ISSN 0564-3783  

Main page
Information to authors
Editorial board
Mobile version

In Ukrainian

Export citations

Otassium transport systems and their role in stress response, plant growth and development

Nestrerenko E.O., Krasnoperova O.E., Isayenkov S.V.


SUMMARY. In this reviewer the K+ transport systems were selected and characterized. Detailed literature analysis and data summarising regarding main members of K+ transport systems, their biological roles in plant growth and developments, mechanisms of abiotic stress tolerance were conducted. The processes of K+ uptake, transport tissue and cellular distribution were described. Structure characteristic and topology of K+ transport proteins, their role in function specificity were analysed. The role of these membrane transport proteins in signaling, drought and salt tolerance or K+ deficiency were critically evaluated. The new perspective directions for further research of K+ transport proteins were suggested.

Key words: potassium transport, two-pore TPK channels, Shaker-like channels, Kir-like channels, nonselective cation channels NCCC, KUP/HAK/KT transporters, Trk/HKT transporters, CPA transporters

Tsitologiya i Genetika 2021, vol. 55, no. 1, pp. 75-92

  1. Institute of Food Biotechnology and Genomics, NAS of Ukraine, Osipovskogo str. 2a, 04123, Kyiv, Ukraine
  2. Institute of Molecular Biology and Genetics NAS of Ukraine, Zabolotnogo str. 150, 03143, Kyiv, Ukraine

E-mail: yevheniya.nesterenko, krasnopio524, stan.isayenkov

Nestrerenko E.O., Krasnoperova O.E., Isayenkov S.V. Otassium transport systems and their role in stress response, plant growth and development, Tsitol Genet., 2021, vol. 55, no. 1, pp. 75-92.

In "Cytology and Genetics":
E. O. Nestrerenko, O. E. Krasnoperova & S. V. Isayenkov Potassium Transport Systems and Their Role in Stress Response, Plant Growth, and Development, Cytol Genet., 2021, vol. 55, no. 1, pp. 6379
DOI: 10.3103/S0095452721010126


1. Ahmad, I. and Maathuis, F.J.M., Cellular and tissue distribution of potassium: physiological relevance, mechanisms and regulation, J. Plant Physiol., 2013, vol. 171, no. 9, pp. 708714.

2. Ahmad, I., Devonshire, J., Mohamed, R.M.M.E., et al., Overexpression of the potassium channel TPKb in small vacuoles confers osmotic and drought tolerance to rice, New Phytol., 2016, vol. 209, no. 3, pp. 10401048.

3. Ali, R., Zielinski, R.E., and Berkowitz, G.A., Expression of plant cyclic nucleotide-gated cation channels in yeast, J. Exp. Bot., 2006, vol. 57, no. 1, pp. 125138.

4. Almeida, P., Katschnig, D., and de Boer, A.H., HKT transportersstate of the art, Int. J. Mol. Sci., 2013, vol. 14, no. 10, pp. 2035920385.

5. Amtamnn, A., Troufflard, S., and Armengaud, P., The effect of potassium nutrition on pest and disease resistance in plants, Physiol. Plant., 2008, vol. 133, pp. 682691.

6. Apse, M.P., Aharon, G.S., Snedden, W.A., et al., Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis, Science, 1999, vol. 285, no. 5431, pp. 12561288.

7. Aranda-Sicilia, M.N., Aboukila, A., Armbruster, U., et al., Envelope K+/H+ antiporters AtKEA1 and AtKEA2 function in plastid development, Plant Physiol., 2016, vol. 172, no. 1, pp. 441449.

8. Ayadi, M., Ayed, R.B., Mzid, R., et al., Computational approach for structural feature determination of grapevine NHX antiporters, Biomed. Res. Int., 2019a, vol. 2019, pp. 113.

9. Ayadi, M., Martins, V., Ayed, R.B., et al., Genome wide identification, molecular characterization, and gene expression analyses of grapevine NHX antiporters suggest their involvement in growth, ripening, seed dormancy, and stress response, Biochem. Genet., 2019b, vol. 58, no. 1, pp. 102128.

10. Barragan, V., Leidi, E.O., Andres, Z., et al., Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis, Plant Cell, 2012, vol. 24, no. 3, pp. 11271142.

11. Bassil, E., Blumwald, E., and Coku, A., Cellular ion homeostasis: emerging roles of intracellular NHX Na+/H+ antiporters in plant growth and development, J. Exp. Bot., 2012, vol. 63, no. 16, pp. 57275740.

12. Bassil, E., Zhang, S., Gong, H., et al., Cation specificity of vacuolar NHX-type cation/H+ antiporters, Plant Physiol., 2019, vol. 179, no. 2, pp. 616629.

13. Becker, D., Geiger, D., Dunkel, M., et al., AtTPK4, an Arabidopsis tandem-pore K+ channel, poised to control the pollen membrane voltage in a pH- and Ca2+-dependent manner, Proc. Natl. Acad. Sci. U. S. A., 2004, vol. 101, no. 44, pp. 1562115626.

14. Britto, D.T. and Kronzucker, H.J., Cellular mechanisms of potassium transport in plants, Physiol. Plant., 2008j, vol. 133, pp. 637650.

15. Busch, W., The transporter classification (TC) system, Crit. Rev. Biochem. Mol. Biol., 2002, vol. 37, no. 5, pp. 287237.

16. Campbell, M.T., Bandillo, N., Razzaq, F., et al., Allelic variants of OsHKT1;1 underlie the divergence between indica and japonica subspecies of rice (Oryza sativa) for root sodium content, PLoS Genet., 2017, vol. 13, no. 6, pp. 131.

17. Cao, Y., Liang, X., Yin, P., et al., A domestication-associated reduction in K+-preferring HKT transporter activity underlies maize shoot K+ accumulation and salt tolerance, New Phytol., 2018, vol. 222, no. 1, pp. 301317.

18. Cao, B., Xia, Z., Liu, C., et al., New insights into the structure-function relationship of the endosomal-type Na+,K+/H+ antiporter NHX6 from mulberry (Morus notabilis), Int. J. Mol. Sci., 2020, vol. 28, no. 2, pp. 119.

19. Carraretto, L., Formentin, E., Teardo, E., et al., A thylakoid-located two-pore K+ channel controls photosynthetic light utilization in plants, Science, 2013, vol. 342, no. 6154, pp. 114118.

20. Chanroj, S., Lu, Y., Padmanaban, S., et al., Plant-specific cation/H+ exchanger 17 and its homologs are endomembrane K+ transporters with roles in protein sorting, J. Biol. Chem., 2011, vol. 286, no. 39, pp. 3393133941.

21. Chanroj, S., Wang, G., Venema, K., et al., Conserved and diversified gene families of monovalent cation/ H+ antiporters from algae to flowering plants, Front Plant Sci., 2012, vol. 25, no. 3, pp. 118.

22. Cheng, X., Liu, X., Mao, W., et al., Genome-wide identification and analysis of HAK/KUP/KT potassium transporters gene family in wheat (Triticum aestivum L.), Mol. Sci., 2018, vol. 19, no. 3969, pp. 121.

23. Chen, G., Liu, C., Gao, Z., et al., OsHAK1, a high-affinity potassium transporter, positively regulates responses to drought stress in rice, Front. Plant Sci., 2017, vol. 8, no. 1885, pp. 117.

24. Chen, G., Liu, C., Gao, Z., et al., OsHAK1, a high-affinity potassium transporter, positively regulates responses to drought stress in rice, Front. Plant Sci., 2017, vol. 8, no. 2017, pp. 117.

25. Corratgu-Faillie, C., Ronzier, E., Sanchez, F., et al., The Arabidopsis guard cell outward potassium channel GORK is regulated by CPK33, FEBS Lett., 2017, vol. 591, pp. 19821992.

26. Cuin, T.A., Dreyer, I., and Machard, E., 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., 2018, vol. 19, pp. 117.

27. Dana, S., Herdean, A., Lundin, B., et al., Each of the chloroplast potassium efflux antiporters affects photosynthesis and growth of fully developed Arabidopsis rosettes under short-day photoperiod, Physiol. Plant., 2016, vol. 158, no. 4, pp. 483491.

28. Demidchik, V., Straltsova, D., Medvedev, S.S., et al., Stress-induced electrolyte leakage: the role of K+-permeable channels and involvement in programmed cell death and metabolic adjustment, J. Exp. Bot., 2014, vol. 65, pp. 12591270.

29. Demidchik, V., Shabala, S., Isayenkov, S.V., et al., Calcium transport across plant membranes: mechanisms and functions, New Phytol., 2018, vol. 220, no. 1, pp. 4969.

30. Dong, W., Li, D., Qiu, N., et al., The functions of plant cation/proton antiporters, Biol. Plant., 2018, vol. 62, no. 3, pp. 421427.

31. Dragwidge, J.M., Scholl, S., Schumacher, K., et al., NHX-type Na+(K+)/H+ antiporters are required for TGN/EE trafficking and endosomal ion homeostasis in Arabidopsis thaliana, J. Cell Sci., 2019, vol. 132, pp. 110.

32. Epstein, E., Rains, D.V., and Elzam, O.E., Resolution of dual mechanisms of potassium absorption by barley roots, Proc. Natl. Acad. Sci. U. S. A., 1961, vol. 49, pp. 684692.

33. Evans, A.R., Hall, D., Pritchard, J., et al., The roles of the cation transporters CHX21 and CHX23 in the development of Arabidopsis thaliana, J. Exp. Bot., 2011, vol. 63, no. 1, pp. 5967.

34. Forster, S., Schmidt, L.K., and Kopic, E., Wounding-induced stomatal closure requires jasmonate-mediated activation of GORK K+ channels by a Ca2+ sensor-kinase CBL1CIPK5 complex, Dev. Cell, 2019, vol. 48, pp. 113.

35. Gajdanowicz, P., Michard, E., Sandmann, M., et al., Potassium (K+) gradients serve as a mobile energy source in plant vascular tissues, Proc. Natl. Acad. Sci. U. S. A., 2011, vol. 108, no. 2, pp. 864869.

36. Gambale, F. and Uozumi, N., Properties of shaker-type potassium channels in higher plants, J. Membr. Biol., 2006, vol. 210, no. 1, pp. 119.

37. Gaymard, F., Pilot, G., Lacombe, B., et al., Identification and disruption of a plant shaker-like outward channel involved in K1 release into the xylem sap, Cell, 1998, vol. 94, pp. 647655.

38. Gierth, M. and Maser, P., Potassium transporters in plantsinvolvement in K+ acquisition, redistribution and homeostasis, FEBS Lett., 2007, vol. 581, pp. 23482356.

39. Gobert, A., Park, G., Amtmann, A., et al., Arabidopsis thaliana cyclic nucleotide gated channel 3 forms a non-selective ion transporter involved in germination and cation transport, J. Exp. Bot., 2006, vol. 57, no. 4, pp. 791800.

40. Gobert, A., Isayenkov, S., Voelker, C., et al., The two-pore channel TPK1 gene encodes the vacuolar K+ conductance and plays a role in K+ homeostasis, Proc. Natl. Acad. Sci. U. S. A., 2007, vol. 104, no. 25, pp. 1072610731.

41. Grabov, A., Plant KT/KUP/HAK potassium transporters: single familymultiple functions, Ann. Bot., 2007, vol. 99, pp. 10351041.

42. Hamamoto, S., Marui, J., Matsuoka, K., et al., Characterization of a tobacco TPK-type K+ channel as a novel tonoplast K+ channel using yeast tonoplasts, J. Biol. Chem., 2008, vol. 283, no. 4, pp. 19111920.

43. Hampton, C.R., Bowen, H.C., Broadley, M.R., et al., Cesium toxicity in Arabidopsis, Plant Physiol., 2004, vol. 136, no. 3, pp. 38243837.

44. Han, M., Wu, W., Wu, W.H., et al., Potassium Transporter KUP7 is involved in K+ acquisition and translocation in Arabidopsis root under K+-limited conditions, Mol. Plant., 2016, vol. 9, no. 3, pp. 437446.

45. Hauser, F. and Horie, T., A conserved primary salt tolerance mechanism mediated by HKT transporters: a mechanism for sodium exclusion and maintenance of high K+/Na+ ratio in leaves during salinity stress, Plant, Cell Environ., 2010, vol. 33, no. 4, pp. 552565.

46. Held, K., Pascaud, F., Eckert, C., et al., Calcium-dependent modulation and plasma membrane targeting of the AKT2 potassium channel by the CBL4/CIPK6 calcium sensor/protein kinase complex, Cell Res., 2011, vol. 21, pp. 11161130.

47. Huhner, R., Galvis, V.C., Strand, D.D., et al., Photosynthesis in Arabidopsis is unaffected by the function of the vacuolar K+ channel TPK3, Plant Physiol., 2019, vol. 180, no. 3, pp. 13221335.

48. Horie, T., Hauser, F., and Schroeder, J.I., HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants, Trend Plant Sci., 2009, vol. 14, no. 12, pp. 660668.

49. Horie, T., Brodsky, D.E., and Costa, A., 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 Physiol., 2011, vol. 156, no. 3, pp. 14931507.

50. Hosy, E., Vavasseur, A., and Mouline, K., The Arabidopsis outward K+ channel GORK is involved in regulation of stomatal movements and plant transpiration, Proc. Natl. Acad. Sci. U. S. A., 2003, vol. 100, no. 29, pp. 55495554.

51. Huang, S., Spielmeyer, W., Lagudah, E.S., et al., Comparative mapping of HKT genes in wheat, barley, and rice, key determinants of Na+ transport, and salt tolerance, J. Exp. Bot., 2008, vol. 59, no. 4, pp. 927937.

52. Huertas, R., Rubio, L., Cagnac, O., et al., The K+/H+ antiporter LeNHX2 increases salt tolerance by improving K+ homeostasis in transgenic tomato, Plant Cell Environ., 2013, vol. 36, pp. 21352149.

53. Isayenkov, S.V., Physiological and molecular aspects of salt stress in plants, Cytol. Genet., 2012, vol. 46, no. 5, pp. 302318.

54. Isaenkov, S. and Maathuis, F.J.M., Arabidopsis thaliana vacuolar TPK channels form functional K+ uptake pathways in Escherichia coli, Plant Signal. Behav., 2013, vol. 8, no. 7, pp. 15.

55. Isayenkov, S.V. and Maathuis, F.J.M., Plant salinity stress: many unanswered questions remain, Front Plant Sci., 2019, vol. 10, pp. 111.

56. Isayenkov, S.V., Isner, J.C., and Maathuis, F.J.M., Membrane localisation diversity of TPK channels and their physiological role, Plant Signal. Behav., 2011a, vol. 6, no. 3, pp. 12011204.

57. Isayenkov, S., Isner, J.C., and Maathuis, F.J.M., Rice two-pore K+ channels are expressed in different types of vacuoles, Plant Cell., 2011b, vol. 23, no. 2, pp. 756768.

58. Isayenkov, S.V., Dabravolski, S.A., Pan, T., et al., Phylogenetic diversity and physiological roles of plant monovalent cation/H+ antiporters, Front. Plant Sci., 2020, vol. 11, p. 573564.

59. Jeanguenin, L., Alcon, C., Duby, G., et al., AtKC1 is a general modulator of Arabidopsis inward Shaker channel activity, Plant J., 2011, vol. 67, pp. 570582.

60. Jegadeeson, V., Kumari, K., Pulipati, S., et al., PcNHX1 promoter (PcNHX1p) confers Na+-specific hypocotyl elongation and stem-specific Na+ accumulation in transgenic tobacco, Plant Physiol. Biochem., 2019, vol. 139, pp. 161170.

61. Jha, S.K., Sharma, M., and Pandey, G.K., Role of cyclic nucleotide gated channels in stress management in plants, Curr. Genom., 2016, vol. 17, no. 4, pp. 315329.

62. Jia, B., Sun, M., DuanMu, H., et al., GsCHX19.3, a member of cation/H+ exchanger superfamily from wild soybean contributes to high salinity and carbonate alkaline tolerance, Sci. Rep., 2017, vol. 7, no. 9423, pp. 112.

63. Jia, Q., Zheng, C., Sun, S., et al., The role of plant cation/proton antiporter gene family in salt tolerance, Biol. Plant., 2018, vol. 62, pp. 617629.

64. Johansson, I., Wulfetange, K., Porue, F., et al., External K+ modulates the activity of the Arabidopsis potassium channel SKOR via an unusual mechanism, Plant J., 2006, vol. 46, no. 2, pp. 269281.

65. Kleeff, P.J.M., Gao, J., Mol, S., et al., The Arabidopsis GORK K+-channel is phosphorylated by calcium-dependent protein kinase 21 (CPK21), which in turn is activated by 14 3-3 proteins, Plant Physiol. Biochem., 2018, vol. 125, pp. 219231.

66. Latz, A., Becker, D., Hekman, M., et al., TPK1, a Ca(2+)-regulated Arabidopsis vacuole two-pore K(+) channel is activated by 14-3-3 proteins, Plant J., 2007, vol. 52, pp. 449459.

67. Laurie, S., Feeney, K.A., Maathuis, F.J.M., et al., A role for HKT1 in sodium uptake by wheat roots, Plant J., 2002, vol. 32, no. 2, pp. 139149.

68. Lebaudy, A., Very, A.A., and Sentenac, H., K+ channel activity in plants: genes, regulations and functions, FEBS Lett., 2007, vol. 581, pp. 23572366.

69. Llopis-Torregrosa, V., Hušekova, B., and Sychrová, H., Potassium uptake mediated by Trk1 is crucial for Candida glabrata growth and fitness, PLoS One, 2016, vol. 11, no. 4, pp. 118.

70. Li, W., Xu, G., Alli, A., et al., Plant HAK/KUP/ KT K+ transporters: function and regulation, Semin. Cell Dev. Biol., 2018, vol. 74, pp. 133141.

71. Liu, K., Li, L., and Luan, S., Intracellular K+ sensing of SKOR, a Shaker-type K+ channel from Arabidopsis, Plant J., 2006, vol. 46, pp. 260268.

72. Maathuis, F.J.M., The role of monovalent cation transporters in plant responses to salinity, J. Exp. Bot., 2006, vol. 57, no. 5, pp. 11371147.

73. Maathuis, F.J.M., Vacuolar two-pore K+ channels act as vacuolar osmosensors, New Phytol., 2011, vol. 191, no. 1, pp. 8491.

74. Maathuis, F.J.M., Filatov, V., Herzyk, P., et al., Transcriptome analysis of root transporters reveals participation of multiple gene families in the response to cation stress, Plant J., 2003, vol. 35, pp. 675692.

75. MacKinnon, R., Potassium channels, FEBS Lett., 2003, vol. 555, pp. 6265.

76. Marcel, D., Muller, T., Hedrich, R., et al., K+ transport characteristics of the plasma membrane tandem-pore channel TPK4 and pore chimeras with its vacuolar homologs, FEBS Lett., 2010, vol. 584, pp. 24332249.

77. Mian, A., Oomen, R.J.F.J., Isayenkov, S., et al., Overexpression of an Na+- and K+-permeable HKT transporter in barley improves salt tolerance, Plant J., 2011, vol. 68, no. 3, pp. 468479.

78. Mishra, S., Singh, B., Panda, K., et al., Association of SNP haplotypes of HKT family genes with salt tolerance in Indian wild rice germplasm, Rice (NY), 2016, vol. 9, no. 1, pp. 115.

79. Mushke, R., Yarra, R., and Kirti, P.B., Improved salinity tolerance and growth performance in transgenic sunflower plants via ectopic expression of a wheat anti-porter gene (TaNHX2), Mol. Biol. Rep., 2019, vol. 46, pp. 59415953.

80. Mottaleb, S.A., Rodriguez-Navarro, A., and Haro, R., Knockouts of Physcomitrella patens CHX1 and CHX2 transporters reveal high complexity of potassium homeostasis, Plant Cell Physiol., 2013, vol. 54, no. 9, pp. 14551468.

81. Nawaz, I., Iqbal, M., and Hakvoort, H.W.J., Analysis of Arabidopsis thaliana HKT1 and Eutrema salsugineum/botschantzevii HKT1;2 promoters in response to salt stress in Athkt 1:1 Mutant, Mol. Biotechnol., 2019, vol. 61, no. 6, pp. 442450.

82. Nieves-Cordones, M., Alemán, F., Martínez, V., et al., The Arabidopsis thaliana HAK5 K+ transporter is required for plant growth and K+ acquisition from low K+ solutions under saline conditions, Mol. Plant., 2010, vol. 3, no. 2, pp. 326333.

83. Nieves-Cordones, M., Al Shiblawi, F.R., and Sentenac, H., Roles and transport of sodium and potassium in plants, Met. Ions Life Sci., 2016, vol. 16, pp. 291324.

84. Osakabe, Y., Arinaga, N., Umezawa, T., et al., Osmotic stress responses and plant growth controlled by potassium transporters in Arabidopsis, Plant Cell, 2013, vol. 25, pp. 609624.

85. Ou, W., Mao, X., Huang, C., et al., Genome-wide identification and expression analysis of the KUP family under abiotic stress in cassava (Manihot esculenta Crantz), Front. Physiol., 2018, vol. 9, no. 17, pp. 111.

86. Papazian, D.M., Schwarz, T.L., Tempel, B.L., et al., Cloning of the genomic and complementary DNA from Shaker, a putative potassium channel gene from Drosophila, Science, 1987, vol. 237, pp. 749753.

87. Ren, Z.H., Gao, J.P., Li, L.G., et al., A rice quantitative trait locus for salt tolerance encodes a sodium transporter, Nat. Genet., 2005, vol. 37, no. 10, pp. 11411146.

88. Rodríguez-Navarro, A. and Rubio, F., High-affinity potassium and sodium transport systems in plants, J. Exp. Bot., 2006, vol. 57, no. 5, pp. 11491160.

89. Rodríguez-Rosales, M.P., Gálvez, F.J., Huertas, R., et al., Plant NHX cation/proton antiporters, Plant Signal. Behav., 2009, vol. 4, no. 4, pp. 265276. 7919

90. Ruiz-Lau, N., Bojyrquez-Quintal, E., Benito, B., et al., Molecular cloning and functional analysis of a Na+-insensitive K+ transporter of Capsicum chinense Jacq., Front. Plant Sci., 1980, vol. 7, no. 1980, pp. 114.

91. Saier, M.H., Jr., A functional-phylogenetic classification system for transmembrane solute transporters, Microbiol. Mol. Biol. Rev., 2000, vol. 64, no. 2, pp. 354411.

92. Schachtman, D.P. and Schroeder, J.I., Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plants, Nature, 1994, vol. 370, no. 6491, pp. 655658.

93. Sentenac, H., Bonneaud, N., Minet, M., et al., Cloning and expression in yeast of a plant potassium ion transport system, Science, 1992, vol. 256, pp. 663665.

94. Sharma, H., Taneja, M., and Upadhyay, S.K., Identification, characterization and expression profiling of cation-proton antiporter superfamily in Triticum aestivum L. and functional analysis of TaNHX4-B, Genomics, 2020, vol. 112, no. 1, pp. 356370.

95. Sharma, T., Dreyer, I., and Riedelsberger, J., The role of K+ channels in uptake and redistribution of potassium in the model plant Arabidopsis thaliana, Front. Plant Sci., 2013, vol. 4, pp. 116.

96. Su, Y., Luo, W., Lin, W., et al., Model of cation transportation mediated by high-affinity potassium transporters (HKTs) in higher plants, Biol. Proc. Online, 2015, vol. 17, no. 1, pp. 113.

97. Sze, H., Padmanaban, S., Cellier, F., et al., Expression patterns of a novel AtCHX gene family highlight potential roles in osmotic adjustment and K+ homeostasis in pollen development, Plant Physiol., 2004, vol. 131, no. 1, pp. 25322547.

98. Tang, R.J., Zhao, F.G., Yang, Y., et al., Calcium signalling network activates vacuolar K+ remobilization to enable plant adaptation to low-K environments, Nat. Plants, 2020, vol. 6, no. 4, pp. 384393.

99. Tester, M. and Devenport, R., Na+ tolerance and Na+ transport in higher plants, Ann. Bot., 2003, vol. 91, no. 5, pp. 503527.

100. Tsujii, M., Kera, K., Hamamoto, S., et al., Evidence for potassium transport activity of Arabidopsis KEA1KEA6, Sci. Rep., 2019, vol. 9, no. 1, pp. 113.

101. Very, A.A. and Sentenac, H., Molecular mechanisms and regulation of K+ transport in higher plants, Ann. Rev. Plant Biol., 2003, vol. 54, pp. 575603.

102. Voelker, C., Schmidt, D., Mueller-Roeber, B., et al., Members of the Arabidopsis AtTPK/KCO family form homomeric vacuolar channels in planta, Plant J., 2006, vol. 48, no. 2, pp. 296306.

103. Wang, C., Yamamoto, H., Narumiya, F., et al., Fine-tuned regulation of the K+/H+ antiporter KEA3 is required to optimize photosynthesis during induction, Plant J., 2017, vol. 89, no. 3, pp. 540553.

104. Wang, Y., Lü, J., and Chen, D., Genome-wide identification, evolution, and expression analysis of the KT/HAK/KUP family in pear, Genome, 2018, vol. 61, no. 10, pp. 146.

105. Ward, J.M., Maser, P., and Schroeder, J.I., Plant ion channels: gene families, physiology, and functional genomics analyses, Ann. Rev. Physiol., 2009, vol. 71, pp. 5982.

106. Wu, H., Zhang, X., Giraldo, J.P., et al., It is not all about sodium: revealing tissue specificity and signalling roles of potassium in plant responses to salt stress, Plant Soil, 2018, vol. 431, pp. 117.

107. Yamaguchi, T., Hamamoto, N., and Uozumi, N., Sodium transport system in plant cells, Front Plant Sci., 2013, vol. 4, no. 410, pp. 17.

108. Yang, T., Zhang, S., Hu, Y., et al., 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., 2014, vol. 166, pp. 945959.

109. Yokoi, S., Quintero, F.J., Cubero, B., et al., Differential expression and function of Arabidopsis thaliana NHX Na+/H+ antiporters in the salt stress response, Plant J., 2002, vol. 30, no. 5, pp. 529539.

110. Yuen, C.Y.L. and Christopher, D.A., The role of cyclic nucleotide-gated channels in cation nutrition and abiotic stress, in Ion Channels and Plant Stress Responses, Demidchik, V. and Maathuis, F., Eds., Berlin: Springer, 2010, pp. 137157.

111. Zhang, M., Liang, X., Wang, L., et al., HAK family Na+ transporter confers natural variation of salt tolerance in maize, Nat. Plants, 2020, vol. 5, pp. 12971308.

112. Zhang, Y., Fang, J., Wu, X., et al., Na+/K+ balance and transport regulatory mechanisms in weedy and cultivated rice (Oryza sativa L.) under salt stress, BMC Plant Biol., 2018, vol. 18, no. 375, pp. 114.

113. Zhang, S., Tong, Y., and Li, Y., Genome-wide identification of the HKT genes in five Rosaceae species and expression analysis of HKT genes in response to salt-stress in Fragaria vesca, Genes Genom., 2019, vol. 41, pp. 325336.

114. Zhao, J., Li, P., Motes, C.M., et al., CHX14 is a plasma membrane K-efflux transporter that regulates K+ redistribution in Arabidopsis thaliana, Plant Cell Environ., 2015, vol. 38, pp. 22232238.

115. Zheng, S., Pan, T., Fan, L., et al., A novel AtKEA gene family, homolog of bacterial K+/H+ antiporters, plays potential roles in K+ homeostasis and osmotic adjustment in Arabidopsis, PLoS One, 2013, vol. 8, no. 11, pp. 119.

116. Zhou, Y., Yin, X., Duan, R., et al., SpAHA1 and SpSOS1 coordinate in transgenic yeast to improve salt tolerance, PLoS One, 2015, vol. 10, no. 9, pp. 114.

117. Zhu, X., Pan, T., Zhang, X., et al., K+ efflux antiporters 4, 5, and 6 mediate pH and K+ homeostasis in endomembrane compartments, Plant Physiol., 2018, vol. 178, no. 4, pp. 16571678.

Copyright© ICBGE 2002-2021 Coded & Designed by Volodymyr Duplij Modified 21.09.21