Advertisement

Mechanisms of Ion Transport in Halophytes: From Roots to Leaves

  • Vadim Volkov
  • Timothy J. Flowers
Chapter
Part of the Tasks for Vegetation Science book series (TAVS, volume 49)

Abstract

The chapter describes peculiarities of ion transport in halophytic plants, aiming to help understand the mechanisms important for their tolerance of salt. An initial introduction to methods for studying ion transport is followed by analysis of ion transport from a broad thermodynamic point of view. Further detailed survey of ion channels and ion transporters in plants adds to the picture of ion transport pathways through cell membranes. A typical ‘generalised’ plant cell is depicted to illustrate the variety of ion transport systems known so far for all plants. This serves as a basis for a comparison of ion transport in salt-sensitive glycophytes and salt-tolerant halophytes. Next, there is a description of what we know of transport systems in halophytes, beginning from the thermodynamics of ion transport under salinity. In halophytes, low negative stable plasma membrane potentials and cytoplasmic Na+ concentrations that are often higher than in glycophytes are important for their life under salinity. Comparison of similar pairs of plants with contrasting halophytic and glycophytic habits allows us to find specific features of ion transport essential for high salinity tolerance. Mechanisms of high- and low-affinity sodium transport in halophytes are briefly characterised to explain and stress the increased accumulation of Na+ by halophytes compared to glycophytes. Description of ion channels and transporters in halophytes and pathways of ion transport from nutrient solution to their roots, then to the xylem and finally to leaves completes the chapter. Problems and unsolved questions are proposed for the future study of ion transport in halophytes.

Keywords

Glycophyte Halophyte Ion transport Salt tolerance 

References

  1. Akhundova TS, Mardanov AA, Ali Zade VM (1990) Effect of kinetin on the membrane potential of root epidermal cells of Trianea bogotensis in a nutrient medium with an excessive amount of chloride. Izvestiya Akademii Nauk Azerbaidzhana Seriya Biologicheskikh Nauk 0(1):12–17Google Scholar
  2. Alemán F, Nieves-Cordones M, Martínez V, Rubio F (2009) Potassium/sodium steady-state homeostasis in Thellungiella halophila and Arabidopsis thaliana under long-term salinity conditions. Plant Sci 176:768–774CrossRefGoogle Scholar
  3. Alemán F, Caballero F, Ródenas R, Rivero RM, Martínez V, Rubio F (2014) The F130S point mutation in the Arabidopsis high-affinity K+ transporter AtHAK5 increases K+ over Na+ and Cs+ selectivity and confers Na+ and Cs+ tolerance to yeast under heterologous expression. Front Plant Sci 5:430PubMedPubMedCentralCrossRefGoogle Scholar
  4. Ali A, Park HC, Aman R, Ali Z, Yun D-J (2013) Role of HKT1 in Thellungiella salsuginea, a model extremophile plant. Plant Signal Behav 8:e25196PubMedPubMedCentralCrossRefGoogle Scholar
  5. Amtmann A (2009) Learning from evolution: Thellungiella generates new knowledge on essential and critical components of abiotic stress tolerance in plants. Mol Plant 2:3–12PubMedPubMedCentralCrossRefGoogle Scholar
  6. Anderson WP, Willcocks DA, Wright BJ (1977) Electrophysiological measurements on root of Atriplex hastata. J Exp Bot 28:894–901CrossRefGoogle Scholar
  7. Armengaud P, Sulpice R, Miller AJ, Stitt M, Amtmann A, Gibon Y (2009) Multilevel analysis of primary metabolism provides new insights into the role of potassium nutrition for glycolysis and nitrogen assimilation in Arabidopsis roots. Plant Physiol 150:772–785PubMedPubMedCentralCrossRefGoogle Scholar
  8. Ashcroft F, Gadsby D, Miller C (2009) Introduction. The blurred boundary between channels and transporters: we dedicate this volume to the memory of Peter Läuger, a pioneer of the link between channels and pumps. Phil Trans R S B: Biol Sci 364:145–147CrossRefGoogle Scholar
  9. Axelsson L, Mercado J, Figueroa F (2000) Utilization of HCO3 at high pH by the brown macroalga Laminaria saccharina. Eur J Phycol 35:53–59CrossRefGoogle Scholar
  10. Balnokin YV, Kurkova EB, Khalilova LA, Myasoedov NA, Yusufov AG (2007) Pinocytosis in the root cells of a salt-accumulating halophyte and its possible involvement in chloride transport. Russ J Plant Physiol 54:797–805CrossRefGoogle Scholar
  11. Bañuelos MA, Klein RD, Alexander-Bowman SJ, Rodriguez-Navarro A (1995) A potassium transporter of the yeast Schwanniomyces occidentalis homologous to the Kup system of Escherichia coli has a high concentrative capacity. EMBO J 14:3021–3027PubMedPubMedCentralCrossRefGoogle Scholar
  12. Barkla BJ, Vera-Estrella R, Pantoja O (2012) Protein profiling of epidermal bladder cells from the halophyte Mesembryanthemum crystallinum. Proteomics 12:2862–2865PubMedCrossRefPubMedCentralGoogle Scholar
  13. Bazzanella A, Lochmann H, Tomos AD, Bächmann K (1998) Determination of inorganic cations and anions in single plant cells by capillary zone electrophoresis. J Chromatogr 809:231–239CrossRefGoogle Scholar
  14. Benito B, Rodríguez-Navarro A (2003) Molecular cloning and characterization of a sodium-pump ATPase of the moss Physcomitrella patens. Plant J 36:382–389PubMedCrossRefPubMedCentralGoogle Scholar
  15. Benito B, Haro R, Amtmann A, Cuin TA, Dreyer I (2014) The twins K+ and Na+ in plants. J Plant Physiol 171:723–731PubMedCrossRefPubMedCentralGoogle Scholar
  16. Bennett TH, Flowers TJ, Bromham L (2013) Repeated evolution of salt-tolerance in grasses. Biol Lett 9:20130029.  https://doi.org/10.1098/rsbl.2013.0029 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Blatt MR (1987) Electrical characteristics of stomatal guard cells: the ionic basis of the membrane potential and the consequence of potassium chlorides leakage from microelectrodes. Planta 170:272–287PubMedCrossRefPubMedCentralGoogle Scholar
  18. Blatt MR (1991) A primer in plant electrophysiological methods. In: Hostettmann K (ed) Methods in plant biochemistry. Academic, London, pp 281–321Google Scholar
  19. Boscari A, Clément M, Volkov V, Golldack D, Hybiak J, Miller AJ, Amtmann A, Fricke W (2009) Potassium channels in barley: cloning, functional characterization and expression analyses in relation to leaf growth and development. Plant Cell Environ 32:1761–1777PubMedCrossRefPubMedCentralGoogle Scholar
  20. Bose J, Rodrigo-Moreno A, Lai D, Xie Y, Shen W, Shabala S (2015) Rapid regulation of the plasma membrane H+-ATPase activity is essential to salinity tolerance in two halophyte species, Atriplex lentiformis and Chenopodium quinoa. Ann Bot 115:481–494PubMedCrossRefPubMedCentralGoogle Scholar
  21. Briggs GE, Hope AB (1958) Electric potential differences and the Donnan equilibrium in plant tissues. J Exp Bot 9:365–371CrossRefGoogle Scholar
  22. Briggs GE, Robertson RN (1957) Apparent free space. Ann Rev Plant Physiol 8:11–30CrossRefGoogle Scholar
  23. Britto DT, Kronzucker HJ (2008) Cellular mechanisms of potassium transport in plants. Physiol Plant 133:637–650CrossRefGoogle Scholar
  24. Cakirlar H, Bowling DJF (1981) The effect of salinity on the membrane potential of sunflower roots. J Exp Bot 32:479–485CrossRefGoogle Scholar
  25. Campion DS (1974) Resting membrane potential and ionic distribution in fast- and slow-twitch mammalian muscle. J Clin Invest 54:514–518PubMedPubMedCentralCrossRefGoogle Scholar
  26. Cao Y, Jin X, Huang H, Derebe MG, Levin EJ, Kabaleeswaran V et al (2011) Crystal structure of a potassium ion transporter, TrkH. Nature 471:336–340PubMedPubMedCentralCrossRefGoogle Scholar
  27. Carden DE, Diamond D, Miller AJ (2001) An improved Na+-selective microelectrode for intracellular measurements in plant cells. J Exp Bot 52:1353–1359PubMedPubMedCentralGoogle Scholar
  28. Carden DE, Walker DJ, Flowers TJ, Miller AJ (2003) Single-cell measurements of the contributions of cytosolic Na+ and K+ to salt tolerance. Plant Physiol 131:676–683PubMedPubMedCentralCrossRefGoogle Scholar
  29. Carpaneto A, Koepsell H, Bamberg E, Hedrich R, Geiger D (2010) Sucrose- and H+-dependent charge movements associated with the gating of sucrose transporter ZmSUT1. PLoS One 5:e12605PubMedPubMedCentralCrossRefGoogle Scholar
  30. Carr H, Axelsson L (2008) Photosynthetic utilization of bicarbonate in Zostera marina is reduced by inhibitors of mitochondrial ATPase and electron transport. Plant Physiol 147:879–885PubMedPubMedCentralCrossRefGoogle Scholar
  31. Chakrapani S, Auerbach A (2005) A speed limit for conformational change of an allosteric membrane protein. Proc Natl Acad Sci U S A 102:87–92PubMedCrossRefPubMedCentralGoogle Scholar
  32. Chen ZH, Pottosin II, Cuin TA, Fuglsang AT, Tester M, Jha D, Zepeda-Jazo I, Zhou MX, Palmgren MG, Newman IA, Shabala S (2007) Root plasma membrane transporters controlling K+/Na+ homeostasis in salt-stressed barley. Plant Physiol 145:1714–1725PubMedPubMedCentralCrossRefGoogle Scholar
  33. Clipson NJW, Flowers TJ (1987) Salt tolerance in the halophyte Suaeda maritima (L) Dum – the effect of salinity on the concentration of sodium in the xylem. New Phytol 105:359–366CrossRefGoogle Scholar
  34. Collins KD (1997) Charge density-dependent strength of hydration and biological structure. Biophys J 72:65–76PubMedPubMedCentralCrossRefGoogle Scholar
  35. Cuin TA, Miller AJ, Laurie SA, Leigh RA (2003) Potassium activities in cell compartments of salt-grown barley leaves. J Exp Bot 54:657–661PubMedCrossRefPubMedCentralGoogle Scholar
  36. Dassanayake M, Larkin J (2017) Making plants break a sweat: the structure, function, and evolution of plant salt glands. Front Plant Sci 8:406.  https://doi.org/10.3389/fpls.2017.00406 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Dassanayake M, Oh DH, Haas JS, Hernandez A, Hong H, Ali S, Yun DJ, Bressan RA, Zhu JK, Bohnert HJ, Cheeseman JM (2011) The genome of the extremophile crucifer Thellungiella parvula. Nat Genet 43:913–918PubMedPubMedCentralCrossRefGoogle Scholar
  38. Davenport R (2002) Glutamate receptors in plants. Ann Bot 90:549–557PubMedPubMedCentralCrossRefGoogle Scholar
  39. de Almeida PMF (2014) The role of HKT transporters in salinity tolerance of tomato. Ph.D. thesis, Vrije Universiteit, Amsterdam, p 219Google Scholar
  40. De Boer AH (1985) Xylem/symplast ion exchange: mechanism and function in salt tolerance and growth. Ph.D. thesis, Rijksuniversiteit Groningen, GroningenGoogle Scholar
  41. De Boer AH, Volkov V (2003) Logistics of water and salt transport through the plant: structure and functioning of the xylem. Plant Cell Environ 26:87–101CrossRefGoogle Scholar
  42. Demidchik V, Maathuis FJ (2007) Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytol 175:387–404PubMedCrossRefPubMedCentralGoogle Scholar
  43. Demidchik V, Tester M (2002) Sodium fluxes through nonselective cation channels in the plasma membrane of protoplasts from Arabidopsis roots. Plant Physiol 128:379–387PubMedPubMedCentralCrossRefGoogle Scholar
  44. Demidchik V, Cuin TA, Svistunenko D, Smith SJ, Miller AJ, Shabala S et al (2010) Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. J Cell Sci 123:1468–1479PubMedCrossRefPubMedCentralGoogle Scholar
  45. Doyle DA, Cabral MJ, Pfuetzner RA, Kuo A, Gulbis JM, Cohen SL et al (1998) The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280:69–77PubMedCrossRefPubMedCentralGoogle Scholar
  46. English JP, Colmer TD (2013) Tolerance of extreme salinity in two stem-succulent halophytes (Tecticornia species). Funct Plant Biol 40:897–912CrossRefGoogle Scholar
  47. Erdei L, Kuiper PJC (1979) The effect of salinity on growth. Cation content, Na+-uptake and translocation in salt-sensitive and salt-tolerant Plantago species. Physiol Plant 47:95–99CrossRefGoogle Scholar
  48. Essah PA, Davenport R, Tester M (2003) Sodium influx and accumulation in Arabidopsis. Plant Physiol 133:307–318PubMedPubMedCentralCrossRefGoogle Scholar
  49. Evans A, Hall D, Pritchard J, Newbury HJ (2012) The roles of the cation transporters CHX21 and CHX23 in the development of Arabidopsis thaliana. J Exp Bot 63:59–67PubMedCrossRefPubMedCentralGoogle Scholar
  50. Fernández JA, García-Sánchez MJ, Felle HH (1999) Physiological evidence for a proton pump and sodium exclusion mechanisms at the plasma membrane of the marine angiosperm Zostera marina L. J Exp Bot 50:1763–1768Google Scholar
  51. Field CD, Flowers TJ, Hall JL (1980) Rubidium transport in membrane vesicles from the halophyte Suaeda maritima. Ann Bot 46:401–407CrossRefGoogle Scholar
  52. Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963PubMedCrossRefPubMedCentralGoogle Scholar
  53. Flowers TJ, Dalmond D (1992) Protein synthesis in halophytes: the influence of potassium, sodium and magnesium in vitro. Plant Soil 146:153–161CrossRefGoogle Scholar
  54. Flowers TJ, Yeo AR (1986) Ion relations of plants under drought and salinity. Aust J Plant Physiol 13:75–91Google Scholar
  55. Flowers T, Yeo AR (2007) The driving forces for water and solute movement. In: Yeo AR, Flowers TJ (eds) Plant solute transport. Blackwell, Oxford, pp 29–46CrossRefGoogle Scholar
  56. Flowers TJ, Troke PF, Yeo AR (1977) The mechanism of salt tolerance in halophytes. Annu Rev Plant Physiol 28:89–121CrossRefGoogle Scholar
  57. Flowers TJ, Galal HK, Bromham L (2010) Evolution of halophytes: multiple origins of salt tolerance in land plants. Funct Plant Biol 37:604–612CrossRefGoogle Scholar
  58. Flowers TJ, Munns R, Colmer TD (2015) Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Ann Bot 115:419–431PubMedCrossRefPubMedCentralGoogle Scholar
  59. Flowers TJ, Glenn EP, Volkov V (2018) Could vesicular transport of Na+ and Cl- be a feature of salt tolerance in halophytes? Ann Bot  https://doi.org/10.1093/aob/mcy164 CrossRefGoogle Scholar
  60. Fricke W, Leigh RA, Tomos AD (1994) Epidermal solute concentrations and osmolality in barley leaves studied at the single-cell level. Planta 192:317–323Google Scholar
  61. Fricke W, Akhiyarova G, Wei W, Alexandersson E, Miller A, Kjellbom PO et al (2006) The short-term growth response to salt of the developing barley leaf. J Exp Bot 57:1079–1095PubMedCrossRefPubMedCentralGoogle Scholar
  62. Gadsby DC (2009) Ion channels versus ion pumps: the principal difference, in principle. Nat Rev Mol Cell Biol 10:344–352PubMedPubMedCentralCrossRefGoogle Scholar
  63. Galdiero S, Falanga A, Cantisani M, Tarallo R, Della Pepa ME, D’Oriano V et al (2012) Microbe-host interactions: structure and role of Gram-negative bacterial porins. Curr Protein Pept Sci 13:843–854PubMedPubMedCentralCrossRefGoogle Scholar
  64. Garciadeblás B, Senn ME, Bañuelos MA, Rodríguez-Navarro A (2003) Sodium transport and HKT transporters: the rice model. Plant J 34:788–801PubMedCrossRefPubMedCentralGoogle Scholar
  65. Gibson TS, Speirs J, Brady CJ (1984) Salt-tolerance in plants. II. In vivo translation of m-RNAs from salt-tolerant and salt-sensitive plants on wheat germ ribosomes. Responses to ions and compatible organic solutes. Plant Cell Environ 7:579–587Google Scholar
  66. Grabov A (2007) Plant KT/KUP/HAK potassium transporters: single family – multiple functions. Ann Bot 99:1035–1041PubMedPubMedCentralCrossRefGoogle Scholar
  67. Greiner T, Ramos J, Alvarez MC, Gurnon JR, Kang M, Van Etten JL et al (2011) Functional HAK/KUP/KT-like potassium transporter encoded by chlorella viruses. Plant J 68:977–986PubMedCrossRefPubMedCentralGoogle Scholar
  68. Hajibagheri MA, Flowers TJ (1989) X-ray microanalysis of ion distribution within root cortical cells of the halophyte Suaeda maritima (L.) Dum. Planta 177:131–134PubMedCrossRefPubMedCentralGoogle Scholar
  69. Hajibagheri MA, Flowers TJ, Collins JC, Yeo AR (1988) A comparison of the methods of X-ray microanalysis. J Exp Bot 39:279–290CrossRefGoogle Scholar
  70. Hall JL, Flowers TJ (1973) The effect of salt on protein synthesis in the halophyte Suaeda maritima. Planta 110:361–368PubMedCrossRefPubMedCentralGoogle Scholar
  71. Halperin SJ, Lynch JP (2003) Effects of salinity on cytosolic Na+ and K+ in root hairs of Arabidopsis thaliana: in vivo measurements using the fluorescent dyes SBFI and PBFI. J Exp Bot 54:2035–2043PubMedCrossRefPubMedCentralGoogle Scholar
  72. Hammou KA, Rubio L, Fernández JA, García-Sánchez MJ (2014) Potassium uptake in the halophyte Halimione portulacoides L. Aellen. Environ Exp Bot 107:15–24CrossRefGoogle Scholar
  73. Haro R, Bañuelos MA, Senn ME, Barrero-Gil J, Rodríguez-Navarro A (2005) HKT1 mediates sodium uniport in roots. Pitfalls in the expression of HKT1 in yeast. Plant Physiol 139:1495–1506PubMedPubMedCentralCrossRefGoogle Scholar
  74. Haro R, Bañuelos MA, Rodríguez-Navarro A (2010) High-affinity sodium uptake in land plants. Plant Cell Physiol 51:68–79PubMedCrossRefPubMedCentralGoogle Scholar
  75. Heginbotham L, Abramson T, MacKinnon R (1992) A functional connection between the pores of distantly related ion channels as revealed by mutant K+ channels. Science 258:1152–1155PubMedCrossRefPubMedCentralGoogle Scholar
  76. Hellblom F, Beer S, Björk M, Axelsson L (2001) A buffer sensitive inorganic carbon utilisation system in Zostera marina. Aquat Bot 69:55–62CrossRefGoogle Scholar
  77. Higinbotham N (1973) Electropotentials of plant cells. Annu Rev Plant Physiol 24:25–46CrossRefGoogle Scholar
  78. Hille B (2001) Ion channels and excitable membranes, 3rd edn. Sinauer Associates, Sunderland. 814 pGoogle Scholar
  79. Hinke JAM (1959) Glass micro-electrodes for measuring intracellular activities of sodium and potassium. Nature 184:1257–1258PubMedCrossRefPubMedCentralGoogle Scholar
  80. Hirsch RE, Lewis BD, Spalding EP, Sussman MR (1998) A role for the AKT1 potassium channel in plant nutrition. Science 280:918–921PubMedCrossRefPubMedCentralGoogle Scholar
  81. Hu J, Ma Q, Kumar T, Duan H-R, Zhang J-L, Yuan H-J, Wang Q, Ali Khan S, Wang P, Suo-Min Wang S-M (2016) ZxSKOR is important for salinity and drought tolerance of Zygophyllum xanthoxylum by maintaining K+ homeostasis. Plant Growth Regul 80:195–205.  https://doi.org/10.1007/s10725-016-0157-z CrossRefGoogle Scholar
  82. Hughes FM Jr, Cidlowski JA (1999) Potassium is a critical regulator of apoptotic enzymes in vitro and in vivo. Adv Enzym Regul 39:157–171CrossRefGoogle Scholar
  83. Huh GH, Damsz B, Matsumoto TK, Reddy MP, Rus AM, Ibeas JI et al (2002) Salt causes ion disequilibrium-induced programmed cell death in yeast and plants. Plant J 29:649–659PubMedCrossRefPubMedCentralGoogle Scholar
  84. Hunte C, Screpanti E, Venturi M, Rimon A, Padan E, Michel H (2005) Structure of a Na+/H+ antiporter and insights into mechanism of action and regulation by pH. Nature 435:1197–1202PubMedCrossRefPubMedCentralGoogle Scholar
  85. Jennings DH (1976) The effects of sodium chloride on higher plants. Biol Rev 51:453–486CrossRefGoogle Scholar
  86. Jiang Y, Lee A, Chen J, Cadene M, Chait BT, MacKinnon R (2002) The open pore conformation of potassium channels. Nature 417:523–526PubMedCrossRefPubMedCentralGoogle Scholar
  87. Kato N, Akai M, Zulkifli L, Matsuda N, Kato Y, Goshima S et al (2007) Role of positively charged amino acids in the M2D transmembrane helix of Ktr/Trk/HKT type cation transporters. Channels (Austin) 1:161–171CrossRefGoogle Scholar
  88. Katsuhara M, Kawasaki T (1996) Salt stress induced nuclear and DNA degradation in meristematic cells of barley roots. Plant Cell Physiol 37:169–173CrossRefGoogle Scholar
  89. Köhler B (2007) Step by step: deciphering ion transport in the root xylem parenchyma. Plant Signal Behav 2:303–305PubMedPubMedCentralCrossRefGoogle Scholar
  90. Korolev AV, Tomos AD, Bowtell R, Farrar JF (2000) Spatial and temporal distribution of solutes in the developing carrot taproot measured at single-cell resolution. J Exp Bot 51:567–577PubMedCrossRefPubMedCentralGoogle Scholar
  91. Kronzucker HJ, Britto DT (2011) Sodium transport in plants: a critical review. New Phytol 189:54–81PubMedCrossRefPubMedCentralGoogle Scholar
  92. Kronzucker HJ, Coskun D, Schulze LM, Wong JR, Britto DT (2013) Sodium as nutrient and toxicant. Plant Soil 369:1–23CrossRefGoogle Scholar
  93. L’Roy A, Hendrix DL (1980) Effect of salinity upon cell membrane potential in the marine halophyte, Salicornia bigelovii Torr. Plant Physiol 65:544–549PubMedPubMedCentralCrossRefGoogle Scholar
  94. Li L, Kim B-G, Cheong YH, Pandey GK, Luan S (2006) A Ca2+ signaling pathway regulates a K+ channel for low-K response in Arabidopsis. PNAS 103:12625–12630PubMedCrossRefPubMedCentralGoogle Scholar
  95. Longpré JP, Lapointe JY (2011) Determination of the Na+/glucose cotransporter (SGLT1) turnover rate using the ion-trap technique. Biophys J 100:52–59PubMedPubMedCentralCrossRefGoogle Scholar
  96. Lunde C, Drew DP, Jacobs AK, Tester M (2007) Exclusion of Na+ via sodium ATPase (PpENA1) ensures normal growth of Physcomitrella patens under moderate salt stress. Plant Physiol 144:1786–1796PubMedPubMedCentralCrossRefGoogle Scholar
  97. M’Rah S, Ouerghi Z, Eymery F, Rey P, Hajji M, Grignon C, Lachaal M (2007) Efficiency of biochemical protection against toxic effects of accumulated salt differentiates Thellungiella halophila from Arabidopsis thaliana. J Plant Physiol 164:375–384PubMedCrossRefPubMedCentralGoogle Scholar
  98. Ma Q, Li YX, Yuan HJ, Hu J, Wei L, Bao AK, Zhang JL, Wang S-M (2014) ZxSOS1 is essential for long-distance transport and spatial distribution of Na+ and K+ in the xerophyte Zygophyllum xanthoxylum. Plant Soil 374:661–676CrossRefGoogle Scholar
  99. Maathuis FJM, Amtmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Ann Bot 84:123–133CrossRefGoogle Scholar
  100. Maathuis FJ, Prins HB (1990) Patch clamp studies on root cell vacuoles of a salt-tolerant and a salt-sensitive Plantago species. Plant Physiol 92:23–28PubMedPubMedCentralCrossRefGoogle Scholar
  101. Maathuis FJM, Sanders D (2001) Sodium uptake in Arabidopsis roots is regulated by cyclic nucleotides. Plant Physiol 127:1617–1625PubMedPubMedCentralCrossRefGoogle Scholar
  102. Maathuis FJM, Flowers TJ, Yeo AR (1992) Sodium-chloride compartmentation in leaf vacuoles of the halophyte Suaeda maritima (L) Dum. and its relation to tonoplast permeability. J Exp Bot 43:1219–1223CrossRefGoogle Scholar
  103. Maathuis FJM, Ahmad I, Patishtan J (2014) Regulation of Na+ fluxes in plants. Front Plant Sci 5:467.  https://doi.org/10.3389/fpls.2014.00467 CrossRefPubMedPubMedCentralGoogle Scholar
  104. MacKinnon R (2004) Potassium channels and the atomic basis of selective ion conduction (Nobel Lecture). Angew Chem Int Ed Engl 43:4265–4277PubMedCrossRefPubMedCentralGoogle Scholar
  105. Maffeo C, Bhattacharya S, Yoo J, Wells D, Aksimentiev A (2012) Modeling and simulation of ion channels. Chem Rev 112:6250–6284PubMedPubMedCentralCrossRefGoogle Scholar
  106. Mähler J, Persson I (2012) A study of the hydration of the alkali metal ions in aqueous solution inorganic chemistry. Am Chem Soc 51:425–438Google Scholar
  107. Malone M, Leigh RA, Tomos AD (1991) Concentrations of vacuolar inorganic ions in individual cells of intact wheat leaf epidermis. J Exp Bot 42:305–309CrossRefGoogle Scholar
  108. Martinoia E, Meyer S, De Angeli A, Nagy R (2012) Vacuolar transporters in their physiological context. Annu Rev Plant Biol 63:183–213PubMedCrossRefPubMedCentralGoogle Scholar
  109. Mäser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H et al (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667PubMedPubMedCentralCrossRefGoogle Scholar
  110. Matzke AJ, Matzke M (2013) Membrane “potential-omics”: toward voltage imaging at the cell population level in roots of living plants. Front Plant Sci 4:311.  https://doi.org/10.3389/fpls.2013.00311 CrossRefPubMedPubMedCentralGoogle Scholar
  111. Mercado JM, Niell FX, Silva J, Santos R (2003) Use of light and inorganic carbon acquisition by two morphotypes of Zostera noltii Hornem. J Exp Mar Biol Ecol 297:71–84CrossRefGoogle Scholar
  112. Mercado JM, Andría JR, Pérez-Llorens JL, Vergara JJ, Axelsson L (2006) Evidence for a plasmalemma-based CO2 concentrating mechanism in Laminaria saccharina. Photosynth Res 88:259–268PubMedCrossRefPubMedCentralGoogle Scholar
  113. Murthy M, Tester M (2006) Cation currents in protoplasts from the roots of a Na+ hyperaccumulating mutant of Capsicum annuum. J Exp Bot 57:1171–1180PubMedCrossRefPubMedCentralGoogle Scholar
  114. Mutoh H, Akemann W, Knöpfel T (2012) Genetically engineered fluorescent voltage reporters. ACS Chem Neurosci 3:585–592PubMedPubMedCentralCrossRefGoogle Scholar
  115. Neales TF, Sharkey PJ (1981) Effect of salinity on growth and on mineral and organic constituents of the halophyte Disphyma australe (Soland.) J.M. Black. Aust J Plant Physiol 8:165–179Google Scholar
  116. Nieves-Cordones M, Martinez V, Benito B, Rubio F (2016) 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 CrossRefPubMedPubMedCentralGoogle Scholar
  117. Nightingale ER Jr (1959) Phenomenological theory of ion solvation. Effective radii of hydrated ions. Ions J Phys Chem 63:1381–1387CrossRefGoogle Scholar
  118. Niu X, Narasimhan ML, Salzman RA, Bressan RA, Hasegawa PH (1993) NaCl regulation of plasma membrane H+-ATPase gene expression in a glycophyte and a halophyte. Plant Physiol 103:713–718PubMedPubMedCentralCrossRefGoogle Scholar
  119. Nobel PS (2005) Physicochemical and environmental plant physiology, 3rd edn. Academic, Burlington. 540 pGoogle Scholar
  120. Núñez-Ramírez R, Sánchez-Barrena MJ, Villalta I, Vega JF, Pardo JM, Quintero FJ et al (2012) Structural insights on the plant salt-overly-sensitive 1 (SOS1) Na+/H+ antiporter. J Mol Biol 424:283–294PubMedCrossRefPubMedCentralGoogle Scholar
  121. Oh DH, Leidi E, Zhang Q, Hwang SM, Li Y, Quintero FJ, Jiang X, D’Urzo MP, Lee SY, Zhao Y, Bahk JD, Bressan RA, Yun D-J, Pardo JM, Bohnert HJ (2009) Loss of halophytism by interference with SOS1 expression. Plant Physiol 151:210–222PubMedPubMedCentralCrossRefGoogle Scholar
  122. Palmgren MG (2001) PLANT PLASMA MEMBRANE H+-ATPases: powerhouses for nutrient uptake. Annu Rev Plant Physiol Plant Mol Biol 52:817–845PubMedCrossRefPubMedCentralGoogle Scholar
  123. Pan Y-Q, Guo H, Wang S-M, Zhao B, Zhang J-L, Ma Q, Yin H-J, Bao A-K (2016) The photosynthesis, Na+/K+ homeostasis and osmotic adjustment of Atriplex canescens in response to salinity. Front Plant Sci 7:848.  https://doi.org/10.3389/fpls.2016.00848 CrossRefPubMedPubMedCentralGoogle Scholar
  124. Parrondo RT, Gosselink JG, Hopkinson CS (1978) Effects of salinity and drainage on the growth of three salt marsh grasses. Bot Gaz 139:102–107CrossRefGoogle Scholar
  125. Pitman MG, Läuchli A, Stelzer R (1981) Ion distribution in roots of barley seedlings measured by electron probe x-ray microanalysis. Plant Physiol 68:673–679PubMedPubMedCentralCrossRefGoogle Scholar
  126. Premkumar L, Greenblatt HM, Bagashwar UK, Savchenko T, Gokhman I, Sussman JL et al (2005) 3D structure of a halotolerant algal carbonic anhydrase predicts halotolerance of a mammalian homolog. Proc Natl Acad Sci U S A 102:7493–7498PubMedPubMedCentralCrossRefGoogle Scholar
  127. Qi Z, Spalding EP (2004) Protection of plasma membrane K+ transport by the salt overly sensitive Na+–H+ antiporter during salinity stress. Plant Physiol 136:2548–2555PubMedPubMedCentralCrossRefGoogle Scholar
  128. Robinson MF, Véry A-A, Sanders D, Mansfield TA (1997) How can stomata contribute to salt tolerance? Ann Bot 80:387–393CrossRefGoogle Scholar
  129. Rodriguez-Navarro A (2000) Potassium transport in fungi and plants. BBA Rev Biomembr 1469:1–30Google Scholar
  130. Rodríguez-Navarro A, Rubio F (2006) High-affinity potassium and sodium transport systems in plants. J Exp Bot 57:1149–1160PubMedCrossRefPubMedCentralGoogle Scholar
  131. Rubio L, Belver A, Venema K, García-Sánchez MJ, Fernández JA (2011) Evidence for a sodium efflux mechanism in the leaf cells of the seagrass Zostera marina L. J Exp Mar Biol Ecol 402:56–64CrossRefGoogle Scholar
  132. Sejersted OM, Sjøgaard G (2000) Dynamics and consequences of potassium shifts in skeletal muscle and heart during exercise. Physiol Rev 80:1411–1481PubMedCrossRefPubMedCentralGoogle Scholar
  133. Serrano R (1988) Structure and function of proton translocating ATPase in plasma membranes of plants and fungi. Biochim Biophys Acta 947:1–28PubMedCrossRefPubMedCentralGoogle Scholar
  134. Shabala S (2009) Salinity and programmed cell death: unravelling mechanisms for ion specific signalling. J Exp Bot 60:709–712PubMedCrossRefPubMedCentralGoogle Scholar
  135. Shabala SN, Lew RR (2002) Turgor regulation in osmotically stressed Arabidopsis epidermal root cells. Direct support for the role of inorganic ion uptake as revealed by concurrent flux and cell turgor measurements. Plant Physiol 129:290–299PubMedPubMedCentralCrossRefGoogle Scholar
  136. Shabala S, Mackay A (2011) Ion transport in halophytes. Adv Bot Res 57:151–199CrossRefGoogle Scholar
  137. Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ, Miller AJ et al (2006) Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+-permeable channels. Plant Physiol 141:1653–1665PubMedPubMedCentralCrossRefGoogle Scholar
  138. Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci U S A 97:6896–6901PubMedPubMedCentralCrossRefGoogle Scholar
  139. Shomer I, Novacky AJ, Pike SM, Yermiyahu U, Kinraide TB (2003) Electrical potentials of plant cell walls in response to the ionic environment. Plant Physiol 133:411–422PubMedPubMedCentralCrossRefGoogle Scholar
  140. Shuyskaya EV, Rakhamkulova ZF, Lebedeva MP, Kolesnikov AV, Safarova A, Borisochkina TI, Toderich KN (2017) Different mechanisms of ion homeostasis are dominant in the recretohalophyte Tamarix ramosissima under different soil salinity. Acta Physiol Plant 39:1–12CrossRefGoogle Scholar
  141. Skou JC (1998) Nobel Lecture. The identification of the sodium pump. Biosci Rep 18:155–169PubMedCrossRefPubMedCentralGoogle Scholar
  142. Stelzer R, Läuchli A (1977) Salt- and flooding tolerance of Puccinellia peisonis. I The effect of NaCl- and KCl-salinity on growth at varied oxygen supply to the root. Zeitschrift Fur Pflanzenphysiologie 83:35–42CrossRefGoogle Scholar
  143. Su H, Golldack D, Katsuhara M, Zhao C, Bohnert HJ (2001) Expression and stress-dependent induction of potassium channel transcripts in the common ice plant. Plant Physiol 125:604–614PubMedPubMedCentralCrossRefGoogle Scholar
  144. Su H, Golldack D, Zhao C, Bohnert HJ (2002) The expression of HAK-type K+ transporters is regulated in response to salinity stress in common ice plant. Plant Physiol 129:1482–1493PubMedPubMedCentralCrossRefGoogle Scholar
  145. Su H, Balderas E, Vera-Estrella R, Golldack D, Quigley F, Zhao C, Pantoja O, Bohnert HJ (2003) Expression of the cation transporter McHKT1 in a halophyte. Plant Mol Biol 52:967–980PubMedCrossRefPubMedCentralGoogle Scholar
  146. Subbarao GV, Ito O, Berry WL, Wheeler RM (2003) Sodium – a functional plant nutrient. Crit Rev Plant Sci 22:391–416Google Scholar
  147. Sze H, Li X, Palmgren MG (1999) Energization of plant cell membranes by H+-pumping ATPases. Regulation and biosynthesis. Plant Cell 11:677–690PubMedPubMedCentralGoogle Scholar
  148. Thiyagarajah M, Fry SC, Yeo AR (1996) In vitro salt tolerance of cell wall enzymes from halophytes and glycophytes. J Exp Bot 47:1717–1724CrossRefGoogle Scholar
  149. Véry A-A, Robinson MF, Mansfield TA, Sanders D (1998) Guard cell cation channels are involved in Na+ induced stomatal closure in a halophyte. Plant J 14:509–521CrossRefGoogle Scholar
  150. Volkov V (2015a) Quantitative description of ion transport via plasma membrane of yeast and small cells. Front Plant Sci 6:425.  https://doi.org/10.3389/fpls.2015.00425 CrossRefPubMedPubMedCentralGoogle Scholar
  151. Volkov V (2015b) Salinity tolerance in plants. Quantitative approach to ion transport starting from halophytes and stepping to genetic and protein engineering for manipulating ion fluxes. Front Plant Sci 6:873.  https://doi.org/10.3389/fpls.2015.00873 CrossRefPubMedPubMedCentralGoogle Scholar
  152. Volkov V, Amtmann A (2006) Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana, has specific root ion-channel features supporting K+/Na+ homeostasis under salinity stress. Plant J 48:342–353PubMedCrossRefPubMedCentralGoogle Scholar
  153. Volkov V, Wang B, Dominy PJ, Fricke W, Amtmann A (2004) Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana, possesses effective mechanisms to discriminate between potassium and sodium. Plant Cell Environ 27:1–14CrossRefGoogle Scholar
  154. Walker DJ, Smith SJ, Miller AJ (1995) Simultaneous measurement of intracellular pH and K+ or NO3 in barley root cells using triple-barreled, ion-selective microelectrodes. Plant Physiol 108:743–751PubMedPubMedCentralCrossRefGoogle Scholar
  155. Walker DJ, Black CR, Miller AJ (1998) The role of cytosolic potassium and pH in the growth of barley roots. Plant Physiol 118:957–964PubMedPubMedCentralCrossRefGoogle Scholar
  156. Wang B (2006) Physiological and molecular strategies for salt tolerance in Thellungiella halophila, a close relative of Arabidopsis thaliana. Ph.D. thesis, Division of Biochemistry and Molecular Biology, Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow, p 235Google Scholar
  157. Wang B, Davenport RJ, Volkov V, Amtmann A (2006) Low unidirectional sodium influx into root cells restricts net sodium accumulation in Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana. J Exp Bot 57:1161–1170PubMedCrossRefPubMedCentralGoogle Scholar
  158. Wang S-M, Zhang J-L, Flowers TJ (2007) Low-affinity Na+ uptake in the halophyte Suaeda maritima. Plant Physiol 145:559–571PubMedPubMedCentralCrossRefGoogle Scholar
  159. Waters S, Gilliham M, Hrmova M (2013) Plant high-affinity potassium (HKT) transporters involved in salinity tolerance: structural insights to probe differences in ion selectivity. Int J Mol Sci 14:7660–7680PubMedPubMedCentralCrossRefGoogle Scholar
  160. Wegner LH, De Boer AH (1997a) Properties of two outward-rectifying channels in root xylem parenchyma cells suggest a role in K+ homeostasis and long-distance signaling. Plant Physiol 115:1707–1719PubMedPubMedCentralCrossRefGoogle Scholar
  161. Wegner LH, De Boer AH (1997b) Two inward K+ channels in the xylem parenchyma cells of barley roots are regulated by G-protein modulators through a membrane-delimited pathway. Planta 203:506–516CrossRefGoogle Scholar
  162. Wegner LH, Raschke K (1994) Ion channels in the xylem parenchyma of barley roots. Plant Physiol 105:799–813PubMedPubMedCentralCrossRefGoogle Scholar
  163. White PJ, Lemtiri-Chlieh F (1995) Potassium currents across the plasma membrane of protoplasts derived from rye roots: a patch clamp study. J Exp Bot 46:497–511CrossRefGoogle Scholar
  164. Wu SJ, Ding L, Zhu JK (1996) SOS1, a genetic locus essential for salt tolerance and potassium acquisition. Plant Cell 8:617–627PubMedPubMedCentralCrossRefGoogle Scholar
  165. Wyn Jones RGA, Pollard A (1983) Proteins, enzymes and inorganic ions. In: Lauchli A, Person A (eds) Encyclopedia of plant physiology, New series, vol 15B. Springer, New York, pp 528–562Google Scholar
  166. Xu J, Li H-D, Chen L-Q, Wang Y, Liu L-L, He L, Wu W-H (2006) A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125:1347–1360PubMedCrossRefPubMedCentralGoogle Scholar
  167. Yamaguchi T, Hamamoto S, Uozumi N (2013) Sodium transport system in plant cells. Front Plant Sci 4:410PubMedPubMedCentralCrossRefGoogle Scholar
  168. Yeo AR (1981) Salt tolerance in the halophyte Suaeda maritima (L.) Dum.: intracellular compartmentation of ions. J Exp Bot 32:487–497CrossRefGoogle Scholar
  169. Yeo AR, Flowers TJ (1980) Salt tolerance in the halophyte Suaeda maritima (L.) Dum.: evaluation of the effect of salinity upon growth. J Exp Bot 31:1171–1183CrossRefGoogle Scholar
  170. Yeo AR, Flowers TJ (1986) Ion transport in Suaeda maritima: its relation to growth and implications for the pathway of radial transport of ions across the root. J Exp Bot 37:143–159CrossRefGoogle Scholar
  171. Yuan H-J, Ma Q, Wu G-Q, Wang P, Hu J, Wang S-M (2015) ZxNHX controls Na+ and K+ homeostasis at the whole-plant level in Zygophyllum xanthoxylum through feedback regulation of the expression of genes involved in their transport. Ann Bot 115:495–507PubMedCrossRefPubMedCentralGoogle Scholar
  172. Yuan F, Leng B, Wang B (2016) Progress in studying salt secretion from the salt glands in Recretohalophytes: how do plants secrete salt? Front Plant Sci 7:977.  https://doi.org/10.3389/fpls.2016.00977 CrossRefPubMedPubMedCentralGoogle Scholar
  173. Yue LJ, Li SX, Ma Q, Zhou XR, Wu GQ, Bao AK, Zhang JL, Wang SM (2012) NaCl stimulates growth and alleviates water stress in the xerophyte Zygophyllum xanthoxylum. J Arid Environ 87:153–160CrossRefGoogle Scholar
  174. Zahran HH, Marín-Manzano MC, Sánchez-Raya AJ, Bedmar EJ, Venema K, Rodríguez-Rosales MP (2007) Effect of salt stress on the expression of NHX-type ion transporters in Medicago intertexta and Melilotus indicus plants. Physiol Plant 131:122–130PubMedCrossRefPubMedCentralGoogle Scholar
  175. Zhao KF, Fan H, Song J, Sun MX, Wang BZ, Zhang SQ et al (2005) Two Na+ and Cl hyperaccumulators of the Chenopodiaceae. J Integr Plant Biol 47:311–318CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Vadim Volkov
    • 1
    • 2
  • Timothy J. Flowers
    • 3
    • 4
  1. 1.Faculty of Life Sciences and ComputingLondon Metropolitan UniversityLondonUK
  2. 2.Department of Plant Sciences, College of Agricultural and Environmental SciencesUniversity of CaliforniaDavisUSA
  3. 3.School of Life SciencesUniversity of SussexBrightonUK
  4. 4.School of Plant BiologyThe University of Western AustraliaCrawleyAustralia

Personalised recommendations