Research Paper

Identification and characterization of potassium (K+) transporters in potato (Solanum tuberosum L.)

Wan Li, Min Cheng, Yongping Zhao

Published on: 10 August 2022

Page: 422 - 434

DOI: 10.6165/tai.2022.67.422


Potassium (K+) transporter genes have important roles in K+ acquisition, allocation and signal transduction. The purpose of this study was to analyze the characteristics of the K+ transporter genes/proteins and to study their expression profiles under K+ deficiency condition in potato (Solanum tuberosum). Strict homology searches were used to find 33 K+ transporter genes located on potato chromosomes 1 to 12. Gene features, protein features and subcellular Localization were analyzed, and 10 segment duplications were identified from these 33 genes. The functions of K+ transporter genes were predicted by phylogenetic analysis and analysis of promoter sequences. After Potassium starvation, 12, 13 and 18 K+ transporter genes were up regulated in roots, stems and leaves, respectively. In addition, the expression of StHAK5, StHAK11 and StKCO2 were up-regulated in potato roots, stems and leaves under phosphate deficiency. Our findings provide a comprehensive view of members of the K+ transporter family involved in the response to K+ starvation growth.

Keyword: K+ starvation, Potassium transporters, Promoter site, Solanum tuberosum

Literature Cited

Ahn, S. J., R. Shin and D.P. Schachtman 2004. Expression of KT/KUP genes in Arabidopsis and the role of root hairs in K+ uptake. Plant Physiol. 134(3): 1135–1145.
DOI: 10.1104/pp.103.034660View Article Google Scholar

Amrutha, R.N., P.N. Sekhar, R.K. Varshney and P.B.K. Kishor 2007. Genome-wide analysis and identification of genes related to potassium transporter families in rice (Oryza sativa L.). Plant Sci. 172(4): 708–721.
DOI: 10.1016/j.plantsci.2006.11.019View Article Google Scholar

Amtmann, A., J.P. Hammond, P. Armengaud and P.J. White 2006. Nutrient sensing and signalling in plants: Potassium and Phosphorus. Adv. Bot. Res. 43: 209–257.
DOI: 10.1016/S0065-2296(05)43005-0View Article Google Scholar

Ansch?tz, U., D. Becker and S. Shabala 2014. Going beyond nutrition: regulation of potassium homoeostasis as a common denominator of plant adaptive responses to environment. J. Plant Physiol. 171(9): 670–687.
DOI: 10.1016/j.jplph.2014.01.009View Article Google Scholar

Aranda-Sicilia, M.N., A. Aboukila, U. Armbruster, O. Cagnac, T. Schumann, H.H. Kunz, P. Jahns, M.P. Rodr?guez-Rosales, H. Sze and K. Venema 2016. Envelope K+/H+ Antiporters AtKEA1 and AtKEA2 Function in Plastid Development. Plant Physiol. 172(1): 441–449.
DOI: 10.1104/pp.16.00995View Article Google Scholar

Aranda-Sicilia, M.N., O. Cagnac, S. Chanroj, H. Sze, M.P. Rodr?guez-Rosales and K. Venema 2012. Arabidopsis KEA2, a homolog of bacterial KefC, encodes a K+/H+ antiporter with a chloroplast transit peptide. Biochim. Biophys. Acta (BBA) - Biomembranes 1818(9): 2362–2371.
DOI: 10.1016/j.bbamem.2012.04.011View Article Google Scholar

Ba?uelos, M.A., B. Garciadeblas, B. Cubero and A. Rodr?guez-Navarro 2002. Inventory and Functional Characterization of the HAK Potassium Transporters of Rice. Plant Physiol. 130(2): 784–795.
DOI: 10.1104/pp.007781View Article Google Scholar

Cellier, F., G. Con?j?ro, L. Ricaud, D.T. Luu, M. Lepetit, F. Gosti and F. Casse 2004. Characterization of AtCHX17, a member of the cation/H+ exchangers, CHX family, from Arabidopsis thaliana suggests a role in K+ homeostasis. Plant J. 39(6): 834–846.
DOI: 10.1111/j.1365-313X.2004.02177.xView Article Google Scholar

Chen, G., Q. Hu, L. Luo, T. Yang, S. Zhang, Y. Hu, L. Yu and G. Xu 2016. 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(12): 2747–2765.
DOI: 10.1111/pce.12585View Article Google Scholar

Chen, H., H. He and D. Yu 2011. Overexpression of a novel soybean gene modulating Na? and K? transport enhances salt tolerance in transgenic tobacco plants. Physiol. Plant. 141(1): 11–18.
DOI: 10.1111/j.1399-3054.2010.01412.xView Article Google Scholar

Ch?rel, I., E. Michard, N. Platet, K. Mouline, C. Alcon, H. Sentenac and J.B. Thibaud 2002. Physical and Functional Interaction of the Arabidopsis K+ Channel AKT2 and Phosphatase AtPP2CA. Plant Cell 14(5): 1133–1146.
DOI: 10.1105/tpc.000943View Article Google Scholar

Czempinski, K., S. Zimmermann, T. Ehrhardt, and B. M?ller?R?ber 2014. New structure and function in plant K+ channels: KCO1, an outward rectifier with a steep Ca2+ dependency. EMBO J. 16(10): 2565–2575.
DOI: 10.1093/emboj/16.10.2565View Article Google Scholar

Davies, C., R. Shin, W. Liu, M.R. Thomas and D.P. Schachtman 2006. Transporters expressed during grape berry (Vitis vinifera L.) development are associated with an increase in berry size and berry potassium accumulation. J. Exp. Bot. 57(12): 3209–3216.
DOI: 10.1093/jxb/erl091View Article Google Scholar

Dennison, K.L., W.R. Robertson, B.D. Lewis, R.E. Hirsch, M.R. Sussman and E.P. Spalding 2001. Functions of AKT1 and AKT2 potassium channels determined by studies of single and double mutants of Arabidopsis. Plant Physiol. 127(3): 1012–1019.
DOI: 10.1104/pp.010193View Article Google Scholar

Drews, O., G. Reil, H. Parlar and A. G?rg 2004. Setting up standards and a reference map for the alkaline proteome of the Gram-positive bacterium Lactococcus lactis. Proteomics 4(5): 1293–1304.
DOI: 10.1002/pmic.200300720View Article Google Scholar

Dreyer, I., F. Por?e, A. Schneider, J. Mittelst?dt, A. Bertl, H. Sentenac, J.B. Thibaud and B. Mueller-Roeber 2004. Assembly of plant Shaker-Like Kout channels requires two distinct sites of the channel α-Subunit. Biophys. J. 87(2): 858–872.
DOI: 10.1529/biophysj.103.037671View Article Google Scholar

Elumalai, R.P., P. Nagpal and J.W. Reed 2002. A mutation in the Arabidopsis KT2/KUP2 potassium transporter gene affects shoot cell expansion. Plant Cell 14(1): 119–131.
DOI: 10.1105/tpc.010322View Article Google Scholar

Fu, H.H. and S. Luan. 1998. AtKUP1: A dual-affinity K+ transporter from Arabidopsis. Plant Cell 10(1): 63–73.
DOI: 10.1105/tpc.10.1.63View Article Google Scholar

Gaber, R.F., C.A. Styles and G.R. Fink 1988. TRK1 Encodes a plasma membrane protein required for high-affinity potassium transport in Saccharomyces cerevisiae. Mol. Cell. Biol. 8(7): 2848–2859.
DOI: 10.1128/MCB.8.7.2848View Article Google Scholar

Gajdanowicz, P., E. Michard, M. Sandmann, M. Rocha, L.G. Corr?a, S.J. Ram?rez-Aguilar, J.L. Gomez-Porras, W. Gonz?lez, J.B. Thibaud, J.T. van Dongen and I. Dreyer 2011. Potassium (K+) gradients serve as a mobile energy source in plant vascular tissues. Proc. Natl. Acad. Sci. USA 108(2): 864–869.
DOI: 10.1073/pnas.1009777108View Article Google Scholar

Gaymard, F., G. Pilot, B. Lacombe, D. Bouchez, D. Bruneau, J. Boucherez, N. Michaux-Ferri?re, J.B. Thibaud and H. Sentenac 1998. Identification and disruption of a plant shaker-like outward channel involved in K+ release into the xylem sap. Cell 94(5): 647–655.
DOI: 10.1016/S0092-8674(00)81606-2View Article Google Scholar

Gierth, M. and P. M?ser 2007. Potassium transporters in plants – Involvement in K+ acquisition, redistribution and homeostasis. FEBS Lett. 581(12): 2348–2356.
DOI: 10.1016/j.febslet.2007.03.035View Article Google Scholar

Goldstein, S.A., L.A. Price, D.N. Rosenthal and M.H. Pausch 1996. ORK1, a potassium-selective leak channel with two pore domains cloned from Drosophila melanogaster by expression in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 93(23): 13256–13261.
DOI: 10.1073/pnas.93.23.13256View Article Google Scholar

Grabov, A. 2007. Plant KT/KUP/HAK potassium transporters: single family – Multiple functions. Ann. Bot.-London 99(6): 1035–1041.
DOI: 10.1093/aob/mcm066View Article Google Scholar

Gu, Z., A. Cavalcanti, F.C. Chen, P. Bouman and W.H. Li 2002. Extent of gene duplication in the genomes of Drosophila, nematode, and yeast. Mol. Biol. Evol. 19(3): 256–262.
DOI: 10.1093/oxfordjournals.molbev.a004079View Article Google Scholar

Han, L., J.L. Li, L. Wang, W.M. Shi and Y.H. Su 2015. Identification and localized expression of putative K+/H+ antiporter genes in Arabidopsis. Acta Physiol. Plant 37(5): 1–14.
DOI: 10.1007/s11738-015-1845-4View Article Google Scholar

Heginbotham, L., T. Abramson and R. Mackinnon 1992. A functional connection between the pores of distantly related ion channels as revealed by mutant K+ channels. Science 258(5085): 1152–1155.
DOI: 10.1126/science.1279807View Article Google Scholar

Hille, B. 1992. Ionic Channels of Excitable Membranes. Neurology. 42(7): 1439–1439.
DOI: 10.1212/WNL.42.7.1439-aView Article Google Scholar

Hoagland, D.R. and D.I. Arnon 1950. The water-culture method for growing plants without soil. Univ. Calif. Agric. Exp. Stn. 347: 1–32.

Horie, T., A. Costa, T.H. Kim, M.J. Han, R. Horie, H.Y. Leung, A. Miyao, H. Hirochika, G. An and J.I. Schroeder 2014. Rice OsHKT2;1 transporter mediates large Na+ influx component into K+-starved roots for growth. EMBO J. 26(12): 3003–3014.
DOI: 10.1038/sj.emboj.7601732View Article Google Scholar

Hosy, E., A. Vavasseur, K. Mouline, I. Dreyer, F. Gaymard, F. Por?e, J. Boucherez, A. Lebaudy, D. Bouchez, A.A. V?ry, T. Simonneau, J.B. Thibaud and H. Sentenac 2003. The Arabidopsis outward K+ channel GORK is involved in regulation of stomatal movements and plant transpiration. Proc. Natl. Acad. Sci. USA 100(9): 5549–5554.
DOI: 10.1073/pnas.0733970100View Article Google Scholar

Jiang, S.Y., J.M. Gonz?lez and S. Ramachandran 2013. Comparative genomic and transcriptomic analysis of tandemly and segmentally duplicated genes in Rice. PLoS One 8(5): e63551.
DOI: 10.1371/journal.pone.0063551View Article Google Scholar

Kader, M.A. and S. Lindberg 2005. Uptake of sodium in protoplasts of salt-sensitive and salt-tolerant cultivars of rice, Oryza sativa L. determined by the fluorescent dye SBFI. J Exp Bot. 56(422): 3149–3158.
DOI: 10.1093/jxb/eri312View Article Google Scholar

Ketchum, K.A., W.J. Joiner, A.J. Sellers, L.K. Kaczmarek and S.A. Goldstein 1995. A new family of outwardly rectifying potassium channel proteins with two pore domains in tandem. Nature 376(6542): 690–695.
DOI: 10.1038/376690a0View Article Google Scholar

Kim, E.J., J.M. Kwak, N. Uozumi and J.I. Schroeder 1998. AtKUP1: An Arabidopsis gene encoding high-affinity potassium transport activity. Plant Cell 10(1): 51–62.
DOI: 10.1105/tpc.10.1.51View Article Google Scholar

Krzywinski, M., J. Schein, I. Birol, J. Connors, R. Gascoyne, D. Horsman, S.J. Jones and M.A. Marra 2009. Circos: An information aesthetic for comparative genomics. Genome Res. 19(9): 1639–1645.
DOI: 10.1101/gr.092759.109View Article Google Scholar

Kunz, H.H., M. Gierth, A. Herdean, M. Satoh-Cruz, D.M. Kramer, C. Spetea and J.I. Schroeder 2014. Plastidial transporters KEA1, -2, and -3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis. Proc. Natl. Acad. Sci. USA 111(20): 7480–7485.
DOI: 10.1073/pnas.1323899111View Article Google Scholar

Lacombe, B., G. Pilot, E. Michard, F. Gaymard, H. Sentenac and J.B. Thibaud 2000. A shaker-like K+ channel with weak rectification is expressed in both source and sink phloem tissues of Arabidopsis. Plant Cell 12(6): 837–851.
DOI: 10.1105/tpc.12.6.837View Article Google Scholar

Lam, E. and N.H. Chua 1989. ASF-2: A factor that binds to the cauliflower mosaic virus 35S promoter and a conserved GATA motif in Cab Promoters. Plant Cell. 1(12): 1147–1156.
DOI: 10.1105/tpc.1.12.1147View Article Google Scholar

Langer, K., P. Ache, D. Geiger, A. Stinzing, M. Arend, C. Wind, S. Regan, J. Fromm and R. Hedrich 2002. Poplar potassium transporters capable of controlling K+ homeostasis and K+-dependent xylogenesis. Plant J. 32(6): 997–1009.
DOI: 10.1046/j.1365-313X.2002.01487.xView Article Google Scholar

Leigh, R.A. and R.G.W. Jones 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): 1–13.
DOI: 10.1111/j.1469-8137.1984.tb04103.xView Article Google Scholar

Lescot, M., P. D?hais, G. Thijs, K. Marchal, Y. Moreau, Y. Van de Peer, P. Rouz? and S. Rombauts 2002. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 30(1): 325–327.
DOI: 10.1093/nar/30.1.325View Article Google Scholar

Li, J., Z. Zhang, S. Vang, J. Yu, G.K.S. Wong and J. Wang 2009. Correlation between Ka/Ks and Ks is related to substitution model and evolutionary lineage. J. Mol. Evol. 68(4): 414–423.
DOI: 10.1007/s00239-009-9222-9View Article Google Scholar

Librado, P. and J. Rozas 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11): 1451–1452.
DOI: 10.1093/bioinformatics/btp187View Article Google Scholar

Liu, B., G. Zhang, A. Murphy, D.D. Koeyer, H. Tai, B. Bizimungu, H. Si and X.Q. Li 2016. Differences between bud-end and stem-end of potatoes in dry matter content, starch granule size, and carbohydrate metabolic gene Expression at the Growing and Sprouting Stages. J. Agric. Food Chem. 64(5): 1176–1184.
DOI: 10.1021/acs.jafc.5b05238View Article Google Scholar

Liu, B., S. Zhao, X. Wu, X. Wang, Y. Nan, D. Wang and Q. Chen 2017. Identification and characterization of phosphate transporter genes in potato. J. Biotechnol. 264: 17–28.
DOI: 10.1016/j.jbiotec.2017.10.012View Article Google Scholar

Liu, F., Y. Xu, H. Jiang, C. Jiang, Y. Du, C. Gong, W. Wang, S. Zhu, G. Han and B. Cheng 2016. Systematic identification, evolution and expression analysis of the Zea mays PHT1 gene family reveals several new members involved in root colonization by arbuscular mycorrhizal fungi. Int. J. Mol. Sci. 17(6): 930.
DOI: 10.3390/ijms17060930View Article Google Scholar

Lynch, M. and J.S. Conery 2000. The evolutionary fate and consequences of duplicate genes. Science. 290(5459): 1151–1155.
DOI: 10.1126/science.290.5494.1151View Article Google Scholar

Maathuis, F.J.M., A.M. Ichida, D. Sanders and J.I. Schroeder 1997. Roles of higher plant K+ channels. Plant Physiol. 114(4): 1141–1149.
DOI: 10.1104/pp.114.4.1141View Article Google Scholar

M?ser, P., B. Eckelman, R. Vaidyanathan, T. Horie, D.J. Fairbairn, M. Kubo, M. Yamagami, K. Yamaguchi, M. Nishimura, N. Uozumi, W. Robertsonf, M.R. Sussmanf and J.I. Schroeder 2002. Altered shoot/root Na+ distribution and bifurcating salt sensitivity in Arabidopsis by genetic disruption of the Na+ transporter AtHKT1. FEBS Lett. 531(2): 157–161.
DOI: 10.1016/S0014-5793(02)03488-9View Article Google Scholar

M?ser, P., S. Thomine, J.I. Schroeder, J.M. Ward, K. Hirschi, H. Sze, I.N. Talke, A. Amtmann, F.J.M. Maathuis, D. Sanders, J.F. Harper, J. Tchieu, M. Gribskov, M.W. Persans, D.E. Salt, S.A. Kim and M.L Guerinot 2001. Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol. 126(4): 1646–1667.
DOI: 10.1104/pp.126.4.1646View Article Google Scholar

Munro, A.W., G.Y. Ritchie, A.J. Lamb, R.M. Douglas and I.R. Booth 2010. The cloning and DNA sequence of the gene for the glutathione-regulated potassium-efflux system KefC of Escherichia coli. Mol. Microbiol. 5(3): 607–616.
DOI: 10.1111/j.1365-2958.1991.tb00731.xView Article Google Scholar

Nieves-Cordones, M., M.A. Mart?nez-Cordero, V. Mart?nez and F. Rubio 2007. An NH4+-sensitive component dominates high-affinity K+ uptake in tomato plants. Plant Sci. 172(2): 273–280.
DOI: 10.1016/j.plantsci.2006.09.003View Article Google Scholar

Nieves-Cordones, M., A.J. Miller, A. Fernando, M. Vicente and R. Francisco 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(6): 521–532.
DOI: 10.1007/s11103-008-9388-3View Article Google Scholar

Osakabe, Y., N. Arinaga, T. Umezawa, S. Katsura, K. Nagamachi, H. Tanaka, H. Ohiraki, K. Yamada, S.U. Seo, M. Abo, E. Yoshimura, K. Shinozaki and K. Yamaguchi-Shinozaki 2013. Osmotic stress responses and plant growth controlled by potassium transporters in Arabidopsis. Plant Cell 25(2): 609–624.
DOI: 10.1105/tpc.112.105700View Article Google Scholar

Quintero, F.J. and M.R. Blatt 1997. A new family of K+ transporters from Arabidopsis that are conserved across phyla. FEBS Lett. 415(2): 206–211.
DOI: 10.1016/S0014-5793(97)01125-3View Article Google Scholar

Reintanz, B., A. Szyroki, N. Ivashikina, P. Ache, M. Godde, D. Becker, K. Palme and R. Hedrich 2002. AtKC1, a silent Arabidopsis potassium channel alpha-subunit modulates root hair K+ influx. Proc. Natl. Acad. Sci. USA 99(6): 4079–4084.
DOI: 10.1073/pnas.052677799View Article Google Scholar

Rigas, S., G. Debrosses, K. Haralampidis, F. Vicente-Agullo, K.A. Feldmann, A. Grabov, L. Dolan and P. Hatzopoulos 2001. TRH1 Encodes a potassium transporter required for tip growth in Arabidopsis root hairs. Plant Cell 13(1): 139–151.
DOI: 10.2307/3871159View Article Google Scholar

Rigas, S., F.A. Ditengou, K. Ljung, G. Daras, O. Tietz, K. Palme and P. Hatzopoulos 2013. Root gravitropism and root hair development constitute coupled developmental responses regulated by auxin homeostasis in the Arabidopsis root apex. New Phytol. 197(4): 1130–1141.
DOI: 10.1111/nph.12092View Article Google Scholar

Rocchetti, A., T. Sharma, C. Wulfetange, J. Scholzstarke, A. Grippa, A. Carpaneto, I. Dreyer, A. Vitale, K. Czempinski and E. Pedrazzini 2012. The putative K+ channel subunit AtKCO3 forms stable dimers in Arabidopsis. Front. Plant Sci. 3: 251.
DOI: 10.3389/fpls.2012.00251View Article Google Scholar

Rodr?guez-Navarro, A. 2000. Potassium transport in fungi and plants. Biochim. Biophys. Acta (BBA) - Biomembranes 1469(1): 1–30.
DOI: 10.1016/S0304-4157(99)00013-1View Article Google Scholar

Ruan, Y.L., D.J. Llewellyn and R.T. Furbank 2001. The control of single-celled cotton fiber elongation by developmentally reversible gating of plasmodesmata and coordinated expression of sucrose and K+ transporters and expansin. Plant Cell 13(1): 47–60.
DOI: 10.1105/tpc.13.1.47View Article Google Scholar

Rubio, F., G.E. Santa-Mar?a and A. Rodr?guez-Navarro 2001. Cloning of Arabidopsis and barley cDNAs encoding HAK potassium transporters in root and shoot cells. Physiol. Plantarum 109(1): 34–43.
DOI: 10.1034/j.1399-3054.2000.100106.xView Article Google Scholar

Rus, A., B.H. Lee, A. Munoz-Mayor, A. Sharkhuu, K. Miura, J.K. Zhu, R.A. Bressan and P.M. Hasegawa 2004. AtHKT1 Facilitates Na+ homeostasis and K+ nutrition in planta. Plant Physiol. 136(1): 2500–2511.
DOI: 10.1104/pp.104.042234View Article Google Scholar

Santa-Mar?a, G.E., F. Rubio, J. Dubcovsky and A. Rodr?guez-Navarro 1997. The HAKl gene of barley is a member of a large gene family and encodes a high-affinity potassium transporter. Plant Cell 9(12): 2281–2289.
DOI: 10.1105/tpc.9.12.2281View Article Google Scholar

Sarkar, C. and A. Maitra 2008. Deciphering the cis-regulatory elements of co-expressed genes in PCOS by in silico analysis. Gene 408(1-2): 72–84.
DOI: 10.1016/j.gene.2007.10.026View Article Google Scholar

Schachtman, D.P. and R. Shin 2007. Nutrient sensing and signaling: NPKS. Annu. Rev. Plant Biol. 58(1): 47–69.
DOI: 10.1146/annurev.arplant.58.032806.103750View Article Google Scholar

Schleyer, M. and E.P. Bakker 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(21): 6925–6931.
DOI: 10.1128/jb.175.21.6925-6931.1993View Article Google Scholar

Sch?nknecht, G., P. Spoormaker, R. Steinmeyer, L. Br?ggeman, P. Ache, R. Dutta, B. Reintanz, M. Godde, R. Hedrich and K. Palme 2002. KCO1 is a component of the slow-vacuolar (SV) ion channel. FEBS Lett. 511(1-3): 28–32.
DOI: 10.1016/S0014-5793(01)03273-2View Article Google Scholar

Schroeder, J.I., J.M. Ward and W. Gassmann 1994. Perspecives on the physiology and structues of inwardrectifying K+ channels in higher plants: Biophysical Implications for K+ Uptake. Annu. Rev. Biophys. Biomol. Struct. 23(1): 441–471.
DOI: 10.1146/ Article Google Scholar

Shen, Y., L. Shen, Z. Shen, W. Jing, H. Ge, J. Zhao and W. Zhang 2016. The potassium transporter OsHAK21 functions in the maintenance of ion homeostasis and tolerance to salt stress in rice. Plant Cell Environ. 38(12): 2766–2779.
DOI: 10.1111/pce.12586View Article Google Scholar

Sunarpi, T. Horie, J. Motoda, M. Kubo, H. Yang, K. Yoda, R. Horie, W.Y. Chan, H.Y. Leung, K. Hattori, M. Konomi, M. Osumi, M. Yamagami, J.I. Schroeder and N. Uozumi 2005. Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na+ unloading from xylem vessels to xylem parenchyma cells. Plant J. 44(6): 928–938.
DOI: 10.1111/j.1365-313X.2005.02595.xView Article Google Scholar

Suzuki, M., K. Takahashi, M. Ikeda, H. Hayakawa, A. Ogawa, Y. Kawaguchi and O. Sakai 1994. Cloning of a pH-sensitive K+ channel possessing two transmembrane segments. Nature 367(6464): 642–645.
DOI: 10.1038/367642a0View Article Google Scholar

Sze, H., M. Geisler and A.S. Murphy 2014. Linking the evolution of plant transporters to their functions. Front. Plant Sci. 4: 547.
DOI: 10.3389/fpls.2013.00547View Article Google Scholar

Sze, H., S. Padmanaban, F. Cellier, D. Honys, N.H. Cheng, K.W. Bock, G. Con?j?ro, X. Li, D. Twell, J.M. Ward and K.D. Hirschi 2004. Expression patterns of a novel AtCHX gene family highlight potential roles in osmotic adjustment and K+ homeostasis in pollen development. Plant Physiol. 136(1): 2532–2547.
DOI: 10.1104/pp.104.046003View Article Google Scholar

Tempel, B.L., D.M. Papazian, T.L. Schwarz, Y.N. Jan and L.Y. Jan 1987. Sequence of a probable potassium channel component encoded at Shaker Locus of Drosophila. Science. 237(4816): 770–775.
DOI: 10.1126/science.2441471View Article Google Scholar

Terzaghi, W.B. and A.R. Cashmore 1995. Light-Regulated transcription. Annu. Rev. Plant physiol. Mol. Biol. 46(1): 445–474.
DOI: 10.1146/annurev.pp.46.060195.002305View Article Google Scholar

Tester, M. and R. Davenport 2003. Na+ tolerance and Na+ transport in higher plants. Ann. Bot.-London 91(5): 503–527.
DOI: 10.1093/aob/mcg058View Article Google Scholar

Uozumi, N., E.J. Kim, F. Rubio, T. Yamaguchi, S. Muto, A. Tsuboi, E.P. Bakker, T. Nakamura and J.I. Schroeder 2000. The Arabidopsis HKT1 gene homolog mediates inward Na+ currents in Xenopus laevis oocytes and Na+ uptake in Saccharomyces cerevisiae. Plant Physiol. 122(4): 1249–1260.
DOI: 10.1104/pp.122.4.1249View Article Google Scholar

V?ry, A.A. and H. Sentenac 2003. Molecular mechanisms and regulation of K+ transport in higher plants. Annu. Rev. Plant Biol. 54(1): 575–603.
DOI: 10.1146/annurev.arplant.54.031902.134831View Article Google Scholar

Vicente-Agullo, F., S. Rigas, G. Desbrosses, L. Dolan, P. Hatzopoulos and A. Grabov 2004. Potassium carrier TRH1 is required for auxin transport in Arabidopsis roots. Plant J. 40(4): 523–535.
DOI: 10.1111/j.1365-313X.2004.02230.xView Article Google Scholar

Wang, M., Q. Zheng, Q. Shen and S. Guo 2013. The critical role of potassium in plant stress response. Int. J. Mol. Sci. 14(4): 7370–7390.
DOI: 10.3390/ijms14047370View Article Google Scholar

Wang, Y. and W. Wu 2009. Molecular genetic mechanism of high efficient potassium uptake in plants. Chinese Bulletin of Botany 44: 27–36.

Wang, Y. and W.H. Wu 2010. Plant sensing and signaling in response to K+-deficiency. Mol. Plant. 3(2): 280–287.
DOI: 10.1093/mp/ssq006View Article Google Scholar

Wang, Y. and W.H. Wu 2013. Potassium transport and signaling in higher plants. Annu. Rev. Plant Biol. 64(1): 451–476.
DOI: 10.1146/annurev-arplant-050312-120153View Article Google Scholar

Waters, S., M. Gilliham and M. Hrmova 2013. Plant high-affinity potassium (HKT) transporters involved in salinity tolerance: Structural insights to probe differences in ion selectivity. Int. J. Mol. Sci. 14(4): 7660–7680.
DOI: 10.3390/ijms14047660View Article Google Scholar

Yang, X., G.A. Tuskan and M.Z. Cheng 2006. Divergence of the dof gene families in poplar, Arabidopsis, and rice suggests multiple modes of gene evolution after duplication. Plant Physiol. 142(3): 820–830.
DOI: 10.1104/pp.106.083642View Article Google Scholar

Yang, X.E., J.X. Liu, W.M. Wang, Z.Q. Ye and A.C. Luo 2004. Potassium internal use efficiency relative to growth vigor, potassium distribution, and carbohydrate allocation in rice genotypes. J. Plant Nutr. 27(5): 837–852.
DOI: 10.1081/PLN-120030674View Article Google Scholar

Zhang, Z., J. Li, X.Q. Zhao, J. Wang, K.S. Wong and J. Yu 2006. KaKs_calculator: Calculating Ka and Ks through model selection and model averaging. Genom. Proteom. Bioinf. 4(4): 259–263.
DOI: 10.1016/S1672-0229(07)60007-2View Article Google Scholar