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Mechanisms of Ion Transport in Halophytes: From Roots to Leaves

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Sabkha Ecosystems

Part of the book series: Tasks for Vegetation Science ((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.

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Notes

  1. 1.

    We have used names as in The Plant List (http://www.theplantlist.org) and added in parentheses the name used in the publications we cite. However, we have NOT changed the names of genes or proteins.

References

  • 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):12–17

    CAS  Google Scholar 

  • 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 176:768–774

    Google Scholar 

  • 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 5:430

    PubMed  PubMed Central  Google Scholar 

  • 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:e25196

    PubMed  PubMed Central  Google Scholar 

  • Amtmann A (2009) Learning from evolution: Thellungiella generates new knowledge on essential and critical components of abiotic stress tolerance in plants. Mol Plant 2:3–12

    CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson WP, Willcocks DA, Wright BJ (1977) Electrophysiological measurements on root of Atriplex hastata. J Exp Bot 28:894–901

    CAS  Google Scholar 

  • 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 150:772–785

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 364:145–147

    Google Scholar 

  • Axelsson L, Mercado J, Figueroa F (2000) Utilization of HCO3− at high pH by the brown macroalga Laminaria saccharina. Eur J Phycol 35:53–59

    Google Scholar 

  • 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 54:797–805

    CAS  Google Scholar 

  • 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 14:3021–3027

    PubMed  PubMed Central  Google Scholar 

  • Barkla BJ, Vera-Estrella R, Pantoja O (2012) Protein profiling of epidermal bladder cells from the halophyte Mesembryanthemum crystallinum. Proteomics 12:2862–2865

    CAS  PubMed  Google Scholar 

  • 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 809:231–239

    CAS  Google Scholar 

  • Benito B, Rodríguez-Navarro A (2003) Molecular cloning and characterization of a sodium-pump ATPase of the moss Physcomitrella patens. Plant J 36:382–389

    CAS  PubMed  Google Scholar 

  • Benito B, Haro R, Amtmann A, Cuin TA, Dreyer I (2014) The twins K+ and Na+ in plants. J Plant Physiol 171:723–731

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 170:272–287

    CAS  PubMed  Google Scholar 

  • Blatt MR (1991) A primer in plant electrophysiological methods. In: Hostettmann K (ed) Methods in plant biochemistry. Academic, London, pp 281–321

    Google Scholar 

  • 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 32:1761–1777

    CAS  PubMed  Google Scholar 

  • 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 115:481–494

    PubMed  Google Scholar 

  • Briggs GE, Hope AB (1958) Electric potential differences and the Donnan equilibrium in plant tissues. J Exp Bot 9:365–371

    CAS  Google Scholar 

  • Briggs GE, Robertson RN (1957) Apparent free space. Ann Rev Plant Physiol 8:11–30

    CAS  Google Scholar 

  • Britto DT, Kronzucker HJ (2008) Cellular mechanisms of potassium transport in plants. Physiol Plant 133:637–650

    CAS  PubMed  Google Scholar 

  • Cakirlar H, Bowling DJF (1981) The effect of salinity on the membrane potential of sunflower roots. J Exp Bot 32:479–485

    Google Scholar 

  • Campion DS (1974) Resting membrane potential and ionic distribution in fast- and slow-twitch mammalian muscle. J Clin Invest 54:514–518

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cao Y, Jin X, Huang H, Derebe MG, Levin EJ, Kabaleeswaran V et al (2011) Crystal structure of a potassium ion transporter, TrkH. Nature 471:336–340

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carden DE, Diamond D, Miller AJ (2001) An improved Na+-selective microelectrode for intracellular measurements in plant cells. J Exp Bot 52:1353–1359

    CAS  PubMed  Google Scholar 

  • 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 131:676–683

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e12605

    PubMed  PubMed Central  Google Scholar 

  • Carr H, Axelsson L (2008) Photosynthetic utilization of bicarbonate in Zostera marina is reduced by inhibitors of mitochondrial ATPase and electron transport. Plant Physiol 147:879–885

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chakrapani S, Auerbach A (2005) A speed limit for conformational change of an allosteric membrane protein. Proc Natl Acad Sci U S A 102:87–92

    CAS  PubMed  Google Scholar 

  • 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 145:1714–1725

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 105:359–366

    CAS  PubMed  Google Scholar 

  • Collins KD (1997) Charge density-dependent strength of hydration and biological structure. Biophys J 72:65–76

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cuin TA, Miller AJ, Laurie SA, Leigh RA (2003) Potassium activities in cell compartments of salt-grown barley leaves. J Exp Bot 54:657–661

    CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 43:913–918

    CAS  PubMed  PubMed Central  Google Scholar 

  • Davenport R (2002) Glutamate receptors in plants. Ann Bot 90:549–557

    CAS  PubMed  PubMed Central  Google Scholar 

  • de Almeida PMF (2014) The role of HKT transporters in salinity tolerance of tomato. Ph.D. thesis, Vrije Universiteit, Amsterdam, p 219

    Google Scholar 

  • De Boer AH (1985) Xylem/symplast ion exchange: mechanism and function in salt tolerance and growth. Ph.D. thesis, Rijksuniversiteit Groningen, Groningen

    Google Scholar 

  • De Boer AH, Volkov V (2003) Logistics of water and salt transport through the plant: structure and functioning of the xylem. Plant Cell Environ 26:87–101

    Google Scholar 

  • Demidchik V, Maathuis FJ (2007) Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytol 175:387–404

    CAS  PubMed  Google Scholar 

  • Demidchik V, Tester M (2002) Sodium fluxes through nonselective cation channels in the plasma membrane of protoplasts from Arabidopsis roots. Plant Physiol 128:379–387

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 123:1468–1479

    CAS  PubMed  Google Scholar 

  • 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 280:69–77

    CAS  PubMed  Google Scholar 

  • English JP, Colmer TD (2013) Tolerance of extreme salinity in two stem-succulent halophytes (Tecticornia species). Funct Plant Biol 40:897–912

    CAS  PubMed  Google Scholar 

  • 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 47:95–99

    CAS  Google Scholar 

  • Essah PA, Davenport R, Tester M (2003) Sodium influx and accumulation in Arabidopsis. Plant Physiol 133:307–318

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 63:59–67

    CAS  PubMed  Google Scholar 

  • 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 50:1763–1768

    Google Scholar 

  • Field CD, Flowers TJ, Hall JL (1980) Rubidium transport in membrane vesicles from the halophyte Suaeda maritima. Ann Bot 46:401–407

    CAS  Google Scholar 

  • Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963

    CAS  PubMed  Google Scholar 

  • Flowers TJ, Dalmond D (1992) Protein synthesis in halophytes: the influence of potassium, sodium and magnesium in vitro. Plant Soil 146:153–161

    CAS  Google Scholar 

  • Flowers TJ, Yeo AR (1986) Ion relations of plants under drought and salinity. Aust J Plant Physiol 13:75–91

    CAS  Google Scholar 

  • 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 29–46

    Google Scholar 

  • Flowers TJ, Troke PF, Yeo AR (1977) The mechanism of salt tolerance in halophytes. Annu Rev Plant Physiol 28:89–121

    CAS  Google Scholar 

  • Flowers TJ, Galal HK, Bromham L (2010) Evolution of halophytes: multiple origins of salt tolerance in land plants. Funct Plant Biol 37:604–612

    Google Scholar 

  • Flowers TJ, Munns R, Colmer TD (2015) Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Ann Bot 115:419–431

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  Google Scholar 

  • Fricke W, Leigh RA, Tomos AD (1994) Epidermal solute concentrations and osmolality in barley leaves studied at the single-cell level. Planta 192:317–323

    CAS  Google Scholar 

  • 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 57:1079–1095

    CAS  PubMed  Google Scholar 

  • Gadsby DC (2009) Ion channels versus ion pumps: the principal difference, in principle. Nat Rev Mol Cell Biol 10:344–352

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 13:843–854

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garciadeblás B, Senn ME, Bañuelos MA, Rodríguez-Navarro A (2003) Sodium transport and HKT transporters: the rice model. Plant J 34:788–801

    PubMed  Google Scholar 

  • 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 7:579–587

    CAS  Google Scholar 

  • Grabov A (2007) Plant KT/KUP/HAK potassium transporters: single family – multiple functions. Ann Bot 99:1035–1041

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 68:977–986

    CAS  PubMed  Google Scholar 

  • Hajibagheri MA, Flowers TJ (1989) X-ray microanalysis of ion distribution within root cortical cells of the halophyte Suaeda maritima (L.) Dum. Planta 177:131–134

    CAS  PubMed  Google Scholar 

  • Hajibagheri MA, Flowers TJ, Collins JC, Yeo AR (1988) A comparison of the methods of X-ray microanalysis. J Exp Bot 39:279–290

    CAS  Google Scholar 

  • Hall JL, Flowers TJ (1973) The effect of salt on protein synthesis in the halophyte Suaeda maritima. Planta 110:361–368

    CAS  PubMed  Google Scholar 

  • 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 54:2035–2043

    CAS  PubMed  Google Scholar 

  • Hammou KA, Rubio L, Fernández JA, García-Sánchez MJ (2014) Potassium uptake in the halophyte Halimione portulacoides L. Aellen. Environ Exp Bot 107:15–24

    Google Scholar 

  • 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 139:1495–1506

    CAS  PubMed  PubMed Central  Google Scholar 

  • Haro R, Bañuelos MA, Rodríguez-Navarro A (2010) High-affinity sodium uptake in land plants. Plant Cell Physiol 51:68–79

    CAS  PubMed  Google Scholar 

  • 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 258:1152–1155

    CAS  PubMed  Google Scholar 

  • Hellblom F, Beer S, Björk M, Axelsson L (2001) A buffer sensitive inorganic carbon utilisation system in Zostera marina. Aquat Bot 69:55–62

    CAS  Google Scholar 

  • Higinbotham N (1973) Electropotentials of plant cells. Annu Rev Plant Physiol 24:25–46

    CAS  Google Scholar 

  • Hille B (2001) Ion channels and excitable membranes, 3rd edn. Sinauer Associates, Sunderland. 814 p

    Google Scholar 

  • Hinke JAM (1959) Glass micro-electrodes for measuring intracellular activities of sodium and potassium. Nature 184:1257–1258

    CAS  PubMed  Google Scholar 

  • Hirsch RE, Lewis BD, Spalding EP, Sussman MR (1998) A role for the AKT1 potassium channel in plant nutrition. Science 280:918–921

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Hughes FM Jr, Cidlowski JA (1999) Potassium is a critical regulator of apoptotic enzymes in vitro and in vivo. Adv Enzym Regul 39:157–171

    CAS  Google Scholar 

  • 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 29:649–659

    CAS  PubMed  Google Scholar 

  • 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 435:1197–1202

    CAS  PubMed  Google Scholar 

  • Jennings DH (1976) The effects of sodium chloride on higher plants. Biol Rev 51:453–486

    CAS  Google Scholar 

  • Jiang Y, Lee A, Chen J, Cadene M, Chait BT, MacKinnon R (2002) The open pore conformation of potassium channels. Nature 417:523–526

    CAS  PubMed  Google Scholar 

  • 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) 1:161–171

    Google Scholar 

  • Katsuhara M, Kawasaki T (1996) Salt stress induced nuclear and DNA degradation in meristematic cells of barley roots. Plant Cell Physiol 37:169–173

    CAS  Google Scholar 

  • Köhler B (2007) Step by step: deciphering ion transport in the root xylem parenchyma. Plant Signal Behav 2:303–305

    PubMed  PubMed Central  Google Scholar 

  • 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 51:567–577

    CAS  PubMed  Google Scholar 

  • Kronzucker HJ, Britto DT (2011) Sodium transport in plants: a critical review. New Phytol 189:54–81

    CAS  PubMed  Google Scholar 

  • Kronzucker HJ, Coskun D, Schulze LM, Wong JR, Britto DT (2013) Sodium as nutrient and toxicant. Plant Soil 369:1–23

    CAS  Google Scholar 

  • L’Roy A, Hendrix DL (1980) Effect of salinity upon cell membrane potential in the marine halophyte, Salicornia bigelovii Torr. Plant Physiol 65:544–549

    PubMed  PubMed Central  Google Scholar 

  • 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 103:12625–12630

    CAS  PubMed  PubMed Central  Google Scholar 

  • Longpré JP, Lapointe JY (2011) Determination of the Na+/glucose cotransporter (SGLT1) turnover rate using the ion-trap technique. Biophys J 100:52–59

    PubMed  PubMed Central  Google Scholar 

  • 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 144:1786–1796

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 164:375–384

    PubMed  Google Scholar 

  • 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 374:661–676

    CAS  Google Scholar 

  • Maathuis FJM, Amtmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Ann Bot 84:123–133

    CAS  Google Scholar 

  • Maathuis FJ, Prins HB (1990) Patch clamp studies on root cell vacuoles of a salt-tolerant and a salt-sensitive Plantago species. Plant Physiol 92:23–28

    CAS  PubMed  Google Scholar 

  • Maathuis FJM, Sanders D (2001) Sodium uptake in Arabidopsis roots is regulated by cyclic nucleotides. Plant Physiol 127:1617–1625

    CAS  PubMed  Google Scholar 

  • 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 43:1219–1223

    CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • MacKinnon R (2004) Potassium channels and the atomic basis of selective ion conduction (Nobel Lecture). Angew Chem Int Ed Engl 43:4265–4277

    CAS  PubMed  Google Scholar 

  • Maffeo C, Bhattacharya S, Yoo J, Wells D, Aksimentiev A (2012) Modeling and simulation of ion channels. Chem Rev 112:6250–6284

    CAS  PubMed  Google Scholar 

  • Mähler J, Persson I (2012) A study of the hydration of the alkali metal ions in aqueous solution inorganic chemistry. Am Chem Soc 51:425–438

    Google Scholar 

  • Malone M, Leigh RA, Tomos AD (1991) Concentrations of vacuolar inorganic ions in individual cells of intact wheat leaf epidermis. J Exp Bot 42:305–309

    CAS  Google Scholar 

  • Martinoia E, Meyer S, De Angeli A, Nagy R (2012) Vacuolar transporters in their physiological context. Annu Rev Plant Biol 63:183–213

    CAS  PubMed  Google Scholar 

  • 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 126:1646–1667

    PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 297:71–84

    CAS  Google Scholar 

  • 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 88:259–268

    CAS  PubMed  Google Scholar 

  • Murthy M, Tester M (2006) Cation currents in protoplasts from the roots of a Na+ hyperaccumulating mutant of Capsicum annuum. J Exp Bot 57:1171–1180

    CAS  PubMed  Google Scholar 

  • Mutoh H, Akemann W, Knöpfel T (2012) Genetically engineered fluorescent voltage reporters. ACS Chem Neurosci 3:585–592

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 8:165–179

    CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Nightingale ER Jr (1959) Phenomenological theory of ion solvation. Effective radii of hydrated ions. Ions J Phys Chem 63:1381–1387

    CAS  Google Scholar 

  • 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 103:713–718

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nobel PS (2005) Physicochemical and environmental plant physiology, 3rd edn. Academic, Burlington. 540 p

    Google Scholar 

  • 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 424:283–294

    PubMed  Google Scholar 

  • 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 151:210–222

    CAS  PubMed  PubMed Central  Google Scholar 

  • Palmgren MG (2001) PLANT PLASMA MEMBRANE H+-ATPases: powerhouses for nutrient uptake. Annu Rev Plant Physiol Plant Mol Biol 52:817–845

    CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Parrondo RT, Gosselink JG, Hopkinson CS (1978) Effects of salinity and drainage on the growth of three salt marsh grasses. Bot Gaz 139:102–107

    CAS  Google Scholar 

  • Pitman MG, Läuchli A, Stelzer R (1981) Ion distribution in roots of barley seedlings measured by electron probe x-ray microanalysis. Plant Physiol 68:673–679

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 102:7493–7498

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qi Z, Spalding EP (2004) Protection of plasma membrane K+ transport by the salt overly sensitive Na+–H+ antiporter during salinity stress. Plant Physiol 136:2548–2555

    CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson MF, Véry A-A, Sanders D, Mansfield TA (1997) How can stomata contribute to salt tolerance? Ann Bot 80:387–393

    CAS  Google Scholar 

  • Rodriguez-Navarro A (2000) Potassium transport in fungi and plants. BBA Rev Biomembr 1469:1–30

    CAS  Google Scholar 

  • Rodríguez-Navarro A, Rubio F (2006) High-affinity potassium and sodium transport systems in plants. J Exp Bot 57:1149–1160

    PubMed  Google Scholar 

  • 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 402:56–64

    CAS  Google Scholar 

  • Sejersted OM, Sjøgaard G (2000) Dynamics and consequences of potassium shifts in skeletal muscle and heart during exercise. Physiol Rev 80:1411–1481

    CAS  PubMed  Google Scholar 

  • Serrano R (1988) Structure and function of proton translocating ATPase in plasma membranes of plants and fungi. Biochim Biophys Acta 947:1–28

    CAS  PubMed  Google Scholar 

  • Shabala S (2009) Salinity and programmed cell death: unravelling mechanisms for ion specific signalling. J Exp Bot 60:709–712

    CAS  PubMed  Google Scholar 

  • 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 129:290–299

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shabala S, Mackay A (2011) Ion transport in halophytes. Adv Bot Res 57:151–199

    CAS  Google Scholar 

  • 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 141:1653–1665

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 97:6896–6901

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 133:411–422

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 39:1–12

    CAS  Google Scholar 

  • Skou JC (1998) Nobel Lecture. The identification of the sodium pump. Biosci Rep 18:155–169

    CAS  PubMed  Google Scholar 

  • 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 83:35–42

    CAS  Google Scholar 

  • 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 125:604–614

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 129:1482–1493

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 52:967–980

    CAS  PubMed  Google Scholar 

  • Subbarao GV, Ito O, Berry WL, Wheeler RM (2003) Sodium – a functional plant nutrient. Crit Rev Plant Sci 22:391–416

    Google Scholar 

  • Sze H, Li X, Palmgren MG (1999) Energization of plant cell membranes by H+-pumping ATPases. Regulation and biosynthesis. Plant Cell 11:677–690

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thiyagarajah M, Fry SC, Yeo AR (1996) In vitro salt tolerance of cell wall enzymes from halophytes and glycophytes. J Exp Bot 47:1717–1724

    CAS  Google Scholar 

  • 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 14:509–521

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 48:342–353

    CAS  PubMed  Google Scholar 

  • 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 27:1–14

    CAS  Google Scholar 

  • 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 108:743–751

    CAS  PubMed  PubMed Central  Google Scholar 

  • Walker DJ, Black CR, Miller AJ (1998) The role of cytosolic potassium and pH in the growth of barley roots. Plant Physiol 118:957–964

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 235

    Google Scholar 

  • 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 57:1161–1170

    CAS  PubMed  Google Scholar 

  • Wang S-M, Zhang J-L, Flowers TJ (2007) Low-affinity Na+ uptake in the halophyte Suaeda maritima. Plant Physiol 145:559–571

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 14:7660–7680

    PubMed  PubMed Central  Google Scholar 

  • 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 115:1707–1719

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 203:506–516

    CAS  Google Scholar 

  • Wegner LH, Raschke K (1994) Ion channels in the xylem parenchyma of barley roots. Plant Physiol 105:799–813

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 46:497–511

    CAS  Google Scholar 

  • Wu SJ, Ding L, Zhu JK (1996) SOS1, a genetic locus essential for salt tolerance and potassium acquisition. Plant Cell 8:617–627

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 528–562

    Google Scholar 

  • 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 125:1347–1360

    CAS  PubMed  Google Scholar 

  • Yamaguchi T, Hamamoto S, Uozumi N (2013) Sodium transport system in plant cells. Front Plant Sci 4:410

    PubMed  PubMed Central  Google Scholar 

  • Yeo AR (1981) Salt tolerance in the halophyte Suaeda maritima (L.) Dum.: intracellular compartmentation of ions. J Exp Bot 32:487–497

    CAS  Google Scholar 

  • 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 31:1171–1183

    CAS  Google Scholar 

  • 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 37:143–159

    Google Scholar 

  • 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 115:495–507

    CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 87:153–160

    Google Scholar 

  • 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 131:122–130

    CAS  PubMed  Google Scholar 

  • 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 47:311–318

    CAS  Google Scholar 

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Authors and Affiliations

  1. Faculty of Life Sciences and Computing, London Metropolitan University, London, UK

    Vadim Volkov

  2. Department of Plant Sciences, College of Agricultural and Environmental Sciences, University of California, Davis, CA, USA

    Vadim Volkov

  3. School of Life Sciences, University of Sussex, Brighton, UK

    Timothy J. Flowers

  4. School of Plant Biology, The University of Western Australia, Crawley, WA, Australia

    Timothy J. Flowers

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  1. Vadim Volkov
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  2. Timothy J. Flowers
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Editors and Affiliations

  1. Institute of Sustainable Halophyte Utilization (ISHU), University of Karachi, Karachi, Pakistan

    Bilquees Gul

  2. UNESCO Bangkok Asia and Pacific Regional Bureau for Education, Bangkok, Thailand

    Benno Böer

  3. Institute of Sustainable Halophyte Utilization (ISHU), University of Karachi, Karachi, Pakistan

    M. Ajmal Khan

  4. UNESCO Division of Ecological and Earth Sciences, Man and the Biosphere (MAB) Programme, Paris cedex 15, France

    Miguel Clüsener-Godt

  5. Institute of Sustainable Halophyte Utilization (ISHU), University of Karachi, Karachi, Pakistan

    Abdul Hameed

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Volkov, V., Flowers, T.J. (2019). Mechanisms of Ion Transport in Halophytes: From Roots to Leaves. In: Gul, B., Böer, B., Khan, M., Clüsener-Godt, M., Hameed, A. (eds) Sabkha Ecosystems. Tasks for Vegetation Science, vol 49. Springer, Cham. https://doi.org/10.1007/978-3-030-04417-6_10

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