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The Role of Ion Channels in Plant Salt Tolerance

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Ion Channels and Plant Stress Responses

Part of the book series: Signaling and Communication in Plants ((SIGCOMM))

Abstract

Salinisation of agricultural land threatens world food production because it exposes crops to low water potential and high concentration of toxic ions in the soil. In particular, all major crops are sensitive to high concentrations of sodium (Na+). Due to the negative electrical potential inside cells Na+ influx into plant roots can occur through ion channels or other membrane transport proteins that facilitate passive diffusion of Na+ across the plasma membrane. In this chapter, we discuss the contribution of different types of ion channels to Na+ influx. In the first part of the chapter, we recapitulate the basic properties of different types of plant ion channels such as voltage-dependence of gating and relative selectivity for Na+ and potassium and build a simple model to assess how these channels contribute to whole-cell ionic current and Na+ uptake. In the second part of the chapter, we describe a number of experimental studies that have investigated Na+ flux and ion channel currents in different plant species. The combined evidence suggests that salt tolerance in plants is based on the restriction of Na+ influx through voltage-independent ion channels.

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Abbreviations

VIC:

Voltage-independent channel

IRC:

Inward-rectifying channel

ORC:

Outward-rectifying channel

GHK:

Goldman-Hodgkin-Katz

I–V :

Current–Voltage

P K:P Na :

Relative Na+/K+ permeability

CNGC:

Cyclic nucleotide gated channel

References

  • Aleman F, Nieves-Cordones M, Martinez V, Rubio F (2009a) Differential regulation of the HAK5 genes encoding the high-affinity K+ transporters of Thellungiella halophila and Arabidopsis thaliana. Environ Exp Bot 65:263–269

    Article  CAS  Google Scholar 

  • Aleman F, Nieves-Cordones M, Martinez V, Rubio F (2009b) Potassium/sodium steady-state homeostasis in Thellungiella halophila and Arabidopsis thaliana under long-term salinity conditions. Plant Sci 176:768–774

    Article  CAS  Google Scholar 

  • Al Khazaaly S, Walker NA, Beilby MJ, Shepherd VA (2009) Membrane potential fluctuations in Chara australis: a characteristic signature of high external sodium. Eur Biophys J 39:167–174

    Article  PubMed  Google Scholar 

  • Al Khazaaly S, Beilby MJ (2007) Modeling ion transporters at the time of hypertonic regulation in Lamprothamnium succinctum. Charophytes 1:28–47

    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

    Article  CAS  PubMed  Google Scholar 

  • Amtmann A, Armengaud P, Volkov V (2004) Potassium nutrition and salt stress. In: Blatt MR (ed) Membrane transport in plants. Blackwell, Oxford, pp 293–339

    Google Scholar 

  • Amtmann A, Blatt MR (2009) Regulation of macronutrient transport. New Phytol 181:35–52

    Article  CAS  PubMed  Google Scholar 

  • Amtmann A, Bohnert HJ, Bressan RA (2005) Abiotic stress and plant genome evolution. Search for new models. Plant Physiol 138:127–130

    Article  CAS  PubMed  Google Scholar 

  • Amtmann A, Laurie S, Leigh R, Sanders D (1997) Multiple inward channels provide flexibility in Na+/K+ discrimination at the plasma membrane of barley suspension culture cells. J Exp Bot 48:481–497

    CAS  Google Scholar 

  • Amtmann A, Sanders D (1999) Mechanisms of Na+ uptake by plant cells. Adv Bot Res l 29:75–112

    Article  CAS  Google Scholar 

  • Anil VS, Krishnamurthy H, Mathew MK (2007) Limiting cytosolic Na+ confers salt tolerance to rice cells in culture: a two-photon microscopy study of SBFI-loaded cells. Physiol Plant 129:607–621

    Article  CAS  Google Scholar 

  • Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256–1258

    Article  CAS  PubMed  Google Scholar 

  • Beilby MJ (1989) Electrophysiology of giant algal cells. Meth Enzymol 174:403–443

    Article  CAS  Google Scholar 

  • Beilby MJ (1990) Current voltage curves for plant membrane studies – a critical analysis of the method. J Exp Bot 41:165–182

    Article  Google Scholar 

  • Beilby MJ, Shepherd VA (2001) Modeling the current–voltage characteristics of charophyte membranes. II. The effect of salinity on membranes of Lamprothamnium papulosum. J Membrane Biol 181:77–89

    CAS  Google Scholar 

  • Beilby MJ, Shepherd VA (2006) The electrophysiology of salt tolerance in charophytes. Cryptogamie Algologie 27:403–417

    Google Scholar 

  • Beilby MJ, Al Khazaaly S (2009) The role of H+/OH− channels in salt stress response of Chara australis. J Membrane Biol 230:21–34

    Article  CAS  Google Scholar 

  • Binzel ML, Hasegawa PM, Handa AK, Bressan RA (1985) Adaptation of tobacco cells to NaCl. Plant Physiol 79:118–125

    Article  CAS  PubMed  Google Scholar 

  • Bisson MA, Kirst GO (1980) Lamprothamnium, a euryhaline charophyte. 2. Time Course of Turgor Regulation. J Exp Bot 31:1237–1244

    Article  Google Scholar 

  • Blatt MR, Gradmann D (1997) K+-sensitive gating of the K+ outward rectifier in Vicia guard cells. J Membrane Biol 158:241–256

    Article  CAS  Google Scholar 

  • Britto DT, Kronzucker HJ (2006) Futile cycling at the plasma membrane: a hallmark of low-affinity nutrient transport. Trends Plant Sci 11:529–534

    Article  CAS  PubMed  Google Scholar 

  • Byrt CS, Platten JD, Spielmeyer W, James RA, Lagudah ES, Dennis ES, Tester M, Munns R (2007) HKT1;5-like cation transporters linked to Na+ exclusion loci in wheat, Nax2 and Kna1. Plant Physiol 143:1918–1928

    Article  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

    Article  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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Davenport RJ, Tester M (2000) A weakly voltage-dependent, nonselective cation channel mediates toxic sodium influx in wheat. Plant Physiol 122:823–834

    Article  CAS  PubMed  Google Scholar 

  • Demidchik V, Davenport RJ, Tester M (2002) Nonselective cation channels in plants. Ann Rev Plant Biol 53:67–107

    Article  CAS  Google Scholar 

  • Demidchik V, Essah PA, Tester M (2004) Glutamate activates cation currents in the plasma membrane of Arabidopsis root cells. Planta 219:167–175

    Article  CAS  PubMed  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

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Dreyer I, MullerRober B, Kohler B (2004) Voltage-gated ion channels. In: Blatt MR (ed) Membrane transport in plants. Blackwell, Oxford, pp 150–192

    Google Scholar 

  • Edgell HS (2003) Upper devonian charophyta of Western Australia. Micropaleontology 49:359–374

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Felle HH, Zimmermann MR (2007) Systemic signalling in barley through action potentials. Planta 226:203–214

    Article  CAS  PubMed  Google Scholar 

  • Flowers TJ, Hajibagheri MA (2001) Salinity tolerance in Hordeum vulgare: ion concentrations in root cells of cultivars differing in salt tolerance. Plant Soil 231:1–9

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Hall D, Evans AR, Newbury HJ, Pritchard J (2006) Functional analysis of CHX21: a putative sodium transporter in Arabidopsis. J Exp Bot 57:1201–1210

    Article  CAS  PubMed  Google Scholar 

  • Hille B (2001) Ion channel of excitable membranes, 3rd edn. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Horie T, Yoshida K, Nakayama H, Yamada K, Oiki S, Shinmyo A (2001) Two types of HKT transporters with different properties of Na+ and K+ transport in Oryza sativa. Plant J 27:129–138

    Article  CAS  PubMed  Google Scholar 

  • Huang SB, Spielmeyer W, Lagudah ES, James RA, Platten JD, Dennis ES, Munns R (2006) A sodium transporter (HKT7) is a candidate for Nax1, a gene for salt tolerance in durum wheat. Plant Physiol 142:1718–1727

    Article  CAS  PubMed  Google Scholar 

  • Inan G, Zhang Q, Li PH, Wang ZL, Cao ZY, Zhang H, Zhang CQ, Quist TM, Goodwin SM, Zhu JH, Shi HH, Damsz B, Charbaji T, Gong QQ, Ma SS, Fredricksen M, Galbraith DW, Jenks MA, Rhodes D, Hasegawa PM, Bohnert HJ, Joly RJ, Bressan RA, Zhu JK (2004) Salt cress. A halophyte and cryophyte Arabidopsis relative model system and its applicability to molecular genetic analyses of growth and development of extremophiles. Plant Physiol 135:1718–1737

    Article  CAS  PubMed  Google Scholar 

  • James RA, Davenport RJ, Munns R (2006) Physiological characterization of two genes for Na+ exclusion in durum wheat, Nax1 and Nax2. Plant Physiol 142:1537–1547

    Article  CAS  PubMed  Google Scholar 

  • Kader MA, Lindberg S (2005) Uptake of sodium in protoplasts of salt-sensitive and salt-tolerant cultivars of rice. Oryza sativa L. determined by the fluorescent dye SBFI. J Exp Bot 56:3149–3158

    Article  CAS  PubMed  Google Scholar 

  • Karol KG, McCourt RM, Cimino MT, Delwiche CF (2001) The closest living relatives of land plants. Science 294:2351–2353

    Article  CAS  PubMed  Google Scholar 

  • Kelman R, Feist M, Trewin NH, Hass H (2004) Charophyte algae from the Rhynie chert. Transactions Roy Soc Edinburgh: Earth Sciences 94:445–455

    Google Scholar 

  • Kronzucker HJ, Szczerba MW, Moazami-Goudarzi M, Britto DT (2006) The cytosolic Na+: K+ ratio does not explain salinity-induced growth impairment in barley: a dual-tracer study using 42K+ and 24Na+. Plant Cell Environ 29:2228–2237

    Article  CAS  PubMed  Google Scholar 

  • Kronzucker HJ, Szczerba MW, Schulze LM, Britto DT (2008) Non-reciprocal interactions between K+ and Na+ ions in barley (Hordeum vulgare L.). J Exp Bot 59:2793–2801

    Article  CAS  PubMed  Google Scholar 

  • Leng Q, Mercier RW, Hua BG, Fromm H, Berkowitz GA (2002) Electrophysiological analysis of cloned cyclic nucleotide-gated ion channels. Plant Physiol 128:400–410

    Article  CAS  PubMed  Google Scholar 

  • Leng Q, Mercier RW, Yao W, Berkowitz GA (1999) Cloning and first functional characterization of a plant cyclic nucleotide-gated cation channel. Plant Physiol 121:753–761

    Article  CAS  PubMed  Google Scholar 

  • Liu W, Fairbairn DJ, Reid RJ, Schachtman DP (2001) Characterization of two HKT1 homologues from Eucalyptus camaldulensis that display intrinsic osmosensing capability. Plant Physiol 127:283–294

    Article  CAS  PubMed  Google Scholar 

  • Maathuis FJ, Ichida AM, Sanders D, Schroeder JI (1997) Roles of higher plant K+ channels. Plant Physiol 114:1141–1149

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Malagoli P, Britto DT, Schulze LM, Kronzucker HJ (2008) Futile Na+ cycling at the root plasma membrane in rice (Oryza sativa L.): kinetics, energetics, and relationship to salinity tolerance. J Exp Bot 59:4109–4117

    Article  CAS  PubMed  Google Scholar 

  • McCourt RM, Delwiche CF, Karol KG (2004) Charophyte algae and land plant origins. Trends Ecol Evol 19:661–666

    Article  PubMed  Google Scholar 

  • Miedema H, Demidchik V, Very AA, Bothwell JHF, Brownlee C, Davies JM (2008) Two voltage-dependent calcium channels co-exist in the apical plasma membrane of Arabidopsis thaliana root hairs. New Phytol 179:378–385

    Article  CAS  PubMed  Google Scholar 

  • Moller IS, Tester M (2007) Salinity tolerance of Arabidopsis: a good model for cereals? Trends Plant Sci 12:534–540

    Article  PubMed  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Biol 59:651–681

    Article  CAS  Google Scholar 

  • Oertli JJ (1968) Extracellular salt accumulation, a possible mechanism of salt injury in plants. Agrochim 12:461–469

    Google Scholar 

  • Oh DH, Gong QQ, Ulanov A, Zhang Q, Li YZ, Ma WY, Yun DJ, Bressan RA, Bohnert HJ (2007) Sodium stress in the halophyte Thellungiella halophila and transcriptional changes in a thsos1-RNA interference line. J Integr Plant Biol 49:1484–1496

    Article  CAS  Google Scholar 

  • Ohta M, Hayashi Y, Nakashima A, Hamada A, Tanaka A, Nakamura T, Hayakawa T (2002) Introduction of a Na+/H+ antiporter gene from Atriplex gmelini confers salt tolerance to rice. FEBS Lett 532:279–282

    Article  CAS  PubMed  Google Scholar 

  • Qi Z, Spalding EP (2004) Protection of plasma membrane K+ transport by the salt overly sensitive1 Na+-H+ antiporter during salinity stress. Plant Physiol 136:2548–2555

    Article  CAS  PubMed  Google Scholar 

  • Raven JA (1991) Terrestrial rhizophytes and H+ currents circulating over at least a millimeter – an obligate relationship. New Phytol 117:177–185

    Article  Google Scholar 

  • Roberts SK, Tester M (1997) A patch clamp study of Na+ transport in maize roots. J Exp Bot 48:431–440

    Article  CAS  Google Scholar 

  • Rubio F, Gassmann W, Schroeder JI (1995) Sodium-driven potassium uptake by the plant potassium transporter Hkt1 and mutations conferring salt tolerance. Science 270:1660–1663

    Article  CAS  PubMed  Google Scholar 

  • Rus A, Lee BH, Munoz-Mayor A, Sharkhuu A, Miura K, Zhu JK, Bressan RA, Hasegawa PM (2004) AtHKT1 facilitates Na+ homeostasis and K+ nutrition in planta. Plant Physiol 136:2500–2511

    Article  CAS  PubMed  Google Scholar 

  • Serrano R, Mulet JM, Rios G, Marquez JA, de Larrinoa IF, Leube MP, Mendizabal I, Pascual-Ahuir A, Proft M, Ros R, Montesinos C (1999) A glimpse of the mechanisms of ion homeostasis during salt stress. J Exp Bot 50:1023–1036

    Article  CAS  Google Scholar 

  • Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ, Miller AJ, Davies JM, Newman IA (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

    Article  CAS  PubMed  Google Scholar 

  • Shepherd VA, Beilby MJ, Al Khazaaly SAS, Shimmen T (2008) Mechano-perception in Chara cells: the influence of salinity and calcium on touch-activated receptor potentials, action potentials and ion transport. Plant Cell Environ 31:1575–1591

    Article  CAS  PubMed  Google Scholar 

  • Shepherd VA, Beilby MJ, Heslop DJ (1999) Ecophysiology of the hypotonic response in the salt-tolerant charophyte alga Lamprothamnium papulosum. Plant Cell Environ 22:333–346

    Article  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 97:6896–6901

    Article  CAS  PubMed  Google Scholar 

  • Shi H, Quintero FJ, Pardo JM, Zhu JK (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14:465–477

    Article  CAS  PubMed  Google Scholar 

  • Talke IN, Blaudez D, Maathuis FJ, Sanders D (2003) CNGCs: prime targets of plant cyclic nucleotide signalling? Trends Plant Sci 8:286–293

    Article  CAS  PubMed  Google Scholar 

  • Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527

    Article  CAS  PubMed  Google Scholar 

  • Thiel G, Blatt MR (1991) The mechanism of ion permeation through K+-channels of stomatal guard cells – voltage-dependent block by Na+. J Plant Physiol 138:326–334

    CAS  Google Scholar 

  • Tyerman SD, Beilby M, Whittington J, Juswono U, Newman I, Shabala S (2001) Oscillations in proton transport revealed from simultaneous measurements of net current and net proton fluxes from isolated root protoplasts: MIFE meets patch-clamp. Aust J Plant Physiol 28:591–604

    CAS  Google Scholar 

  • Tyerman SD, Skerrett M, Garrill A, Findlay GP, Leigh RA (1997) Pathways for the permeation of Na+ and Cl− into protoplasts derived from the cortex of wheat roots. J Exp Bot 48:459–480

    CAS  Google Scholar 

  • Uozumi N, Kim EJ, Rubio F, Yamaguchi T, Muto S, Tsuboi A, Bakker EP, Nakamura T, Schroeder JI (2000) The Arabidopsis HKT1 gene homolog mediates inward Na+ currents in xenopus laevis oocytes and Na+ uptake in Saccharomyces cerevisiae. Plant Physiol 122:1249–1259

    Article  CAS  PubMed  Google Scholar 

  • Véry AA, Sentenac H (2003) Molecular mechanisms and regulation of K+ transport in higher plants. Ann Rev Plant Biol 54:575–603

    Article  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

    Article  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 Env 27:1–14

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Wang CM, Zhang JL, Liu XS, Li Z, Wu GQ, Cai JY, Flowers TJ, Wang SM (2009) Puccinellia tenuiflora maintains a low Na+ level under salinity by limiting unidirectional Na+ influx resulting in a high selectivity for K+ over Na+. Plant Cell Environ 32:486–496

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • White PJ, Lemitiri-Clieh F (1995) Potassium current across the plasma membrane of protoplast derived from rye roots: a patch clamp study. J Exp Bot 46:497–511

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Wyn Jones RJ, Pollard A (1983) Proteins, enzymes and inorganic ions. In: Lauchli A, Pirson A (eds) Encyclopedia of Plant Physiology. Springer, Berlin, pp 528–562

    Google Scholar 

  • Yadav R, Flowers TJ, Yeo AR (1996) The involvement of the transpirational bypass flow in sodium uptake by high- and low-sodium-transporting lines of rice developed through intravarietal selection. Plant Cell Environ 19:329–336

    Article  CAS  Google Scholar 

  • Zhang HX, Hodson JN, Williams JP, Blumwald E (2001) Engineering salt-tolerant Brassica plants: characterization of yield and seed oil quality in transgenic plants with increased vacuolar sodium accumulation. Proc Natl Acad Sci USA 98:12832–12836

    Article  CAS  PubMed  Google Scholar 

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Amtmann, A., Beilby, M.J. (2010). The Role of Ion Channels in Plant Salt Tolerance. In: Demidchik, V., Maathuis, F. (eds) Ion Channels and Plant Stress Responses. Signaling and Communication in Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-10494-7_2

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