j.jenvrad.2016.03.002
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
Li L, Kim BG, 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 U S A 103:12625–12630. https://doi.org/10.1073/pnas.0605129103
Li W, Xu G, Alli A, Yu L (2018) Plant HAK/KUP/KT K transporters: function and regulation. Semin Cell Dev Biol 74:133–141. https://doi.org/10.1016/j.semcdb.2017.07.009
Liu K, Luan S (1998) Voltage-dependent K channels as targets of osmosensing in guard cells. Plant Cell 10:1957–1970
Lu Y, Chanroj S, Zulkifli L, Johnson MA, Uozumi N, Cheung A, Sze H (2011) Pollen tubes lacking a pair of K+ transporters fail to target ovules in Arabidopsis. Plant Cell 23:81–93. https://doi.org/10.1105/tpc.110.080499
Maathuis FJM, Sanders D (1996) Mechanisms of potassium absorption by higher plant roots. Physiol Plant 96:158–168. https://doi.org/10.1111/j.1399-3054.1996.tb00197.x
Maathuis FJM, Ichida AM, Sanders D, Schroeder JI (1997) Roles of higher plant K channels. Plant Physiol 114:1141–1149
Martínez-Cordero MA, Martínez V, Rubio F (2004) Cloning and functional characterization of the high-affinity K+ transporter HAK1 of pepper. Plant Mol Biol 56:413–421. https://doi.org/10.1007/s11103-004-3845-4
Martínez-Cordero MA, Martínez V, Rubio F (2005) High-affinity K+ uptake in pepper plants. J Exp Bot 416:1553–1562. https://doi.org/10.1093/jxb/eri150
Mattsson S, Lidén K (1975) 137Cs in carpets of the forest moss Pleurozium schreberi 1961-1973. Oikos 26:323–327
Mian A, Oomen RJ, Isayenkov S, Sentenac H, Maathuis FJM, Very AA (2011) Overexpression of a Na(+) and K(+) -permeable HKT transporter in barley improves salt tolerance. Plant J 68:468–479
Mohamed S, Sentenac H, Guiderdoni E, Véry AA, Nieves-Cordones M (2018) Internal Cs+ inhibits root elongation in rice. Plant Signal Behav 13:e1428516. https://doi.org/10.1080/15592324.2018
Muller RB, Ellenberg J, Provart N, Willmitzer L, Busch H, Becker D, Dietrich P, Hoth S, Hedrich R (1995) Cloning and electrophysiological analysis of KST1, an inward rectifying K- channel expressed in potato guard cells. EMBO J 14:2409–2416
Nakamura RL, Gaber RF (2009) Ion selectivity of the Kat1 K+ channel pore. Mol Membr Biol 26:293–308. https://doi.org/10.1080/09687680903188332
Nakamura RL, McKendree Jr WL, Hirsch RE, Sedbrook JC, Gaber RF, Sussman MR (1995) Expression of an Arabidopsis potassium channel gene in guard cells. Plant Physiol 109:371–374. https://doi.org/10.1104/pp.109.2.371
Nieves-Cordones M, Martínez-Cordero MA, Martínez V, Rubio F (2007) An NH4 +-sensitive component dominates high-affinity K+ uptake in tomato plants. Plant Sci 172:273–280. https://doi.org/10.1016/j.plantsci.2006.09.003
Nieves-Cordones M, Alemán F, Martínez V, Rubio F (2014) K+ uptake in plant roots. The systems involved their regulation and parallels in other organisms. J Plant Physiol 171:688–695. https://doi.org/10.1016/j.jplph.2013.09.021
Nieves-Cordones M, Al Shiblawi FR, Sentenac H (2016a) Roles and transport of sodium and potassium in plants. Met Ions Life Sci 16:291–324 https://doi.org/10.1007/978-3-319-21756-7_9
Nieves-Cordones M, Martínez V, Benito B, Rubio F (2016b) Comparison between Arabidopsis and Rice for main pathways of K(+) and Na(+) uptake by roots. Front Plant Sci 7:992. https://doi.org/10.3389/fpls.2016.00992
Nieves-Cordones M, Mohamed S, Tanoi K, Kobayashi NI, Takagi K, Vernet A, Guiderdoni E, Perin C, Sentenac H, Very AA (2017) Production of low-Cs+ rice plants by inactivation of the K+ transporter OsHAK1 with the CRISPR-Cas system. Plant J 92:43–56. https://doi.org/10.1111/tpj.13632
Nikitin AI, Kryshev II, Bashkirov NI, Valetova NK, Dunaev GE, Kabanov AI, Katrich IY, Krutovsky AO, Nikitin VA, Petrenko GI, Polukhina AM, Selivanova GV, Shkuro VN (2012) Up-to-date concentrations of long-lived artificial radionuclides in the tom and Ob rivers in the area influenced by discharges from Siberian chemical combine. J Environ Radioact 108:15–23. https://doi.org/10.1016/j.jenvrad.2011.11.013
Olondo C, Legarda F, Herranz M, Idoeta R (2017) Validating proposed migration equation and parameters' values as a tool to reproduce and predict 137Cs vertical migration activity in Spanish soils. J Environ Radioact 169-170:40–47 https://doi.org/10.1016/j.jenvrad.2016.12.013
Pacheco-Arjona JR, Ruiz-Lau N, Medina-Lara F, Minero-Garcia Y, echevarria-Machado I, santos-Briones CDL, Martinez-Estevez M (2011) Effects of ammonium nitrate, cesium chloride and tetraethyl ammonium on high-affinity potassium uptake in habanero pepper plantlets (Capsicum chinense Jacq.). Afr J Biotechnol 10:13418–13429. https://doi.org/10.5897/AJB10.2097
Papazian DM, Schwarz TL, Tempel BL, Jan YN, Jan LY (1987) Cloning of genomic and complementary DNA from shaker, a putative potassium channel gene from Drosophila. Science 237:749–753
Prorok VV, Dacenko OI, Bulavin LA, Poperenko LV, White PJ (2016) Mechanistic interpretation of the varying selectivity of Cesium-137 and potassium uptake by radish (Raphanus sativus L.) under field conditions near Chernobyl. J Environ Radioact 152:85–91. https://doi.org/10.1016/j.jenvrad.2015.11.005
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
Qi Z, Hampton CR, Shin R, Barkla BJ, White PJ, Schachtman DP (2008) The high affinity K1 transporter AtHAK5 plays a physiological role in planta at very low K1 concentrations and provides a caesium uptake pathway in Arabidopsis. J Exp Bot 59:595–607. https://doi.org/10.1093/jxb/erm330
Rai H, Yokoyama S, Satoh-Nagasawa N, Furukawa J, Nomi T, Ito Y, Fujimura S, Takahashi H, Suzuki R, Yousra ELM, Goto A, Fuji S, Nakamura S, Shinano T, Nagasawa N, Wabiko H, Hattori H (2017) Cesium uptake by rice roots largely depends upon a single gene, HAK1, which encodes a potassium transporter. Plant Cell Physiol 58:1486–1493 https://doi.org/10.1093/pcp/pcx137
Reintanz B, Szyroki A, Ivashikina N, Ache P, Godde M, Becker D, Palme K, Hedrich R (2002) AtKC1, a silent Arabidopsis potassium channel α-subunit modulates root hair K+ influx. Pro Natl Acad Sci USA 99:4079–4084. https://doi.org/10.1073/pnas.052677799
Riedelsberger J, Dreyer I, Gonzalez W (2015) Outward rectification of voltage-gated K+ channels evolved at least twice in life history. PLoS One 10(9):e0137600. https://doi.org/10.1371/journal.pone.0137600
Roberts SK, Tester M (1995) Inward and outward K+-selective currents in the plasma membrane of protoplasts from maize root cortex and stele. Plant J 8:811–825. https://doi.org/10.1046/j.1365-313X.1995.8060811.x
Ródenas R, García-Legaz MF, López-Gómez E, Martínez V, Rubio F, Botellac MÁ (2017) NO3 −, PO4 3− and SO4 2− deprivation reduced LKT1-mediatedlow-affinity K+ uptake and SKOR-mediated K+ translocation in tomato and Arabidopsis plants. Physiol Plant 160:410–424. https://doi.org/10.1111/ppl.12558
Ródenas R, Nieves-Cordones M, Rivero RM, Martinez V, Rubio F (2018) Pharmacological and gene regulation properties point to the SlHAK5 K+ transporter as a system for high-affinity Cs+ uptake in tomato plants. Physiol Plant 162:455–466. https://doi.org/10.1111/ppl.12652
Rosén K, Vinichuk M (2014) Potassium fertilization and (137) Cs transfer from soil to grass and barley in Sweden after the Chernobyl fallout. J Environ Radioact 130:22–32. https://doi.org/10.1016/j.jenvrad.2013.12.019
Rubio F, Nieves-Cordones M, Alem´an F, Martinez V (2008) Relative contribution of AtHAK5 and AtAKT1 to K+ uptake in the high-affinity range of concentrations. Physiol Planta 134:598–608. https://doi.org/10.1111/j.1399-3054.2008.01168.x
Rubio F, Aleman F, Nieves-Cordones M, Martinez V (2010) Studies on Arabidopsis athak5, atakt1 double mutants disclose the range of concentrations at which AtHAK5, AtAKT1 and unknown systems mediate K+ uptake. Physiol Plant 139:220–228. https://doi.org/10.1111/j.1399-3054.2010.01354.x
Ruiz-Lau N, Bojórquez-Quintal E, Benito B, Echevarría-Machado I, Sánchez-Cach LA, Medina-Lara MF, Martínez-Estévez M (2016) Molecular cloning and functional analysis of a Na+ −insensitive K+ transporter of Capsicum chinense Jacq. Front Plant Sci 7:1980. https://doi.org/10.3389/fpls.2016.01980
Sanches N, Anjos RM, Mosquera B (2008) 40K/137Cs discrimination ratios to the above ground organs of tropical plants. J Environ Radioact 99:1127–1135. https://doi.org/10.1016/j.jenvrad.2008.01.003
Sano T, Becker D, Ivashikina N, Wegner LH, Zimmermann U, Roelfsema MR, Nagata T, Hedrich R (2007) Plant cells must pass a K+ threshold to re-enter the cell cycle. Plant J 50:401–413. https://doi.org/10.1111/j.1365-313X.2007.03071.x
Santa-María GE, Rubio F, Dubcovsky J, Rodríguez-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 9:2281–2289
Santa-Marı́a GE, Danna CH, Czibener C (2000) High-affinity potassium transport in barley roots. Ammonium-sensitive and-insensitive pathways. Plant Physiol 12:297–306. https://doi.org/10.1104/pp.123.1.297
Sassi A, Khan I, Véry AA, Sentenac H (2012) Molecular biology of K+ transport across the plant cell membrane: what do we learn from Arabidopsis and Rice model plants? Intl Potash Inst Anniversary Issue 32. https://www.ipipotash.org/udocs/e-ifc_no32_rf4-molecular-biology.pdf
Schachtman DP, Schroeder JI (1994) Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plants. Nature 370:655–658
Schachtman DP, Schroeder JI, Lucas WJ, Anderson JA, Gaber RF (1992) Expression of an inward-rectifying potassium channel by the Arabidopsis KAT1 cDNA. Science 258:1654–1658
Schroeder JI, Hedrich R (1989) Involvement of ion channels and active transport in osmoregulation and signalling of higher plant cells.Trend Biochem Sci 14:187–192
Schroeder JI, Hedrich R, Fernandez JM (1984) Potassium-selective single channels in guard-cell protoplasts of Vicia faba. Nature 312:361–362
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 256:663–665
Shaw G, Hewamanna R, Lillywhite J, Bell JNB (1992) Radiocaesium uptake and translocation in wheat with reference to the transfer factor concept and ion competition effects. J Environ Radioact 16:167–180
Singh SK, Reddy VR (2017) Potassium starvation limits soybean growth more than the photosynthetic processes across CO2 levels. Front Plant Sci 8:991. https://doi.org/10.3389/fpls.2017.00991
Smolders E, Shaw G (1995) Changes in radioceasium uptake and distribution in wheat during plant development: a solution culture study. Plant Soil 176:1–6
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
Straltsova D, Chykun P, Subramaniam S, Sosan A, Kolbanov D, Sokolik A, Demidchik V (2015) Cation channels are involved in brassinosteroid signalling in higher plants. Steroids 97:98–106. https://doi.org/10.1016/j.steroids.2014.10.008
Stuenkel D (2017) Modeling considerations for ingestion pathway dose calculations using CAP88. Health Phys 112:343–351. https://doi.org/10.1097/HP.0000000000000636
Sugiura Y, Shibata M, Ogata Y, Ozawa H, Kanasashi T, Takenaka C (2016) Evaluation of radiocesium concentrations in new leaves of wild plants two years after the Fukushima Dai-ichi nuclear power plant accident. J Environ Radioact 160:8–24. https://doi.org/10.1016/j.jenvrad.2016.04.015
SunarpiHorie T, Motoda J, Kubo M, Yang H, Yoda K, Horie R, Chan WY, Leung HY, Hattori K, Konomi M, Osumi M, Yamagami M, Schroeder JI, Uozumi N (2005) Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na unloading from xylem vessels to xylem parenchyma cells. Plant J 44:928–938. https://doi.org/10.1111/j.1365-313X.2005.02595.x
Suzuki K, Costa A, Nakayama H, Katsuhara M, Shinmyo A, Horie T (2016) OsHKT2; 2/1-mediated Na+ influx over K+ uptake in roots potentially increases toxic Na+ accumulation in a salt-tolerant landrace of rice Nona Bokra upon salinity stress. J Plant Res 129:67–77. https://doi.org/10.1007/s10265-015-0764-1
Szczerba MW, Britto DT, Kronzucker HJ (2009) K+ transport in plants: physiology and molecular biology. J Plant Physiol 166:447–466. https://doi.org/10.1016/j.jplph.2008.12.009
TermiziRamli A, Wahab A, Hussein MA, Khalik Wood A (2005) Environmental 238U and 232Th concentration measurements in an area of high level natural background radiation at Palong, Johor, Malaysia. J Environ Radioact 80:287–304. https://doi.org/10.1016/j.jenvrad.2004.06.008
Turekian KK, Wedepohl KH (1961) Distribution of the elements in some major units of the Earth’s crust. Geol Soc Am Bull 72:175–191
Unwin N (1989) The structure of ion channels in membranes of excitable cells. Neuron 3:665–676
Uozumi N, Dreyer I (2011) Structure–function correlate in plant ion channels. In: Montal M (ed) Comprehensive biophysics, Vol. 6: channel proteins. Elsevier, Amsterdam
Uozumi N, Schroeder JI (2010) Ion channels and plant stress: past, present and future. In: Demidchik V, Maathuis FJ (eds) Ion channels and plant stress responses. Springer, Berlin, pp 1–22
Uozumi N, Kim EJ, Rubio F, Yamaguchi T, Muto S, Tsuboi A, Bakker EP, Nakamura T, Schroeder JI (2000) The Arabidopsis HKT1 gene homolog mediates inward Na+ currents in Xenopuslaevis oocytes and Na+ uptake in Saccharomyces cerevisiae. Plant Physiol 122:1249–1259. https://doi.org/10.1104/pp.122.4.1249
Vallejo AJ, Peralta ML, Santa-Maria GE (2005) Expression of potassium-transporter coding genes, and kinetics of rubidium uptake, along a longitudinal root axis. Plant Cell Environ 28:850–862. https://doi.org/10.1111/j.1365-3040.2005.01334.x
Very AA, Sentenac H (2002) Cation channels in the Arabidopsis plasma membrane. Trends Plant Sci 7:168–175
Véry AA, Nieves-Cordones M, Daly M, Khan I, Fizames C, Sentenac H (2014) Molecular biology of K+ transport across the plant cell membrane: what do we learn from comparison between plant species? J Plant Physiol 171:748–769. https://doi.org/10.1016/j.jplph.2014.01.011
Voronina AV, Kulyaeva IO, Gupta DK (2018) Determination of the parameters of selective 137Cs sorption onto natural and Ferrocyanide-Modified glauconite and clinoptilolite. 60:35–41. https://doi.org/10.1134/S106636221801006X
Waegeneers N, Sauras-Yera T, Thiry Y, Vallejo VR, Smolders E, Madoz-Escande C (2009) Plant uptake of radiocesium from artificially contaminated soil monoliths covering major European soil types. J Environ Radioact 100:439–444. https://doi.org/10.1016/j.jenvrad.2008.08.011
Walker DJ, Leigh RA, Miller AJ (1996) Potassium homeostasis in vacuolate plant cells. Pro Natl Acad Sci USA 93:10510–10514
Walther C, Gupta DK (2015) Radionuclides in the environment: influence of chemical speciation and plant uptake on radionuclide migration. Springer, Cham. https://doi.org/10.1007/978-3-319-22171-7
Wang Y, Wu WH (2013) Potassium transport and signaling in higher plants. Annu Rev Plant Biol 64:451–476. https://doi.org/10.1146/annurev-arplant-050312-120153
Wang Y, Wu WH (2017) Regulation of potassium transport and signaling in plants. Curr Opin Plant Biol 39:123–128. https://doi.org/10.1016/j.pbi.2017.06.006
Wang XP, Chen LM, Liu WX, Shen LK, Wang FL, Zhou Y, Zhang Z, Wu WH, Wang Y (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
Ward JM, Maser P, Schroeder JI (2009) Plant ion channels: gene families, physiology, and functional genomics analyses. Annu Rev Physiol 71:59–82. https://doi.org/10.1146/annurev.physiol.010908.163204
White PJ, Broadley MR (2000) Mechanisms of caesium uptake by plants. New Phytol 147:241–256
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 125:1347–1360. https://doi.org/10.1016/j.cell.2006.06.011
Yamaguchi T, Hamamoto S, Uozumi N (2013) Sodium transport system in plant cells. Front Plant Sci 4:410. https://doi.org/10.3389/fpls.2013.00410
Zhang YD, Very AA, Wang LM, Deng YW, Sentenac H, Huang DF (2011) A K+ channel from salt-tolerant melon inhibited by Na+. New Phytol 189:856–868. https://doi.org/10.1111/j.1469-8137.2010.03526.x
Zhang T, Chen S, Harmon AC (2014) Protein phosphorylation in stomatal movement. Plant Signal Behav 9(11):e972845. https://doi.org/10.4161/15592316.2014.972845
Zhu YG, Shaw G (2000) Soil contamination with radionuclides and potential remediation. Chemosphere 41:121–128. https://doi.org/10.1016/S0045-6535(99)00398-7
Zhu YG, Smolders E (2000) Plant uptake of radiocaesium: a review of mechanisms, regulation and application. J Exp Bot 51:1635–1645
Zimmermann S, Talke I, Ehrhardt T, Nast G, Müller-Röber B (1998) Characterization of SKT1, an inward rectifying K channel from potato, by heterologous expression in insect cells. Plant Physiol 116:879–890
Acknowledgements
DKG and CW are thankful to BMBF, Germany (Funding no. 02S9276D). S.C. is thankful to Director, DRDO, Assam, India. The authors apologize for the many colleagues who are not referenced in this work due to space limitations.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of interest and contributions statement
All the authors listed have approved this manuscript and worked equally and there is no conflict of interest to publish this MS.
Rights and permissions
About this article
Cite this article
Gupta, D.K., Tiwari, S., Chatterjee, S. et al. Potassium and its role in cesium transport in plants. Biologia 73, 885–896 (2018). https://doi.org/10.2478/s11756-018-0110-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.2478/s11756-018-0110-x