Цитологія і генетика 2021, том 55, № 1, 75-92
Cytology and Genetics 2021, том 55, № 1, 63–79, doi: https://www.doi.org/10.3103/S0095452721010126

Системи транспорту калію та їх роль в формуванні стресової відповіді, росту та розвитку рослин

Нестеренко Є.О., Краснопьорова О.Є., Ісаєнков С.В.

  1. ДУ «Інститут харчової біотехнології та геноміки НАН України», вул. Осиповського, 2а, Київ, 04123, Україна
  2. Інститут молекулярної біології і генетики НАН України, вул. Академіка Заболотного, Київ, 04123, Україна

У цій оглядовій статті були відібрані та охарактеризовані головні системи мембранного транспорту калію. Було проведено детальний аналіз літературних джерел та узагальнення даних щодо основних представників транспортних систем K+ в рослині, їх біологічної ролі та фізіологічних функції у процесах росту та розвитку рослинного організму та механізмах стійкості до абіотичних стресів. Описано процеси поглинання, транспорту та перерозподілу калію між тканинами та на рівні клітини. Проаналізовано топологію та особливості структури транспортних білків залучених у транспорт калію та їх ролі у виконанні специфічних біологічних функцій. Критично оцінена роль цих мембранних транспортних білків в сигнальних процесах. механізмах посухо- та солестійкості рослин чи дефіциту калію. Запропоновані подальші перспективні напрямки та області досліджень цих важливих транспортних систем.

Ключові слова: транспорт калію, двопорові канали TPK, Shaker подібні канали, Kir-подібні канали, неселективні катіонні канали NCCC, KUP/HAK/KT транс-портери, Trk/HKT транспортери, CPA транспортери

Цитологія і генетика
2021, том 55, № 1, 75-92

Current Issue
Cytology and Genetics
2021, том 55, № 1, 63–79,
doi: 10.3103/S0095452721010126

Повний текст та додаткові матеріали

Цитована література

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. 708–714. https://doi.org/10.1016/j.jplph.2013.10.016

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. 1040–1048. https://doi.org/10.1111/nph.13708

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. 125–138. https://doi.org/10.1093/jxb/erj012

4. Almeida, P., Katschnig, D., and de Boer, A.H., HKT transporters—state of the art, Int. J. Mol. Sci., 2013, vol. 14, no. 10, pp. 20359–20385. https://doi.org/10.3390/ijms141020359

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. 682–691. https://doi.org/10.1111/j.1399-3054.2008.01075

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. 1256–1288. https://doi.org/10.1126/science.285.5431.1256

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. 441–449. https://doi.org/10.1104/pp.16.00995

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. 1–13. https://doi.org/10.1155/2019/1031839

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. 102–128. https://doi.org/10.1007/s10528-019-09930-4

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. 1127–1142. https://doi.org/10.1105/tpc.111.095273

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. 5727–5740. https://doi.org/10.1093/jxb/ers250

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. 616–629. https://doi.org/10.1104/pp.18.01103

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. 15621–15626. https://doi.org/10.1073/pnas.0401502101

14. Britto, D.T. and Kronzucker, H.J., Cellular mechanisms of potassium transport in plants, Physiol. Plant., 2008j, vol. 133, pp. 637–650. https://doi.org/10.1111/j.1399-3054.2008.01067.x

15. Busch, W., The transporter classification (TC) system, Crit. Rev. Biochem. Mol. Biol., 2002, vol. 37, no. 5, pp. 287–237. https://doi.org/10.1080/10409230290771528

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. 1–31. https://doi.org/10.1371/journal.pgen.1006823

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. 301–317. https://doi.org/10.1111/nph.15605

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. 1–19. https://doi.org/10.3390/ijms21020428

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. 114–118. https://doi.org/10.1126/science.1242113

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. 33931–33941. https://doi.org/10.1074/jbc.M111.252650

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. 1–18. https://doi.org/10.3389/fpls.2012.00025

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. 1–21. https://doi.org/10.3390/ijms19123969

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. 1–17. https://doi.org/10.3389/fpls.2017.01885

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. 1–17. https://doi.org/10.3389/fpls.2017.01885

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. 1982–1992. https://doi.org/10.1002/1873-3468.12687

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. 1–17. https://doi.org/10.3390/ijms19040926

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. 483–491. https://doi.org/10.1111/ppl.12452

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. 1259–1270. https://doi.org/10.1093/jxb/eru004

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. 49–69. https://doi.org/10.1111/nph.15266

30. Dong, W., Li, D., Qiu, N., et al., The functions of plant cation/proton antiporters, Biol. Plant., 2018, vol. 62, no. 3, pp. 421–427. https://doi.org/10.1007/s10535-018-0790-7

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. 1–10. https://doi.org/10.1242/jcs.226472

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. 684–692. https://doi.org/10.1073/pnas.49.5.684

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. 59–67. https://doi.org/10.1093/jxb/err271

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 CBL1–CIPK5 complex, Dev. Cell, 2019, vol. 48, pp. 1–13. https://doi.org/10.1016/j.devcel.2018.11.014

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. 864–869. https://doi.org/10.1073/pnas.1009777108

36. Gambale, F. and Uozumi, N., Properties of shaker-type potassium channels in higher plants, J. Membr. Biol., 2006, vol. 210, no. 1, pp. 1–19. https://doi.org/10.1007/s00232-006-0856-x

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. 647–655. https://doi.org/10.1016/s0092-8674(00)81606-2

38. Gierth, M. and Maser, P., Potassium transporters in plants—involvement in K+ acquisition, redistribution and homeostasis, FEBS Lett., 2007, vol. 581, pp. 2348–2356. https://doi.org/10.1016/j.febslet.2007.03.035

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. 791–800. https://doi.org/10.1093/jxb/erj064

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. 10726–10731. https://doi.org/10.1073/pnas.0702595104

41. Grabov, A., Plant KT/KUP/HAK potassium transporters: single family—multiple functions, Ann. Bot., 2007, vol. 99, pp. 1035–1041. https://doi.org/10.1093/aob/mcm066

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. 1911–1920.https://doi.org/10.1074/jbc.M708213200

43. Hampton, C.R., Bowen, H.C., Broadley, M.R., et al., Cesium toxicity in Arabidopsis, Plant Physiol., 2004, vol. 136, no. 3, pp. 3824–3837. https://doi.org/10.1104/pp.104.046672

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. 437–446. https://doi.org/10.1016/j.molp.2016.01.012

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. 552–565. https://doi.org/10.1111/j.1365-3040.2009.02056.x

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. 1116–1130. https://doi.org/10.1038/cr.2011.50

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. 1322–1335. https://doi.org/10.1104/pp.19.00255

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. 660–668. https://doi.org/10.1016/j.tplants.2009.08.009

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. 1493–1507. https://doi.org/10.1104/pp.110.168047

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. 5549–5554. https://doi.org/10.1073/pnas.0733970100

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. 927–937. https://doi.org/10.1093/jxb/ern033

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. 2135–2149. https://doi.org/10.1111/pce.12109

53. Isayenkov, S.V., Physiological and molecular aspects of salt stress in plants, Cytol. Genet., 2012, vol. 46, no. 5, pp. 302–318. https://doi.org/10.3103/S0095452712050040

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. 1–5. https://doi.org/10.4161/psb.24665

55. Isayenkov, S.V. and Maathuis, F.J.M., Plant salinity stress: many unanswered questions remain, Front Plant Sci., 2019, vol. 10, pp. 1–11. https://doi.org/10.3389/fpls.2019.00080

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. 1201–1204. https://doi.org/10.4161/psb.6.8.15808

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. 756–768. https://doi.org/10.1105/tpc.110.081463

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. https://doi.org/10.3389/fpls.2020.573564

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. 570–582. https://doi.org/10.1111/j.1365-313X.2011.04617.x

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. 161–170. https://doi.org/10.1016/j.plaphy.2019.03.014

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. 315–329. https://doi.org/10.2174/1389202917666160331202125

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. 1–12. https://doi.org/10.1038/s41598-017-09772-3

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. 617–629. https://doi.org/10.1007/s10535-018-0801-8

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. 269–281. https://doi.org/10.1111/j.1365-313X.2006.02690.x

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. 219–231. https://doi.org/10.1016/j.pla-phy.2018.02.013

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. 449–459. https://doi.org/10.1111/j.1365-313X.2007.03255.x

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. 139–149. https://doi.org/10.1046/j.1365-313x.2002.01410.x

68. Lebaudy, A., Very, A.A., and Sentenac, H., K+ channel activity in plants: genes, regulations and functions, FEBS Lett., 2007, vol. 581, pp. 2357–2366. https://doi.org/10.1016/j.febs-let.2007.03.058

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. 1–18. https://doi.org/10.1371/journal.pone.0153374

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. 133–141. https://doi.org/10.1016/j.semcdb.2017.07.009

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. 260–268. https://doi.org/10.1111/j.1365-313X.2006.02689.x

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. 1137–1147. https://doi.org/10.1093/jxb/erj001

73. Maathuis, F.J.M., Vacuolar two-pore K+ channels act as vacuolar osmosensors, New Phytol., 2011, vol. 191, no. 1, pp. 84–91. https://doi.org/10.1111/j.1469-8137.2011.03664.x

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. 675–692. https://doi.org/10.1046/j.1365-313x.2003.01839.x

75. MacKinnon, R., Potassium channels, FEBS Lett., 2003, vol. 555, pp. 62–65. https://doi.org/10.1016/s0014-5793(03)01104-9

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. 2433–2249. https://doi.org/10.1016/j.febslet.2010.04.038

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. 468–479. https://doi.org/10.1111/j.1365-313X.2011.04701.x

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. 1–15. https://doi.org/10.1186/s12284-016-0083-8

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. 5941–5953. https://doi.org/10.1007/s11033-019-05028-7

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. 1455–1468.https://doi.org/10.1093/pcp/pct096

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. 442–450. https://doi.org/10.1007/s12033-019-00175-5

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. 326–333. https://doi.org/10.1093/mp/ssp102

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. 291–324. https://doi.org/10.1007/978-3-319-21756-7_9

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. 609–624. https://doi.org/10.1105/tpc.112.105700

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. 1–11. https://doi.org/10.3389/fphys.2018.00017

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. 749–753. https://doi.org/10.1126/science.2441470

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. 1141–1146. https://doi.org/10.1038/ng1643

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. 1149–1160. https://doi.org/10.1093/jxb/erj068

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. 265–276. https://doi.org/10.4161/psb.4.4. 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. 1–14. https://doi.org/10.3389/fpls.2016.01980

91. Saier, M.H., Jr., A functional-phylogenetic classification system for transmembrane solute transporters, Microbiol. Mol. Biol. Rev., 2000, vol. 64, no. 2, pp. 354–411. https://doi.org/10.1128/mmbr.64.2.354-411.2000

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. 655–658. https://doi.org/10.1038/370655a0

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. 663–665. https://doi.org/10.1126/science.1585180

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. 356–370. https://doi.org/10.1016/j.yge-no.2019.02.015

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. 1–16. https://doi.org/10.3389/fpls.2013.00224

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. 1–13. https://doi.org/10.1186/s12575-014-0013-3

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. 2532–2547. https://doi.org/10.1104/pp.104.046003

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. 384–393. https://doi.org/10.1038/s41477-020-0621-7

99. Tester, M. and Devenport, R., Na+ tolerance and Na+ transport in higher plants, Ann. Bot., 2003, vol. 91, no. 5, pp. 503–527. https://doi.org/10.1093/aob/mcg058

100. Tsujii, M., Kera, K., Hamamoto, S., et al., Evidence for potassium transport activity of Arabidopsis KEA1–KEA6, Sci. Rep., 2019, vol. 9, no. 1, pp. 1–13. https://doi.org/10.1038/s41598-019-46463-7

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. 575–603. https://doi.org/10.1146/annurev.arplant.54.031902.134831

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. 296–306. https://doi.org/10.1111/j.1365-313X.2006.02868.x

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. 540–553. https://doi.org/10.1111/tpj.13405

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. 1–46. https://doi.org/10.1139/gen-2017-0254

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. 59–82. https://doi.org/10.1146/annurev.physiol.010908.163204

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. 1–17. https://doi.org/10.1007/s11104-018-3770-y

107. Yamaguchi, T., Hamamoto, N., and Uozumi, N., Sodium transport system in plant cells, Front Plant Sci., 2013, vol. 4, no. 410, pp. 1–7. https://doi.org/10.3389/fpls.2013.00410

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. 945–959. https://doi.org/10.1104/pp.114.246520

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. 529–539. https://doi.org/10.1046/j.1365-313x.2002.01309.x

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. 137–157. https://doi.org/10.1007/978-3-642-10494-7_7

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. 1297–1308. https://doi.org/10.1038/s41477-019-0565-y

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. 1–14. https://doi.org/10.1186/s12870-018-1586-9

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. 325–336. https://doi.org/10.1007/s13258-018-0767-0

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. 2223–2238. https://doi.org/10.1111/pce.1252

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. 1–19. https://doi.org/10.1371/journal.pone.0081463

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. 1–14. https://doi.org/10.1371/journal.pone.0137447

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. 1657–1678. https://doi.org/10.1104/pp.18.01053