Skip to main content

Advertisement

SpringerLink
Log in

Mechanisms of sodium uptake by roots of higher plants

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

The negative impact of soil salinity on agricultural yields is significant. For agricultural plants, sensitivity to salinity is commonly (but not exclusively) due to the abundance of Na+ in the soil as excess Na+ is toxic to plants. We consider reducing Na+ uptake to be the key, as well as the most efficient approach, to control Na+ accumulation in crop plants and hence to improve their salt resistance. Understanding the mechanism of Na+ uptake by the roots of higher plants is crucial for manipulating salt resistance. Hence, the aim of this review is to highlight and discuss recent advances in our understanding of the mechanisms of Na+ uptake by plant roots at both physiological and molecular levels. We conclude that continued efforts to investigate the mechanisms of root Na+ uptake in higher plants are necessary, especially that of low-affinity Na+ uptake, as it is the means by which sodium enters into plants growing in saline soils.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

AKT:

Arabidopsis K+ transporter

CCC:

cation-Cl− cotransporter

CNGC:

cyclic-nucleotide-gated channel

HAK:

high-affinity K+ transporter

HKT:

high-affinity K+ transporter

KT:

K+ transporter

KUP:

K+ uptake transporter

LCT:

low-affinity cation transporter

NSCC:

non-selective cation channel

SOS:

salt overly sensitive

VIC:

voltage-independent channel

References

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

    CAS  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, Fischer M, Marsh EL, Stefanovic A, Sanders D, Schachtman DP (2001) The wheat cDNA LCT1 generates hypersensitivity to sodium in a salt-sensitive yeast strain. Plant Physiol 126:1061–1071

    CAS  PubMed  Google Scholar 

  • Anderson JA, Huprikar SS, Kochian LV, Lucas WJ, Gaber RF (1992) Functional expression of a probable Arabidopsis thaliana potassium channel in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 89:3736–3740

    CAS  PubMed  Google Scholar 

  • Antosiewicz DM, Hennig J (2004) Overexpression of LCT1 in tobacco enhances the protective action of calcium against cadmium toxicity. Environ Pollut 129:237–245

    CAS  PubMed  Google Scholar 

  • Apse MP, Blumwald E (2007) Na+ transport in plants. FEBS Lett 581:2247–2254

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Apse MP, Sottosanto JB, Blumwald E (2003) Vacuolar cation/H+ exchange, ion homeostasis, and leaf development are altered in a T-DNA insertional mutant of AtNHX1, the Arabidopsis vacuolar Na+/H+ antiporter. Plant J 36:229–239

    CAS  PubMed  Google Scholar 

  • Bao AK, Wang SM, Wu GQ, Xi JJ, Zhang JL, Wang CM (2008) Overexpression of the Arabidopsis H+-PPase enhanced the salt and drought tolerance in transgenic alfalfa (Medicago sativa L.). Plant Sci 176:232–240

    Google Scholar 

  • Barkla BJ, Zingarelli L, Blumwald E, Smith JAC (1995) Tonoplast Na+/H+ antiport activity and its energization by the vacuolar H+-ATPase in the halophytic plant Mesembryanthemum crystallinum L. Plant Physiol 109:549–556

    CAS  PubMed  Google Scholar 

  • Berthomieu P, Conejero G, Nublat A, Brackenbury WJ, Lambert C, Savio C, Uozumi N, Oiki S, Yamada K, Cellier F, Gosti F, Simonneau T, Essah PA, Tester M, Very AA, Sentenac H, Casse F (2003) Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance. Embo J 22:2004–2014

    CAS  PubMed  Google Scholar 

  • Bertorello AM, Zhu JK (2009) SIK1/SOS2 networks: decoding sodium signals via calcium-responsive protein kinase pathways. Pflugers Arch-Eur J Physiol . doi:10.1007/s00424-00009-00646-00422

    Google Scholar 

  • Binzel M, Hess FD, Bressan RA, Hasega PM (1988) Intracellular compartmentation of ion in salt adapted tobacco cells. Plant Physiol 86:607–614

    CAS  PubMed  Google Scholar 

  • Blumwald E (2003) Engineering salt tolerance in plants. In Biotechnology & Genetic Engineering Reviews, Vol 20, pp 261–275. INTERCEPT LTD SCIENTIFIC TECHNICAL & MEDICAL PUBLISHERS, Andover

  • Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. Biochim Biophys Acta-Biomembr 1465:140–151

    CAS  Google Scholar 

  • Bolat I, Kaya C, Almaca A, Timucin S (2006) Calcium sulfate improves salinity tolerance in rootstocks of plum. J Plant Nutr 29:553–564

    CAS  Google Scholar 

  • Box S, Schachtman DP (2000) The effect of low concentrations of sodium on potassium uptake and growth of wheat. Aust J Plant Physiol 27:175–182

    CAS  Google Scholar 

  • Bressan RA, Hasegawa PM (1998) Plants use Calcium to resolve salt stress. Trends Plant Sci 3:411–412

    Google Scholar 

  • Britto DT, Kronzucker HJ (2008) Cellular mechanisms of potassium transport in plants. Physiol Plant 133:637–350

    CAS  PubMed  Google Scholar 

  • Buschmann PH, Vaidyanathan R, Gassmann W, Schroeder JI (2000) Enhancement of Na+ uptake currents, time-dependent inward-rectifying K+ channel currents, and K+ channel transcripts by K+ starvation in wheat root cells. Plant Physiol 122:1387–1397

    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

    CAS  PubMed  Google Scholar 

  • Callahan MJ, Korn SJ (1994) Permeation of Na+ through a delayed rectifier K+ channel in chick dorsal root ganglion neurons. J Gen Physiol 104:747–771

    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  Google Scholar 

  • Chan CWM, Schorrak LM, Smith RK Jr, Bent AF, Sussman MR (2003) A cyclic nucleotide-gated ion channel, CNGC2, is crucial for plant development and adaptation to calcium stress. Plant Physiol 132:728–731

    CAS  PubMed  Google Scholar 

  • Cheeseman JM (1982) Pump leak sodium fluxes in low salt corn Zea mays roots. J Membr Biol 70:157–164

    CAS  Google Scholar 

  • Cheeseman JM (1988) Mechanisms of salinity tolerance in plants. Plant Physiol 87:547–550

    CAS  PubMed  Google Scholar 

  • Chen HX, Li PM, Gao HY (2007) Alleviation of photoinhibition by calcium supplement in salt-treated Rumex leaves. Physiol Plant 129:386–396

    CAS  Google Scholar 

  • Clemens S, Antosiewicz DM, Ward JM, Schachtman DP, Schroeder JI (1998) The plant cDNA LCT1 mediates the uptake of calcium and cadmium in yeast. Proc Natl Acad Sci USA 95:12043–12048

    CAS  PubMed  Google Scholar 

  • Clough SJ, Fengler KA, Yu IC, Lippok B, Smith RK, Bent AF (2000) The Arabidopisis dnd1 “defense, no death” gene encodes a mutated cyclic nucleotide-gated ion channel. Proc Natl Acad Sci USA 97:9323–9328

    CAS  PubMed  Google Scholar 

  • Colmenero-Flores JM, Martinez G, Gamba G, Vazquez N, Iglesias DJ, Brumos J, Talon M (2007) Identification and functional characterization of cation-chloride cotransporters in plants. Plant J 50:278–292

    CAS  PubMed  Google Scholar 

  • Colmer TD, Fan TWM, Higashi RM, Lauchli A (1994) Interactions of Ca2+ and NaCl stress on the ion relations and intracellular pH of Sorghum bicolor root tips: An in vivo P-31-NMR study. J Exp Bot 45:1037–1044

    CAS  Google Scholar 

  • Colmer TD, Flowers TJ, Munns R (2006) Use of wild relatives to improve salt tolerance in wheat. J Exp Bot 57:1059–1078

    CAS  PubMed  Google Scholar 

  • Cramer GR (2002) Sodium-calcium interactions under salinity stress. In: Läuchli A, Lüttge U (eds) Salinity: environment - plants–molecules. Kluwer Academic Publishers, The Netherlands, pp 205–227

    Google Scholar 

  • Cramer GRL, Lauchli A, Polito VS (1985) Displacement of Ca2+ by Na+ from the plasmalemma of root cells. A primary response to salt stress. Plant Physiol 79:207–211

    CAS  PubMed  Google Scholar 

  • Cramer GR, Lynch J, Lauchli A, Epstein E (1987) Influx of Na+, K+, and Ca2+ into roots of salt-stressed cotton seedlings. Plant Physiol 83:510–516

    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

    CAS  PubMed  Google Scholar 

  • Davenport R, Reid RJ, Smith FA (1996) Control of sodium influx by calcium and turgor in two charophytes differing in salinity tolerance. Plant Cell Environ 19:721–728

    CAS  Google Scholar 

  • Davenport RJ, Munoz-Mayor A, Jha D, Essah PA, Rus A, Tester M (2007) The Na+ transporter AtHKT1;1 controls retrieval of Na+ from the xylem in Arabidopsis. Plant Cell Environ 30:497–507

    CAS  PubMed  Google Scholar 

  • Deal KR, Goyal S, Dvorak J (1999) Arm location of Lophopyrum elongatum genes affecting K+/Na+ selectivity under salt stress. Euphytica 108:193–198

    CAS  Google Scholar 

  • Delpire E, Rauchman M, Beier D, Hebert S, Gullans S (1994) Molecular cloning and chromosome localization of a putative basolateral Na+-K+-2Cl− cotransporter from mouse inner medullary collecting duct (mIMCD-3) cells. J Biol Chem 269:25677–25683

    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 379–387

  • Dubcovsky J, María GS, Epstein E, Luo MC, Dvorák J (1996) Mapping of the K+/Na+ discrimination locus Kna1 in wheat. 92, 448–454

  • Dvořák J, Gorham J (1992) Methodology of gene transfer by homoeologous recombination into Triticum turgidum: transfer of K+/Na+ discrimination from Triticum aestivum. Genome 35:639–646

    Google Scholar 

  • Elumalai RP, Nagpal P, Reed JW (2002) A mutation in the arabidopsis KT2/KUP2 potassium transporter gene affects shoot cell expansion. Plant Cell 14:119–131

    CAS  PubMed  Google Scholar 

  • Epstein E (1998) How calcium enhances plant salt tolerance. Science 280:1906–1907

    CAS  PubMed  Google Scholar 

  • Essah PA (2002) Sodium transport and accumulation in Arabidopsis thaliana. PhD thesis. Cambridge University, Cambridge, UK

  • Fairbairn DJ, Liu WH, Schachtman DP, Gomez-Gallego S, Day SR, Teasdale RD (2000) Characterisation of two distinct HKT1-like potassium transporters from Eucalyptus camaldulensis. Plant Mol Biol 43:515–525

    CAS  PubMed  Google Scholar 

  • Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319

    CAS  PubMed  Google Scholar 

  • Flowers TJ, Lauchli A (1983) Sodium versus potassium: substitution and compartmentation. Encycl Plant Physiol 15:651–681

    Google Scholar 

  • Flowers TJ, Yeo AR (1988) Ion relation of salt tolerance. In: Baker DA, Hall JL (eds) Solute transport in plant cells and tissues. Longman Scientific and Technical, Harlow, pp 392–413

    Google Scholar 

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

    CAS  PubMed  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 

  • Fu HH, Luan S (1998) AtKUP1: a dual-affinity K+ transporter from arabidopsis. Plant Cell 10:63–73

    CAS  PubMed  Google Scholar 

  • Gamba G (2005) Molecular physiology and pathophysiology of electroneutral cation-chloride cotransporters. Physiol Rev 85:423–493

    CAS  PubMed  Google Scholar 

  • Garcia A, Rizzo CA, UdDin J, Bartos SL, Senadhira D, Flowers TJ, Yeo AR (1997) Sodium and potassium transport to the xylem are inherited independently in rice, and the mechanism of sodium: potassium selectivity differs between rice and wheat. Plant Cell Environ 20:1167–1174

    CAS  Google Scholar 

  • Garciadeblas B, Benito B, Rodrıguez-Navarro A (2002) Molecular cloning and functional expression in bacteria of the potassium transporters CnHAK1 and CnHAK2 of the seagrass Cymodocea nodosa. Plant Mol Biol 50:623–633

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Gassmann W, Rubio F, Schroeder JI (1996) Alkali cation selectivity of the wheat root high-affinity potassium transporter HKT1. Plant J 10:869–882

    CAS  Google Scholar 

  • Gaxiola RA, Li JS, Undurraga S, Dang LM, Allen GJ, Alper SL, Fink GR (2001) Drought- and salt-tolerant plants result from overexpression of the AVP1 H+-pump. Proc Natl Acad Sci USA 98:11444–11449

    CAS  PubMed  Google Scholar 

  • Genc Y, Mcdonald GK, Tester M (2007) Reassessment of tissue Na+ concentration as a criterion for salinity tolerance in bread wheat. Plant Cell Environ 30:1468–1498

    Google Scholar 

  • Gierth M, Ma¨ser P, Schroeder JI (2005) The potassium transporter AtHAK5 functions in K+ deprivation-induced high-affinity K+ uptake and AKT1 K+ channel contribution to K+ uptake kinetics in arabidopsis roots. Plant Physiol 137:1105–1114

    CAS  PubMed  Google Scholar 

  • Gobert A, Park G, Amtmann A, Sanders D, Maathuis FJM (2006) Arabidopsis thaliana Cyclic Nucleotide Gated Channel 3 forms a non-selective ion transporter involved in germination and cation transport. J Exp Bot 57:791–800

    CAS  PubMed  Google Scholar 

  • Golldack D, Quigley F, Michalowski CB, Kamasani UR, Bohnert HJ (2003) Salinity stress-tolerant and -sensitive rice (Oryza sativa L.) regulate AKT1-type potassium channel transcripts differently. Plant Mol Biol 51:71–81

    CAS  PubMed  Google Scholar 

  • Gorham J (1990a) Salt tolerance in the Triticeae: ion discrimination in rye and Triticale. J Exp Bot 41:609–614

    CAS  Google Scholar 

  • Gorham J (1990b) Salt tolerance in the Triticeae: K/Na discrimination in Aegilops species. J Exp Bot 41:615–621

    CAS  Google Scholar 

  • Gorham J (1990c) Salt tolerance in the Triticeae: K/Na discrimination in synthetic hexaploid wheats. J Exp Bot 41:623–627

    CAS  Google Scholar 

  • Gorham J (1994) Salt tolerance in the Triticeae:K/Na discrimination in some perennial wheatgrasses and their amphiploids with wheat. J Exp Bot 45:441–447

    CAS  Google Scholar 

  • Gorham J, Bristol A, Young EM, Wyn Jones RG, Kashour G (1990) Salt tolerance in the Triticeae: K/Na discrimination in barley. J Exp Bot 41:1095–1101

    CAS  Google Scholar 

  • Gorham J, Bristol A, Young EM, Wyn Jones RG (1991) The presence of the enhanced K/Na discrimination trait in diploid Triticum species. Theor Appl Genet 82:729–736

    Google Scholar 

  • Gorham J, Bridges J, Dubcovsky J, Dvorak J, Hollington PA, Luo MC, Khan JA (1997) Genetic analysis and physiology of a trait for enhanced K+/Na+ discrimination in wheat. New Phytol 137:109–116

    CAS  Google Scholar 

  • Grover A (1999) A novel approach for raising salt tolerant transgenic plants based on altering stress signalling through Ca2+/calmodulin- dependent protein phosphatase calcineurin. Curr Sci 76:136–137

    CAS  Google Scholar 

  • Haas M (1994) The Na-K-Cl cotransporters. Am J Physiol 267:C869–C885

    CAS  PubMed  Google Scholar 

  • Haas M, Forbush B (1998) The Na-K-Cl cotransporters. J Bioenerg Biomembrane 30:161–172

    CAS  PubMed  Google Scholar 

  • Hajibagheri MA, Harvey DMR, Flowers TJ (1987) Quantitative ion distribution within root cells of salt-sensitive and salt-tolerant maize varieties. New Phytol 105:367–379

    CAS  Google Scholar 

  • Halfter U, Ishitani M, Zhu JK (2000) The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc Natl Acad Sci USA 97:3735–3740

    CAS  PubMed  Google Scholar 

  • Haro R, Banuelos MA, Senn MAE, Barrero-Gil J, Rodriguez-Navarro A (2005) HKT1 mediates sodium uniport in roots. Pitfalls in the expression of HKT1 in yeast. Plant Physiol 139:1495–1506

    CAS  PubMed  Google Scholar 

  • He CX, Yan JQ, Shen GX, Fu LH, Holaday AS, Auld D, Blumwald E, Zhang H (2005) Expression of an arabidopsis vacuolar sodium/proton antiporter gene in cotton improves photosynthetic performance under salt conditions and increases fiber yield in the field. Plant Cell Physiol 46:1848–1854

    CAS  PubMed  Google Scholar 

  • He T, Cramer GR (1993) Salt tolerance of rapid-cycling brassica species in relation to potassium sodium ratio and selectivity at the whole plant and callus levels. J Plant Nutr 16:1263–1277

    CAS  Google Scholar 

  • Hebert SC, Mount DB, Gamba G (2004) Molecular physiology of cation-coupled Cl cotransport: the SLC12 family. Pflugers Arch 447:580–593

    CAS  PubMed  Google Scholar 

  • Henriksson E, Henriksson KN (2005) Salt-stress signalling and the role of calcium in the regulation of the Arabidopsis ATHB7 gene. Plant Cell Environ 28:202–210

    CAS  Google Scholar 

  • Hirschi KD (2004) The calcium conundrum. Both versatile nutrient and specific signal. Plant Physiol 136:2438–2442

    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 

  • 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

    CAS  PubMed  Google Scholar 

  • Horie T, Horie R, Chan WY, Leung HY, Schroeder JI (2006) Calcium regulation of sodium hypersensitivities of sos3 and athkt1 mutants. Plant Cell Physiol 47:622–633

    CAS  PubMed  Google Scholar 

  • Horie T, Costa A, Kim TH, Han MJ, Horie R, Leung HY, Miyao A, Hirochika H, An G, Schroeder JI (2007) Rice OsHKT2;1 transporter mediates large Na+ influx component into K+-starved roots for growth. Embo J 26:3003–3014

    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

    CAS  PubMed  Google Scholar 

  • Huang S, Spielmeyer W, Lagudah ES, Munns R (2008) Comparative mapping of HKT genes in wheat, barley, and rice, key determinants of Na+ transport, and salt tolerance. J Exp Bot 59:927–937

    CAS  PubMed  Google Scholar 

  • Isenring P, Forbush B (1997) Ion and bumetanide binding by the Na-K-Cl cotransporter. importance of transmembrane domains. J Biol Chem 272:24556–24562

    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

    CAS  PubMed  Google Scholar 

  • Jayasekaran K, Kim KN, Vivekanandan M, Shin JS, Ok SH (2006) Novel calcium-binding GTPase (AtCBG) involved in ABA-mediated salt stress signaling in Arabidopsis. Plant Cell Rep 25:1255–1262

    CAS  PubMed  Google Scholar 

  • Kader MA, Seidel T, Golldack D, Lindberg S (2006) Expressions of OsHKT1, OsHKT2, and OsVHA are differentially regulated under NaCl stress in salt-sensitive and salt-tolerant rice (Oryza sativa L.) cultivars. J Exp Bot

  • Katiyar-Agarwal S, Zhu J, Kim K, Agarwal M, Fu X, Huang A, Zhu JK (2006) The plasma membrane Na+/H+ antiporter SOS1 interacts with RCD1 and functions in oxidative stress tolerance in Arabidopsis. Proc Natl Acad Sci USA 103:18816–18821

    CAS  PubMed  Google Scholar 

  • Kato Y, Hazama A, Yamagami M, Uozumi N (2003) Addition of a peptide tag at the C terminus of AtHKT1 inhibits its Na+ transport. Biosci Biotechnol Biochem 67:2291–2293

    CAS  PubMed  Google Scholar 

  • Kim EJ, Kwak JM, Uozumi N, Schroeder JI (1998) AtKUP1: An Arabidopsis gene encoding high-affinity potassium transport activity. Plant Cell 10:51–62

    CAS  PubMed  Google Scholar 

  • Kim BG, Waadt R, Cheong YH, Pandey GK, Dominguez-Solis JR, Schultke S, Lee SC, Kudla J, Luan S (2007) The calcium sensor CBL10 mediates salt tolerance by regulating ion homeostasis in Arabidopsis. Plant J 52:473–484

    CAS  PubMed  Google Scholar 

  • Kiss L, Immke D, LoTurco J, Korn S (1998) The interaction of Na+ and K+ in voltage-gated potassium channels: evidence for cation binding sites of different affinity. J Gen Physiol 111:195–206

    CAS  PubMed  Google Scholar 

  • Kiss L, LoTurco J, Korn S (1999) Contribution of the selectivity filter to inactivation in potassium channels. Biophys J 76:253–263

    CAS  PubMed  Google Scholar 

  • Kloareg B, Demarty M, Mabeau S (1987) Ion-exchange properties of isolated of isolated cell walls of brown algae: the interstitial solution. J Exp Bot 38:1652–1662

    CAS  Google Scholar 

  • Knight H, Trewavas AJ, Knight MR (1997) Calcium signalling in Arabidopsis thaliana responding to drought and salinity. Plant J 12:1067–1078

    CAS  PubMed  Google Scholar 

  • Köhler C, Merkle T, Roby D, Neuhaus G (2001) Developmentally regulated expression of a cyclic nucleotidegated ion channel from Arabidopsis indicates its involvement in programmed cell death. Planta 213:327–332

    PubMed  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 42 K+ and 24Na+. Plant Cell Environ 29:2228–2237

    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

    CAS  PubMed  Google Scholar 

  • Laurie S, Feeney KA, Maathuis FJM, Heard PJ, Brown SJ, Leigh RA (2002) A role for HKT1 in sodium uptake by wheat roots. Plant J 32:139–149

    CAS  PubMed  Google Scholar 

  • Lee SC, Lan WZ, Kim BG, Li LG, Cheong YH, Pandey GK, Lu GH, Buchanan BB, Luan S (2007) A protein phosphorylation/dephosphorylation network regulates a plant potassium channel. PNAS 104:15959–15964

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Li JY, Jiang GQ, Huang P, Ma J, Zhang FC (2007) Overexpression of the Na+/H+ antiporter gene from Suaeda salsa confers cold and salt tolerance to transgenic Arabidopsis thaliana. Plant Cell Tiss Organ Cult 90:41–48

    CAS  Google Scholar 

  • Li J, He X, Xu L, Zhou J, Wu P, Shou H, Zhang F (2008) Molecular and functional comparisons of the vacuolar Na+/H+ exchangers originated from glycophytic and halophytic species. J Zhejiang Univ Sci B 9:132–140

    CAS  PubMed  Google Scholar 

  • Lindsay MP, Lagudah ES, Hare RA, Munns R (2004) A locus for sodium exclusion (Nax1), a trait for salt tolerance, mapped in durum wheat. Funct Plant Biol 31:1105–1114

    CAS  Google Scholar 

  • Liu JP, Zhu JK (1997) An Arabidopsis mutant that requires increased calcium for potassium nutrition and salt tolerance. Proc Natl Acad Sci USA 94:14960–14964

    CAS  PubMed  Google Scholar 

  • Liu WH, Schachtman DP, Zhang W (2000) Partial Deletion of a Loop Region in the High Affinity K+ Transporter HKT1 Changes Ionic Permeability Leading to Increased Salt Tolerance. J Biol Chem 275:27924–27932

    CAS  PubMed  Google Scholar 

  • Liu WH, 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

    CAS  PubMed  Google Scholar 

  • Lopez-Barneo J, Hoshi T, Heinemann S, Aldrich R (1993) Effects of external cations and mutations in the pore region on C-type inactivation of shaker potassium channels. Recept Channels 1:61–71

    CAS  PubMed  Google Scholar 

  • Lynch J, Cramer GR, Lauchli A (1987) Salinity reduces membrane-associated calcium in corn root protoplasts. Plant Physiol 83:390–394

    CAS  PubMed  Google Scholar 

  • Lynch J, Polito VS, Läuchli A (1989) Salinity stress increases cytoplasmic Ca activity in maize root protoplasts. Plant Physiol (Bethesda) 90:1271–1274

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

    CAS  PubMed  Google Scholar 

  • Martinez-Atienza J, Jiang X, Garciablades B, Mendoza I, Zhu JK, Pardo JM, Quintero FJ (2007) Conservation of the salt overly sensitive pathway in rice. Plant Physiol 143:1001–1012

    CAS  PubMed  Google Scholar 

  • Maser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJM, Sanders D, Harper JF, Tchieu J, Gribskov M, Persans MW, Salt DE, Kim SA, Guerinot ML (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667

    CAS  PubMed  Google Scholar 

  • Maser P, Eckelman B, Vaidyanathan R, Horie T, Fairbairn DJ, Kubo M, Yamagami M, Yamaguchi K, Nishimura M, Uozumi N, Robertson W, Sussman MR, Schroeder JI (2002) Altered shoot/root Na+ distribution and bifurcating salt sensitivity in Arabidopsis by genetic disruption of the Na+ transporter AtHKTI1. FEBS Lett 531:157–161

    CAS  PubMed  Google Scholar 

  • Melgar JC, Benlloch M, Fernandez-Escobar R (2006) Calcium increases sodium exclusion in olive plants. Sci Hortic 109:303–305

    CAS  Google Scholar 

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Munns R, Hare RA, James RA, Rebetzke GJ (2000) Genetic variation for improving the salt tolerance of durum wheat. Aust J Agric Res 51:69–74

    CAS  Google Scholar 

  • Ogielska E, Aldrich R (1998) A mutation in S6 of Shaker potassium channels decreases the K+ affinity of an ion binding site revealing ionion interactions in the pore. J Gen Physiol 112:243–257

    CAS  PubMed  Google Scholar 

  • Ogielska E, Aldrich R (1999) Functional consequences of a decreased potassium affinity in a potassium channel pore ion interactions and C-type inactivation. J Gen Physiol 113:347–358

    CAS  PubMed  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

    CAS  Google Scholar 

  • Olías R, Eljakaoui Z, Li J, Morales PAD, Marín-manzano MC, Pardo JM, Belver A (2009) The plasma membrane Na+/H+ antiporter SOS1 is essential for salt tolerance in tomato and affects the partitioning of Na+ between plant organs. Plant Cell Environ 32:904–916

    PubMed  Google Scholar 

  • Ozturk ZN, Talame V, Deyholos M, Michalowski CB, Galbraith DW, Gozukirmizi N, Tuberosa R, Bohnert HJ (2002) Monitoring large-scale changes in transcript abundance in drought- and salt-stressed barley. Plant Mol Biol 48:551–573

    CAS  Google Scholar 

  • Panet R, Marcus M, Atlan H (1999) Overexpression of the Na+/K+/Cl− cotransporter gene induces cell proliferation and phenotypic transformation in mouse fibroblasts. J Cell Physiol 182:109–118

    Google Scholar 

  • Pardo JM, Reddy MP, Yang S, Maggio A, Huh GH, Matsumoto T, Coca MA, Koiwa H, Yun DJ, Watad AA, Bressan RA, Hasegawa PM (1998) Stress signalling through Ca2+/calmodulin-dependent protein phosphatase calcineurin mediates saltadaptation in plants. Proc Natl Acad Sci USA 95:9681–9686

    CAS  PubMed  Google Scholar 

  • Phean-O-pas S, Punteeranurak P, Buaboocha T (2005) Calcium signaling-mediated and differential induction of calmodulin gene expression by stress in Oryza sativa L. J Biochem Mol Biol 38:432–439

    CAS  PubMed  Google Scholar 

  • Pitman MG (1984) Transport across the root and shoot/root interactions. In: Staples RC, Toennissen GH (eds) Salinity tolerance in plants: strategies for crop improvement. Wiley, New York, pp 93–123

    Google Scholar 

  • Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci USA 99:8436–8441

    CAS  PubMed  Google Scholar 

  • Quintero FJ, Ohta M, Shi HZ, Zhu JK, Pardo JM (2002) Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na + homeostasis. Proc Natl Acad Sci USA 99:9061–9066

    CAS  PubMed  Google Scholar 

  • Ren ZH, Gao JP, Li LG, Cai XL, Huang W, Chao DY, Zhu MZ, Wang ZY, Luan S, Lin HX (2005) A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat Genet 37:1141–1146

    CAS  PubMed  Google Scholar 

  • Rengasamy P (2006) World salinization with emphasis on Australia. J Exp Bot 57:1017–1023

    CAS  PubMed  Google Scholar 

  • Rodriguez-Navarro A (2000) Potassium transport in fungi and plants. Biochim Biophys Acta 1469:1–30

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Rubio F, Flores P, Navarro JM, Martinez V (2003) Effects of Ca2+, K+ and cGMP on Na+ uptake in pepper plants. Plant Sci 165:1043–1049

    CAS  Google Scholar 

  • Rus A, Yokoi S, Sharkhuu A, Reddy M, Lee BH, Matsumoto TK, Koiwa H, Zhu JK, Bressan RA, Hasegawa PM (2001) AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots. Proc Natl Acad Sci USA 98:14150–14155

    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

    CAS  PubMed  Google Scholar 

  • Rus AM, Bressan RA, Hasegawa PM (2005) Unraveling salt tolerance in crops. Nat Genet 37:1029–1030

    CAS  PubMed  Google Scholar 

  • Rus A, Baxter I, Muthukumar B, Gustin J, Lahner B, Yakubova E, Salt DE (2006) Natural variants of AtHKT1 enhance Na+ accumulation in two wild Populations of Arabidopsis. Plos Genetics 2:1964–1973

    CAS  Google Scholar 

  • Russel J (2000) Sodium-potassium-chloride cotransport. Physiol Rev 80:211–276

    Google Scholar 

  • Sacala E, Biegun A, Demczuk A, Grzys E (2005) Effect of NaCl and supplemental calcium on growth parameters and nitrate reductase activity in maize. Acta Soc Bot Pol 74:119–123

    CAS  Google Scholar 

  • Sanchez-Barrena MJ, Martinez-Ripoll M, Zhu JK, Albert A (2005) The structure of the Arabidopsis thaliana SOS3: Molecular mechanism of sensing calcium for salt stress response. J Mol Biol 345:1253–1264

    CAS  PubMed  Google Scholar 

  • Santa-María GE, Rubio F, Dubcovsky J, Rodríguez-Navarroa A (1997) The HAKl gene of barley is a member of a large gene family and encodes a high-affinity potassium transporter. Plant Cell 9:2281–2289

    PubMed  Google Scholar 

  • Schachtman DP (2000) Molecular insights into the structure and function of plant K+ transport mechanisms. Biochim Biophys Acta 1465:127–139

    CAS  PubMed  Google Scholar 

  • Schachtman DP, Schroeder JI (1994) Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plants. Nature 370:655–658

    CAS  PubMed  Google Scholar 

  • Schachtman DP, Liu WH (1999) Molecular pieces to the puzzle of the interaction between potassium and sodium uptake in plants. Trends Plant Sci 4:281–287

    PubMed  Google Scholar 

  • Schachtman DP, Tyerman SD, Terry BR (1991) The K+/Na+ selectivity of a cation channel in the plasma membrane of root cells does not differ in salt-tolerant and salt-sensitive wheat species. Plant Physiol 97:598–605

    CAS  PubMed  Google Scholar 

  • Schachtman DP, Kumar R, Schroeder JI, Marsh EL (1997) Molecular and functional characterization of a novel low-affinity cation transporter (LCT1) in higher plants. Proc Natl Acad Sci USA 94:11079–11084

    CAS  PubMed  Google Scholar 

  • Schmidt C, He T, Cramer GR (1993) Supplemental calcium does not improve growth of salt-stressed brassicas. Plant Soil 156:415–418

    Google Scholar 

  • Senn ME, Rubio F, Banuelos MA, Rodrıguez-Navarro A (2001) Comparative functional features of plant potassium HvHAK1 and HvHAK2 transporters. J Biol Chem 30:44563–44569

    Google Scholar 

  • Sentenac H, Bonneaud N, Minet M, Lacroute F, Salmon JM, Gaymard F, Grignon C (1992) Cloning and expression in yeast of a plant potassium ion transport system. Science 256:663–665

    CAS  PubMed  Google Scholar 

  • Shah SH, Gorham J, Forster BP, Wyn Jones RGW (1987) Salt tolerance in the Triticeae: the contribution of the D-genome to cation selectivity in hexaploid wheat. J Exp Bot 38:254–269

    CAS  Google Scholar 

  • Shen MR, Chou CY, Hsu KF, Liu HS, Dunham PB, Holtzman EJ, Ellory JC (2001) The KCl cotransporter isoform KCC3 can play an important role in cell growth regulation. Proc Natl Acad Sci USA 98:14714–14719

    CAS  PubMed  Google Scholar 

  • Shi HZ, 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

    CAS  PubMed  Google Scholar 

  • Starkus J, Kuschel L, Rayner M, Heinemann S (1997) Ion conduction through C-type inactivated Shaker channels. J Gen Physiol 110:539–550

    CAS  PubMed  Google Scholar 

  • Starkus J, Kuschel L, Rayner M, Heinemann S (1998) Macroscopic Na+ currents in the "Nonconducting" Shaker potassium channel mutant W434F. J Gen Physiol 112:85–93

    CAS  PubMed  Google Scholar 

  • Starkus J, Heinemann S, Rayner M (2000) Voltage dependence of slow inactivation in Shaker potassium channels results from changes in relative K+ and Na+ permeabilities. J Gen Physiol 115:107–122

    CAS  PubMed  Google Scholar 

  • Stassart JM, Neirinckx L, Dejaegere R (1981) The interactions between monovalent cations and Ca during their absorption on isolated cell walls and absorption by intact barley roots. Ann Bot 47:647–652

    CAS  Google Scholar 

  • Su H, Golldack D, Zhao CS, 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  Google Scholar 

  • Su H, Balderas E, Vera-Estrella R, Golldack D, Quigley F, Zhao CS, Pantoja O, Bohnert JH (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 

  • Sunarpi HT, Motoda J, Kubo M, Yang H, Yoda K, Horie R, Chan WY, Leung HY, Hattori K, Konomi M, Osumi M, Yamagami M, Schroeder JI, Uozumi N (2005) Enhanced salt tolerance mediated by AtHKT1 transporterinduced Naþ unloading from xylem vessels to xylem parenchyma cells. Plant J 44:928–938

    CAS  PubMed  Google Scholar 

  • Takahashi R, Nishio T, Ichizen N, Takano T (2007a) Cloning and functional analysis of the K+ transporter PhaHAK2 from salt-sensitive and salt-tolerant reed plants. Biotechnol Lett 29:501–506

    CAS  PubMed  Google Scholar 

  • Takahashi R, Nishio T, Ichizen N, Takano T (2007b) High affinity K+ transporter PhaHAK5 is expressed only in salt-sensitive reed plants and shows Na+ permeability under NaCl stress. Plant Cell Rep 26:1673–1679

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Tobe K, Zhang LP, Omasa K (2003) Alleviatory effects of calcium on the toxicity of sodium, potassium and magnesium chlorides to seed germination in three non-halophytes. Seed Sci Res 13:47–54

    CAS  Google Scholar 

  • Tuna AL, Kaya C, Ashraf M, Altunlu H, Yokas I, Yagmur B (2007) The effects of calcium sulphate on growth, membrane stability and nutrient uptake of tomato plants grown under salt stress. Environ Exp Bot 59:173–178

    CAS  Google Scholar 

  • Tyerman SD, Skerrett IM (1999) Root ion channels and salinity. Sci Hortic 78:175–235

    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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Wang ZQ, Zhu SQ, Yu RP (1993) Chinese Salinized Soil. Science Press, Beijing

    Google Scholar 

  • Wang Z, Hesketh J, Fedida D (2000) A high-Na+ conduction state during recovery from inactivation in the K+ channel Kv1.5. Biophys Chem 79:2416–2433

    CAS  Google Scholar 

  • Wang SM, Zheng WJ, Ren JZ, Zhang CL (2002) Selectivity of various types of salt-resistant plants for K+ over Na+. J Arid Environ 52:457–472

    Google Scholar 

  • Wang SM, Wan CG, Wang YR, Chen H, Zhou ZY, Fu H, Sosebee RE (2004a) The characteristics of Na+, K+ and free proline distribution in several drought-resistant plants of the Alxa Desert, China. J Arid Environ 56:525–539

    Google Scholar 

  • Wang SM, Zhao GQ, Gao YS, Tang ZC, Zhang CL (2004b) Puccinellia tenuiflora exhibits stronger selectivity for K+ over Na+ than wheat. J Plant Nutr 27:1841–1857

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Wang CM, Zhang JL, Liu XS, Li Z, Wu GQ, Cai JY, 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

    CAS  PubMed  Google Scholar 

  • White PJ (1999) The molecular mechanism of sodium influx to root cells. Trends Plant Sci 4:245–246

    PubMed  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  Google Scholar 

  • Xiong L, Zhu JK (2002) Salt tolerance. In: Somerville CR, Meyerowitz EM (eds) The arabidopsis book. The American Society of Plant Biologists, Rockville, MD, pp 1–22

    Google Scholar 

  • Xu J, Lytle C, Zhu T, Payne J, Benz E, Forbush B (1994) Molecular cloning and functional expression of the bumetanide sensitive Na-K-Cl cotransporter. Proc Natl Acad Sci USA 91:2201–2205

    CAS  PubMed  Google Scholar 

  • Xu J, Li HD, Chen LQ, Wang Y, Liu LL, He L, Wu WH (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, Blumwald E (2005) Developing salt-tolerant crop plants: challenges and opportunities. Trends Plant Sci 10:615–620

    CAS  PubMed  Google Scholar 

  • Yang Q, Chen ZZ, Zhou XF, Yin HB, Li X, Xin XF, Hong XH, Zhu JK, Gong ZZ (2009) Overexpression of SOS (Salt Overly Sensitive) genes increases salt tolerance in transgenic Arabidopsis. Mol Plant 2:22–31

    CAS  PubMed  Google Scholar 

  • Yellen G (1998) The moving parts of voltage-gated ion channels. Q Rev Biophys 31:239–295

    CAS  PubMed  Google Scholar 

  • Yeo AR, Flowers TJ (1985) The absence of an effect of the Na/Ca ratio on sodium chloride uptake by rice (Oryza sativa L.). New Phytol 99:81–90

    CAS  Google Scholar 

  • Zhang JL (2008) Low-affinity Na+ uptake and accumulation in the halophyte Suaeda maritima. Dissertation,. Lanzhou University

  • Zhang HX, Blumwald E (2001) Transgenic salt tolerant tomato plant accumulate salt in the foliage not in the fruit. Nat Biotechnol 19:765–768

    CAS  PubMed  Google Scholar 

  • Zhang H, Kim MS, Sun Y, Dowd SE, Shi H, Paré PW (2008) Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT1. Mol Plant Microb Interact 21:737–744

    Google Scholar 

  • Zhong HL, Läuchli A (1993a) Changes of cell wall composition and polymer size in primary roots of cotton seedlings under high salinity. J Exp Bot 44:773–778

    CAS  Google Scholar 

  • Zhong HL, Läuchli A (1993b) Spatial and temporal aspects of growth in the primary root of cotton seedlings - effects of NaCl and CaCl2. J Exp Bot 44:763–771

    CAS  Google Scholar 

  • Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    CAS  PubMed  Google Scholar 

  • Zimmermann S, Sentenac H (1999) Plant ion channels: from molecular structures to physiological functions. Curr Opin Plant Biol 2:477–482

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Research in our lab was funded by the National Basic Research Program of China (973 Program, grant No. 2007CB108901), the National Natural Science Foundation of China (grant No. 30671488, 30700562 and 30770347), the National High Tech Project of China (grant No. 2006AA10Z126), the program for New Century Excellent Talents, China (grant No. NCET-05-0882) and the Interdisciplinary Innovation Research Fund for Young Scholars, Lanzhou University (grant No. LZU200516).

Author information

Authors and Affiliations

  1. Key Laboratory of Grassland Agro-ecosystem, Ministry of Agriculture, College of Pastoral Agriculture Science and Technology, Lanzhou University, P.O. Box 61, Lanzhou, 730000, People’s Republic of China

    Jin-Lin Zhang & Suo-Min Wang

  2. Department of Biology and Environmental Science, School of Life Sciences, University of Sussex, Falmer, Brighton, Sussex, BN1 9QG, UK

    Timothy J. Flowers

Authors
  1. Jin-Lin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Timothy J. Flowers
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Suo-Min Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Suo-Min Wang.

Additional information

Responsible Editor: Hans Lambers.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, JL., Flowers, T.J. & Wang, SM. Mechanisms of sodium uptake by roots of higher plants. Plant Soil 326, 45–60 (2010). https://doi.org/10.1007/s11104-009-0076-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-009-0076-0

Keywords

Search

Navigation