Sodium as nutrient and toxicant
Tóm tắt
Sodium (Na+) is one of the most intensely researched ions in plant biology and has attained a reputation for its toxic qualities. Following the principle of Theophrastus Bombastus von Hohenheim (Paracelsus), Na+ is, however, beneficial to many species at lower levels of supply, and in some, such as certain C4 species, indeed essential. Here, we review the ion’s divergent roles as a nutrient and toxicant, focusing on growth responses, membrane transport, stomatal function, and paradigms of ion accumulation and sequestration. We examine connections between the nutritional and toxic roles throughout, and place special emphasis on the relationship of Na+ to plant potassium (K+) relations and homeostasis. Our review investigates intriguing connections and disconnections between Na+ nutrition and toxicity, and concludes that several leading paradigms in the field, such as on the roles of Na+ influx and tissue accumulation or the cytosolic K+/Na+ ratio in the development of toxicity, are currently insufficiently substantiated and require a new, critical approach.
Tài liệu tham khảo
Alekseev AM, Abdurakhamanov AA (1966) On the influence of ions of mineral nutrient salts on the state of the protoplasm of plant cells. Fiziol Rast 13:414–419
Allen MB, Arnon DI (1955) Studies on nitrogen-fixing blue-green algae. I. growth and nitrogen fixation by Anabaena cylindrica Lemm. Plant Physiol 30:366–372
Almeida JCR, Laclau JP, de Moraes Gonçalves JL, Ranger J, Saint-André L (2010) A positive growth response to NaCl applications in Eucalyptus plantations established on K-deficient soils. For Ecol Manag 259:1786–1795
Amtmann A, Gradmann D (1994) Na+ transport in Acetabularia bypasses conductance of plasmalemma. J Membr Biol 139:117–125
Amtmann A, Sanders D (1999) Mechanisms of Na+ uptake by plant cells. Adv Bot Res 29:75–112
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
Aoki N, Ohnishi J, Kanai R (1992) 2 different mechanisms for transport of pyruvate into mesophyll chloroplasts of C4 plants-a comparative study. Plant Cell Physiol 33:805–809
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
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
Bañuelos MA, Garciadeblas B, Cubero B, Rodríguez-Navarro (2002) Inventory and functional characterization of the HAK potassium transporters of rice. Plant Physiol 130:784–795
Barbier G, Chambannes J (1951) Accumulation du sodium dans les racines de plantes. C R Acad Sci 232:1372–1374
Baxter I, Brazelton JN, Yu D, Huang YS, Lahner B, Yakubova E, Li Y, Bergelson J, Borevitz JO, Nordborg M, Vitek O, Salt DE (2010) A coastal cline in sodium accumulation in Arabidopsis thaliana is driven by natural variation of the sodium transporter AtHKT1;1. Plos Genet 6:1–8
Bazihizina N, Barrett-Lennard EG, Colmer TD (2012) Plant growth and physiology under heterogeneous salinity. Plant Soil 354:1–19
Benlloch M, Ojeda MA, Ramos J, Rodriguez-Navarro A (1994) Salt sensitivity and low discrimination between potassium and sodium in bean plants. Plant Soil 166:117–123
Binzel HL, Hess FD, Bressan RA, Hasegawa PM (1988) Intracellular compartmentation of ions in salt adapted tobacco cell. Plant Physiol 86:607–614
Blatt MR (1992) K+ channels of stomatal guard cells—characteristics of the inward rectifiers and its control by pH. J Gen Physiol 99:615–644
Blumwald E, Poole RJ (1985) Na+/H+ antiport in isolated tonoplast vesicles from storage issue of Beta vulgaris. Plant Physiol 78:163–167
Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. Biochem Biophys Acta 1465:140–151
Botella MA, Martinez V, Pardines J, Cerdá A (1997) Salinity induced potassium deficiency in maize plants. J Plant Physiol 150:200–205
Bowling DJF, Ansari AQ (1971) Evidence for a sodium influx pump in sunflower roots. Planta 98:323–329
Bowling DJF, Ansari AQ (1972) Control of sodium transport in sunflower roots. J Exp Bot 23:241–246
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
Britto DT, Kronzucker HJ (2001) Can unidirectional influx be measured in higher plants? A mathematical approach using parameters from efflux analysis. New Phytol 150:37–47
Britto DT, Kronzucker HJ (2003) Ion fluxes and cytosolic pool sizes: examining fundamental relationships in transmembrane flux regulation. Planta 217:490–497
Britto DT, Kronzucker HJ (2005) Nitrogen acquisition, PEP carboxylase, and cellular pH homeostasis: new views on old paradigms. Plant Cell Environ 28:1396–1409
Britto DT, Kronzucker HJ (2006) Futile cycling at the plasma membrane: a hallmark of low-affinity nutrient transport. Trends Plant Sci 11:529–534
Britto DT, Kronzucker HJ (2008) Cellular mechanisms of potassium transport in plants. Physiol Plant 133:637–650
Britto DT, Kronzucker HJ (2009) Ussing’s conundrum and the search for transport mechanisms in plants. New Phytol 183:243–246
Britto DT, Kronzucker HJ (2011) Genes do not form channels. Plant Soil 346:15–17
Britto DT, Kronzucker HJ (2012) Isotope techniques to study kinetics of Na+ and K+ transport under salinity conditions. Meths Mol Biol 913:389–398
Britto DT, Ebrahimi-Ardebili S, Hamam AM, Coskun D, Kronzucker HJ (2010) 42K analysis of sodium-induced potassium efflux in barley: mechanism and relevance to salt tolerance. New Phytol 186:373–384
Brownell PF (1965) Sodium as an essential micronutrient element for a higher plant (Atriplex vesicaria). Plant Physiol 40:460–468
Brownell PF (1968) Sodium as an essential micronutrient element for some higher plants. Plant Soil 28:161–164
Brownell PF, Crossland CJ (1972) The requirement for sodium as a micronutrient by species having the C4 dicarboxylic photosynthetic pathway. Plant Physiol 49:794–797
Brownell PF, Jackman ME (1966) Changes during recovery from sodium deficiency in Atriplex. Plant Physiol 41:617–622
Brownell PF, Nicholas DJD (1968) Some effects of sodium on nitrate assimilation and N2 fixation in Anabaena cylindrica. Plant Physiol 42:915–921
Brownell PF, Wood JG (1957) Sodium as an essential micronutrient element for Atriplex vesicaria, Heward. Nature 179:635–636
Cakmak I (2005) The role of potassium in alleviating detrimental effects of abiotic stresses in plants. J Plant Nutr Soil Sci 168:521–530
Carden DE, Walker DJ, Flowers TJ (1998) Root cell cytosolic ion differences between barley cultivars may contribute to salt tolerance. In: Abstracts of the 11th International Workshop on Plant Membrane Biology. The Society of Experimental Biology, 345
Carden DE, Diamond D, Miller AJ (2001) An improved Na+-selective microelectrode for intracellular measurements in plant cells. J Exp Bot 52:1353–1359
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
Cheeseman JM (1982) Pump-leak sodium fluxes in low salt corn roots. J Membr Biol 70:157–164
Cheeseman JM (2013) The integration of activity in saline environments: problems and perspectives. Funct Plant Biol. doi:10.1071/FP12285
Chen H, An R, Tang J-H, Cui XH, Hao F-S, Chen J, Wang XC (2007) Over-expression of a vacuolar Na+/H+ antiporter gene improves salt tolerance in an upland rice. Mol Breeding 19:215–225
Cope JT, Bradfield R, Peech M (1953) Effect of sodium fertilization on yield and cation content of some field crops. Soil Sci 76:65–79
Corratgé-Faillie, Jabnoune M, Zimmermann S, Véry AA, Fizames C, Sentenac H (2010) Potassium and sodium transport in non-animal cells: the Trk/Ktr/HKT transporter family. Cell Mol Life Sci 67:2511–2532
Coskun D, Britto DT, Jean YK, Kabir I, Tolay I, Torun AA, Kronzucker HJ (2013) K+ efflux and retention in response to NaCl stress do not predict salt tolerance in contrasting genotypes of rice (Oryza sativa L.). PLoS One 8:1–16
Cram WJ (1969) Short term influx as a measure of influx across the plasmalemma. Plant Physiol 44:1013–1015
Cramer GR (1992) Kinetics of maize leaf elongation II. Responses of a Na-excluding cultivar and a Na-including cultivar to varying Na/Ca salinities. J Exp Bot 43:857–864
Cramer GR, Läuchli A, Polito VS (1985) Displacement of Ca2+ by Na+ from the plasmalemma of root cells. Plant Physiol 79:207–211
Cramer GR, Alberico GJ, Schmidt C (1994) Salt tolerance is not associated with the sodium accumulation of 2 maize hybrids. Aust J Plant Physiol 21:675–692
Davenport RJ, Tester M (2000) A weakly voltage-dependent, nonselective cation channel mediates toxic sodium influx in wheat. Plant Physiol 122:823–834
Desplanque B, Boudry P, Broomberg K, Saumitou-Laprade P, Cuguen J, Van Dijk H (1999) Genetic diversity and gene flow between wild, cultivated and weedy forms of Beta vulargis L. (Chenopodiaceae), assessed by RFLP and microsatellite markers. Theor Appl Genet 98:1194–1201
Ding L, Zhu JK (1997) Reduced Na+ uptake in the NaCl-hypersensitive sos1 mutant of Arabidopsis thaliana. Plant Physiol 113:795–799
Doyle DA, Cabral JM, Pfuetzner RA, Kuo A, Gulbis JM, Cohen SL, Chait BT, MacKinnon R (1998) The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280:69–77
Draycott AP, Bugg SM (1982) Response by sugarbeet to various amounts and times of application of sodium chloride fertilizer in relation to soil type. J Agric Sci 98:579–592
Draycott AP, Durrant MJ (1976) Response by sugar beet to potassium and sodium fertilizers, particularly in relation to soils containing little exchangeable potassium. J Agric Sci 87:105–112
Draycott AP, Marsh JAP, Tinker PBH (1970) Sodium and potassium relationships in sugar beet. J Agric Sci 74:568–573
Dreyer I, Uozumi N (2011) Potassium channels in plant cells. FEBS J 278:4293–4303
Durrant MJ, Draycott AP, Boyd DA (1974) The response of sugar beet to potassium and sodium fertilizers. J Agric Sci 83:427–434
Durrant MJ, Draycott AP, Milford GFJ (1978) Effect of sodium fertilizer on water status and yield of sugar beet. Ann Appl Biol 88:321–328
El-Sheikh AM, Ulrich A, Broyer TC (1967) Sodium and rubidium as possible nutrients for sugar beet plants. Plant Physiol 42:1202–1208
Epstein E (1961) Essential role of calcium in selective cation transport by plant cells. Plant Physiol 36:437–444
Epstein E, Bloom AJ (2005) Inorganic components of plants. In: Mineral nutrition of plants: principles and perspectives, 2nd edn. Sinauer Associates, Inc., Massachusetts, pp 44–45
Epstein E, Elzam OE, Rains DW (1963) Resolution of dual mechanisms of potassium absorption by barley roots. Proc Natl Acad Sci U S A 49:684–692
Erdei L, Kuiper PJC (1979) Effect of salinity on growth, cation content, Na+ uptake and translocation in salt-sensitive and salt-tolerant Plantago species. Physiol Plant 47:95–99
Eshel A (1985) Response of Suaeda aegyptiaca to KCl, NaCl, and Na2SO4 treatments. Physiol Plant 64:308–315
Essah PA, Davenport R, Tester M (2003) Sodium influx and accumulation in Arabidopsis. Plant Physiol 133:307–318
Evans HJ, Sorger GJ (1966) Role of mineral elements with emphasis on univalent cations. Annu Rev Plant Physiol 17:47–76
Flowers TJ (1974) Salt tolerance in Suaeda maritima (L) Dum. A comparison of mitochondria isolated from green tissues of Suaeda and Pisum. J Exp Bot 101:101–110
Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963
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
Flowers TJ, Läuchli A (1983) Sodium versus potassium: substitution and compartmentation. In: Läuchli A, Bieleski RL (eds) Encyclopedia of plant physiology, new series, vol 15b, inorganic plant nutrition. Springer, Berlin, pp 651–681
Flowers TJ, Hajibagheri MA, Yeo AR (1991) Ion accumulation in the cell walls of rice plants growing under saline conditions—evidence for the Oertli hypothesis. Plant Cell Environ 14:319–325
Fu HH, Luan S (1998) AtKUP1: a dual-affinity K+ transporter from Arabidopsis. Plant Cell 10:63–73
Fuchs I, Stolzle S, Ivanshikina N, Hedrich R (2005) Rice K+ uptake channel OsAKT1 is sensitive to salt stress. Planta 221:212–221
Furbank RT, von Caemmerer S, Sheehy J, Edwards G (2009) C4 rice: a challenge for plant phenomics. Funct Plant Biol 36:845–856
Furumoto T, Yamaguchi T, Ohshima-Ichie Y, Nakamura M, Tsuchida-Iwata Y, Shimamura M, Ohnishi J, Hata S, Gowik U, Westhoff P, Bräutigam A, Weber APM, Izui K (2011) A plastidial sodium-dependent pyruvate transporter. Nature 476:472–475
Galamba N (2012) Mapping structural perturbations of water in ionic solutions. J Phys Chem B 116:5242–5250
Galeev RR (1990) Application of sodium humate to potatoes. Kartofel’ I Ovoshchi 2:12–13
Gammon N (1953) Sodium and potassium requirements of pangola and other pasture grasses. Soil Sci 76:81–90
Gassmann W, Rubio F, Schroeder JI (1996) Alkali cation selectivity of the wheat root high-affinity potassium transporter HKT1. Plant J 10:869–882
Gattward JN, Almeide AAF, Souza JO, Gomes FP, Kronzucker HJ (2012) Sodium-potassium synergism in Theobroma cacao: stimulation of photosynthesis, water-use efficiency and mineral nutrition. Physiol Plant 146:350–362
Gaxiola R, Delarrinoa IF, Villalba JM, Serrano R (1992) A novel and conserved salt-induced protein is an important determinant of salt tolerance in yeast. EMBO J 11:3157–3164
Genc Y, McDonald GK, Tester M (2007) Reassessment of tissue Na+ concentration as a criterion for salinity tolerance in bread wheat. Plant Cell Environ 30:1486–1498
Gierth M, Mäser P (2007) Potassium transporters in plants—involvement in K+ acquisition, redistribution and homeostasis. FEBS Lett 581:2348–2356
Golldack D, Quigley F, Michalowski CB, Kamasani UR, Bohnert HJ (2003) Salinity stress-tolerance and -sensitive rice (Oryza sativa L.) regulate AKT1-type potassium channel transcripts differently. Plant Mol Biol 51:71–81
Greenway H, Munns R (1980) Mechanisms of salt tolerance in non-halophytes. Annu Rev Plant Biol 31:149–190
Greenway H, Osmond CB (1972) Salt responses of enzymes from species differing in salt tolerance. Plant Physiol 49:256–259
Grinstein S, Rothstein A (1986) Mechanisms of the regulation of the Na+/H+ exchanger. J Membr Biol 90:1–12
Grof CPL, Johnston M, Brownell PF (1989) Effect of sodium nutrition on the ultrastructure of chloroplasts of C4 plants. Plant Physiol 89:539–543
Hajibagheri MA, Flowers TJ (2001) Salinity tolerance in Hordeum vulgare: ion concentrations in root cells of cultivars differing in salt tolerance. Plant Soil 231:1–9
Hajibagheri MA, Harvey DMR, Flowers TJ (1987) Quantitative distribution within the root cells of salt-sensitive and salt-tolerant maize varieties. New Phytol 105:367–379
Hajibagheri MA, Flowers TJ, Collins JC, Yeo AR (1988) A comparison of the methods of X-ray microanalysis, compartmental analysis and longitudinal ion profiles to estimate cytoplasmic ion concentrations in two maize varieties. J Exp Bot 39:279–290
Hall JL, Flowers TJ (1973) Effect of salt on protein synthesis in halophyte Suaeda maritima. Planta 110:361–368
Hampe T, Marschner H (1982) Effect of sodium on morphology, water relations and net photosynthesis in sugar beet leaves. Z Pflanzenphysiol 108:151–162
Haneklaus S, Krudsen L, Schnug E (1998) Relationship between potassium and sodium in sugar beet. Commun Soil Sci Plant Anal 29:1793–1798
Harmer PM, Benne EJ (1945) Sodium as a crop nutrient. Soil Sci Soc Am J 60:137–148
Harmer PM, Benne EJ, Laughlin WM, Key C (1953) Factors affecting crop response to sodium applied as a common salt on Michigan muck soil. Soil Sci 76:1–17
Haro R, Bañuelos MA, Senn MAE, 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
Haro R, Bañuelos MA, Rodríguez-Navarro A (2010) High-affinity sodium uptake in land plants. Plant Cell Physiol 51:68–79
Harris L (1996) Concepts in zoology. Harper Collins, New York
Hauser F, Horie T (2010) A conserved primary salt tolerance mechanism mediated by HKT transporters: a mechanism for sodium exclusion and maintenance of high K+/Na+ ratio in leaves during salinity stress. Plant Cell Environ 33:552–565
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
Hedrich R, Neher E (1987) Cytoplasmic calcium regulates voltage-dependent ion channels in plant vacuoles. Nature 329:833–836
Horie T, Yoshia 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
Horie T, Brodsky DE, Costa A, Kaneko T, Lo Schiavo F, Katsuhara M, Schroeder JI (2011) K+ transport by OsHKT2;4 transporter from rice (Oryza sativa) with atypical Na+ transport properties and competition in permeation of K+ over Mg2+ and Ca2+ ions. Plant Physiol 156:1493–1507
Hosy E, Vavasseur A, Mouline K, Dreyer I, Gaymard F, Poree F, Boucherez J, Lebaudy A, Bouchez D, Véry AA, Simonneau T, Thibaud JB, Sentenac H (2003) The Arabidopsis outward K+ channel GORK is involved in regulation of stomatal movements and plant transpiration. Proc Natl Acad Sci U S A 100:5549–5554
Humble GD, Hsiao TC (1969) Specific requirement of potassium for light-activated opening of stomata in epidermal strips. Plant Physiol 44:230–234
Humble GD, Raschke K (1971) Stomatal opening quantitatively related to potassium transport—evidence from electron probe analysis. Plant Physiol 48:447–453
Hylton LO, Ulrich A, Cornelius DR (1967) Potassium and sodium interrelations in growth and mineral content of Italian Ryegrass. Agron J 59:311–314
Isayenkov S, Isner JC, Maathuis FJM (2010) Vacuolar ion channels: roles in plant nutrition and signalling. FEBS Lett 584:1982–1988
Ivashikina N, Hedrich R (2005) K+ currents through SV-type vacuolar channels are sensitive to elevated luminal sodium levels. Plant J 41:606–614
Jarvis RG, Mansfield TA (1980) Reduced stomatal response to light, carbon dioxide and abscisic acid in the presence of sodium ions. Plant Cell Environ 3:279–283
Jennings DH (1976) The effects of sodium chloride on higher plants. Biol Rev 51:453–486
Jeschke WD (1977) K+-Na+ selectivity in roots, localisation of selective fluxes and their regulation. In: Marre E, Ciferri O (eds) Regulation of cell membrane activities in plants. Elselvier, Amsterdam, pp 63–78
Jeschke WD (1982) Shoot—dependent regulation of sodium and potassium fluxes in roots of whole barley seedlings. J Exp Bot 33:601–618
Jha D, Shirley N, Tester M, Roy SJ (2010) Variation in salinity tolerance and shoot sodium accumulation in Arabidopsis ecotypes linked to differences in the natural expression levels of transporters involved in sodium transport. Plant Cell Environ 33:793–804
Johnston M, Grof CPL, Brownell PF (1988) The effect of sodium nutrition on the pool sizes of intermediates of the C4 photosynthetic pathway. Aust J Plant Physiol 15:749–760
Johnston M, Grof CPL, Brownell PF (1989) Chlorophyll a/b ratios and photosystem activity of mesophyll and bundle sheath fractions from sodium-deficient C4 plants. Aust J Plant Physiol 16:449–457
Judel G, Kuhn H (1975) Über die Wirkung einer Natriumdüngung zu Zuckerrüben bei guter Versorgung mit Kalium in Gefäßversuchen. Zucker 28:68–71
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
Kim EJ, Kwak JM, Uozumi N, Schroeder JI (1998) AtKUP1: an Arabidopsis gene encoding high-affinity potassium transport activity. Plant Cell 10:51–62
Kingsbury RW, Epstein E (1985) Salt sensitivity in wheat. A case for specific ion toxicity. Plant Physiol 80:651–654
Kochian LV, Xin-Zhi J, Lucas WJ (1985) Potassium transport in corn roots. IV. characterization of the linear component. Plant Physiol 79:771–776
Krishnamurthy P, Ranathunge K, Nayak S, Schreiber L, Mathew MK (2011) Root apoplastic barriers block Na+ transport to shoots in rice (Oryza sativa L.). J Exp Bot 62:4215–4228
Kronzucker HJ, Britto DT (2011) Sodium transport in plants: a critical review. New Phytol 189:54–81
Kronzucker HJ, Britto DT, Davenport RJ, Tester M (2001) Ammonium toxicity and the real cost of transport. Trends Plant Sci 6:335–337
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
Kronzucker HJ, Szczerba MW, Schulze LM, Britto DT (2008) Non-reciprocal interactions between K+ and Na+ ions in barley. J Exp Bot 59:2793–2801
Lancaster JD, Andrews WB, Jones US (1953) Influence of sodium on yield and quality of cotton lint and seed. Soil Sci 76:29–40
Langdale JA (2011) C4 cycles: past, present, and future research on C4 photosynthesis. Plant Cell 23:3879–3892
Larson WE, Pierre WH (1953) Interaction of sodium and potassium on yield and cation composition of selected crops. Soil Sci Soc Am J 76:51–64
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
Lawlor DW, Milford GFJ (1973) The effect of sodium on growth of water-stressed sugar-beet. Ann Bot 37:597–604
Lebaudy A, Vavasseur A, Hosy E, Dreyer I, Leonhardt N, Thibaud JB, Véry AA, Simonneau T, Sentenac H (2008) Plant adaptation to fluctuating environment and biomass production are strongly dependent on guard cell potassium channels. Proc Natl Acad Sci U S A 105:5271–5276
Lehr JJ (1941) The importance of sodium for plant nutrition I. Soil Sci 52:237–244
Lehr JJ (1950) Importance of sodium for plant nutrition: v. responses of crops other than beet. Soil Sci 72:157–166
Lehr JJ (1953) Sodium as a plant nutrient. J Sci Food Agric 4:460–471
Lehr JJ, Wybenga JM (1955) Exploratory pot experiments on sensitiveness of different crops to sodium. Plant Soil 3:251–261
Leigh RA, Wyn-Jones RG (1986) Cellular compartmentation in plant nutrition: the selective cytoplasm and the promiscuous vacuole. Adv Plant Nutr 2:249–279
Lemtiri-Chlieh F, Berkowitz GA (2004) Cyclic adenosine monophosphate regulates calcium channels in the plasma membrane of Arabidopsis leaf guard and mesophyll cells. J Biol Chem 279:35306–35312
Leonhardt N, Marin E, Vavasseur A, Forestier C (1997) Evidence for the existence of a sulfonylurea-receptor-like protein in plants: modulation of stomatal movements and guard cell potassium channels by sulfonylureas and potassium channel openers. Proc Natl Acad Sci U S A 94:14156–14161
Luo GZ, Wang HW, Huang J, Tian AG, Wang YJ, Zhang JS, Chen SY (2005) A putative plasma membrane cation/proton antiporter from soybean confers salt tolerance in Arabidopsis. Plant Mol Biol 59:809–820
Lutgens FK, Tarbuck EJ (2003) Foundations of earth science. Pearson, New Jersey
Lynch J, Läuchli A (1984) Potassium transport in salt-stressed barley roots. Planta 161:295–301
Maathuis FJM (2007) Monovalent cation transporters; establishing a link between bioinformatics and physiology. Plant Soil 301:1–15
Maathuis FJM, Amtmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Ann Bot 84:123–133
Maathuis FJM, Verlin D, Smith FA, Sanders D, Fernandez JA, Walker NA (1996) The physiological relevance of Na+-coupled K+-transport. Plant Physiol 112:1609–1616
MacRobbie EAC (1971) Fluxes and compartmentation in plant cells. Annu Rev Plant Physiol 22:75–96
Magat SS, Goh KM (1990) Effect of chloride on fertilizers on ionic composition and cation-anion balance and ratio of fodder beet (Beta vulgaris L.) grown under field conditions. New Zealand J Agric Res 33:29–40
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 relation to salinity tolerance. J Exp Bot 59:4109–4117
Mancinelli R, Botti A, Bruni F, Ricci MA, Soper AK (2007) Hydration of sodium, potassium, and chloride ions in solution and the concept of structure maker/breaker. J Phys Chem B 111:13570–13577
Marschner H (1995) Mineral nutrition of higher plants. Academic, London
Marshall JG, Sturgis MB (1953) Effects of sodium fertilizers on yield of cotton. Soil Sci 76:75–80
Martínez-Cordero MA, Martínez V, Rubio F (2005) High-affinity K+ uptake in pepper plants. Plant Mol Biol 56:413–421
Mäser P, Gierth M, Schroeder JI (2002) Molecular mechanisms of potassium and sodium uptake in plants. Plant Soil 247:43–54
Meyerhoff O, Müller K, Roelfsema M, Latz A, Lacombe B, Hedrich R, Dietrich P, Becker D (2005) AtGLR3.4, a glutamate receptor channel-like gene is sensitive to touch and cold. Planta 222:418–427
Mian A, Oomen RJFJ, Isayenkov S, Sentenac H, Maathuis FJM, Véry AA (2011) Over-expression of an Na+ and K+-permeable HKT transporter in barley improves salt tolerance. Plant J 68:468–479
Milford GFJ, Cormack WF, Durrant MJ (1977) Effects of sodium chloride on water status and growth of sugar beet. J Exp Bot 28:1380–1388
Møller IS, Tester M (2007) Salinity tolerance of Arabidopsis: a good model for cereals? Trends Plant Sci 12:534–540
Møller IS, Gilliham M, Jha D, Mayo GM, Roy SJ, Coates JC, Haseloff J, Tester M (2009) Shoot Na+ exclusion and increase salinity tolerance engineered by cell type-specific alteration of Na+ transport in Arabidopsis. Plant Cell 21:2163–2178
Montasir AH, Sharoubeem HH, Sidrak GH (1966) Partial substitution of sodium for potassium in water cultures. Plant Soil 25:181–194
Moore R, Black CC (1979) Nitrogen assimilation pathways in leaf mesophyll and bundle sheath cells of C4 photosynthetic plants formulated from comparative studies with Digitaria sanguinalis (L.) Scop. Plant Physiol 64:309–313
Müller-Röber B, Ellenberg J, Provart N, Willmitzer L, Bush H, Becker D, Dietrich P, Hoth S, Hedrich R (1995) Cloning and electrophysiological analysis of KST1, an inward rectifying K+ channel expressed in potato guard cells. EMBO J 14:2409–2416
Mullison WR, Mullison E (1942) Growth responses of barley seedlings in relation to potassium and sodium nutrition. Plant Physiol 17:632–644
Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250
Munns R, James RA (2003) Screening methods for salinity tolerance: a case study with tetraploid wheat. Plant Soil 253:201–218
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681
Munns R, Schachtman DP, Condon AG (1995) The significance of a two-phase growth response to salinity in wheat and barley. Aust J Plant Physiol 22:561–569
Munns R, James RA, Lauchli A (2005) Increasing salt tolerance in monocotyledonous plants, with emphasis on wheat. Comp Biochem Phys A 141:S337
Nakamura RL, McKendree WL, Hirsch RE, Sedbrook JC, Gaber RF, Sussman MR (1995) Expression of an Arabidopsis potassium channel in guard cells. Plant Physiol 109:371–374
Nassery H (1975) The effect of salt and osmotic stress on the retention of potassium by excised barley and bean roots. New Phytol 75:63–67
Nassery H (1979) Salt-induced loss of potassium from plant roots. New Phytol 83:23–27
Nieves-Cordones M, Martínez-Cordero MA, Martínez V, Rubio F (2007) An NH4+ -sensitive component dominates high affinity K+ uptake in tomato plants. Plant Sci 172:273–280
Nitsos RE, Evans HJ (1969) Effects of univalent cations on activity of particulate starch synthetase. Plant Physiol 44:1260–1266
Nocito FF, Sacchi GA, Cocucci M (2002) Membrane depolarization induces K+ efflux from subapical maize root segments. New Phytol 154:45–51
Nunes MA, Dias MA, Correia M, Oliveira MM (1984) Further studies on growth and osmoregulation of sugar beet leaves under low salinity conditions. J Exp Bot 35:322–331
Obata T, Kitamoto HK, Nakamura A, Fukuda A, Tanaka Y (2007) Rice shaker potassium channel OsKAT1 confers tolerance to salinity stress on year and rice cells. Plant Physiol 144:1978–1985
Ohnishi J, Kanai R (1987) Na+-induced uptake of pyruvate into mesophyll chloroplasts of a C4 plant, Panicum miliaceum. FEBS Lett 219:347–350
Ohnishi J, Flügge UI, Heldt HW, Kanai R (1990) Involvement of Na+ in active uptake of pyruvate in mesophyll chloroplasts of some C4 plants. Plant Physiol 94:950–959
Ohta D, Matoh T, Takahashi E (1987) Early responses of sodium-deficient Amaranthus tricolor L. plants to sodium application. Plant Physiol 84:112–117
Ohta D, Matsui J, Matoh T, Takahashi E (1988) Sodium requirement of monocotyledonous C4 plants for growth and nitrate reductase activity. Plant Cell Physiol 29:1429–1432
Ohta D, Yasuoka S, Matoh T, Takahashi E (1989) Sodium stimulates growth of Amaranthus tricolor L. plants through enhanced nitrate assimilation. Plant Physiol 89:1102–1105
Pallaghy CK (1968) Electrophysiogical studies in guard cells of tobacco. Planta 80:147–153
Pandey S, Zhang W, Assmann SA (2007) Roles of ion channels and transporters in guard cell signal transduction. FEBS Lett 581:2325–2336
Peck NH, van Buren JP, MacDonald GE, Hemmat H, Becker RF (1987) Table beet plant and canned root responses to Na, K, and Cl from soils and from applications of NaCl and KCl. J Am Soc Hort Sci 112:188–194
Peng YH, Zhu YF, Mao YQ, Wang SM, Su WA, Tang ZC (2004) Alkali grass resists salt stress through high [K+] and an endodermis barrier to Na+. J Exp Bot 55:939–949
Pessarakli M (2001) Handbook of plant and crop stress. Biol Plant 44:304–304
Pessarakli M, Marcum KB (2000) Growth responses and Nitrogen-15 absorption of Distichlis under sodium chloride stress. ASA-CSSA-SSSA Annual Meetings, Minneapolis, Minnesota
Pessarakli M, Tucker TC (1985) Uptake of Nitrogen-15 by cotton under salt stress. Soil Sci Soc Am J 49:149–152
Phillips WEJ (1971) Naturally occurring nitrate and nitrite in foods in relation to infant methaemoglobinaemia. Food Comest Toxicol 9:219–228
Pilot G, Gaymard F, Mouline K, Cherel I, Sentenac H (2003) Regulated expression of Arabidopsis Shaker K+ channel genes involved in K+ uptake and distribution in the plant. Plant Mol Biol 51:773–787
Porcelli CA, Boem FHG, Lavado RS (1995) The K/Na and Ca/Na ratios and rapeseed yield, under soil salinity or sodicity. Plant Soil 175:251–255
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
Quintero FJ, Blatt MR (1997) A new family of K+ transporters from Arabidopsis that are conserved across phyla. FEBS Lett 415:206–211
Rains DW, Epstein E (1965) Transport of sodium in plant tissue. Science 148:1161
Rains DW, Epstein E (1967a) Sodium absorption by barley roots—role of dual mechanisms of alkali cation transport. Plant Physiol 42:314–318
Rains DW, Epstein E (1967b) Preferential absorption of potassium by leaf tissue of mangrove Avicennia marina—an aspect of halophytic competence in coping with salt. Aust J Biol Sci 20:847–857
Rains DW, Epstein E (1967c) Sodium absorption by barley roots—its mediation by mechanism 2 of alkali cation transport. Plant Physiol 42:319–323
Rajendran K, Tester M, Roy SJ (2009) Quantifying the three main components of salinity tolerance in cereals. Plant Cell Environ 32:237–249
Redondo-Gómez S, Mateos-Naranjo E, Davy AJ, Fernández-Muñoz F, Castellanos EM, Luque T, Figueroa ME (2007) Growth and photosynthetic responses to salinity of the salt-marsh shrub Atriplex portulacoides. Ann Bot 100:555–563
Redondo-Gómez S, Mateos-Naranjo E, Figueroa ME, Davy AJ (2010) Salt stimulation of growth and photosynthesis in an extreme halophyte, Arthrocnemum macrostachyum. Plant Biol 12:79–87
Robinson MF, Véry AA, Sanders D, Mansfield TA (1997) How can stomata contribute to salt tolerance? Ann Bot 80:387–393
Rodríguez-Navarro A, Rubio F (2006) High-affinity potassium and sodium transport systems in plants. J Exp Bot 57:1149–1160
Roelfsema MRG, Hedrich R (2005) In the light of stomatal opening: new insights into ‘the Watergate’. New Phytol 167:665–691
Roomans GD (1988) Quantitative X-Ray microanalysis of biological specimens. J Electr Micr Tech 9:19–43
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
Rubio F, Santa-María GE, Rodríguez-Navarro A (2000) Cloning of Arabidopsis and barley cDNAs encoding HAK potassium transporters in root and shoot cells. Physiol Plant 109:34–43
Rubio L, Linares-Rueda A, García-Sánchez MJ, Fernández JA (2005) Physiological evidence for a sodium-dependent high-affinity phosphate and nitrate transport at the plasma membrane of leaf and root cells of Zostera marina L. J Exp Bot 56:613–622
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 U S A 98:14150–14155
Rus A, Baxter I, Muthukumar B, Gustin J, Lahner B, Yakubova Y, Salt DE (2006) Natural variants of AtHKT1 enhance Na+ accumulation in two wild populations of Arabidopsis. Plos Genet 2:1964–1973
Sage RF, Christin PA, Edwards EJ (2011) The C4 plant lineages of planet Earth. J Exp Bot 62:3155–3169
Santa-Maria GE, Epstein E (2001) Potassium/sodium selectivity in wheat and the amphiploid cross wheat X Lophopyrum elongatum. Plant Sci 160:523–534
Santa-María GE, Rubio F, Dubcovsky J, Rodríguez-Navarro A (1997) The HAK1 gene of barley is a member of a large gene family and encodes a high-affinity potassium transporter. Plant Cell 9:2281–2289
Schachtman DP, Munns R (1992) Sodium accumulation in leaves of Triticum species that differ in salt tolerance. Funct Plant Biol 19:331–340
Schachtman DP, Schroeder JI (1994) Structure and transport mechanism of a high-affinity potassium uptake transporter from higher-plants. Nature 370:655–658
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
Schönknecht G, Spoormaker P, Steinmeyer R, Brüggeman L, Ache P, Dutta R, Reintanz B, Godde M, Hedrich R, Palme K (2002) KCO1 is a component of the slow-vacuolar (SV) ion channel. FEBS Lett 511:28–32
Schroeder JI (1988) K+ transport properties of K+ channels in the plasma membrane of Vicia faba guard cells. J Gen Physiol 92:667–683
Schroeder JI, Hedrich R, Fernandez JM (1984) Potassium-selective single channels in guard cell protoplasts of Vicia faba. Nature 312:361–362
Schroeder JI, Raschke K, Neher E (1987) Voltage dependence of K+ channels in guard-cell protoplasts. Proc Natl Acad Sci U S A 84:4108–4112
Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D (2001) Guard cell signal transduction. Annu Rev Plant Physiol Mol Biol 52:627–658
Schroeppel-Meier G, Kaiser WM (1988) Ion homeostasis in chloroplasts under salinity and mineral deficiency. Plant Physiol 87:822–827
Schubert S, Läuchli A (1990) Sodium exclusion mechanisms at the root surface of two maize cultivars. Plant Soil 123:205–209
Schulze LM, Britto DT, Li M, Kronzucker HJ (2012) A pharmacological analysis of high-affinity sodium transport in barley (Hordeum vulgare L.): a 24N+/42K+ study. J Exp Bot 63:2479–2489
Schwender J, Goffman F, Ohlrogge JB, Shachar-Hill Y (2004) Rubisco without the Calvin cycle improves the carbon efficiency of developing green seeds. Nature 432:779–782
Seemann JR, Critchley C (1985) Effects of salt stress on the growth, ion content, stomatal behavior and photosynthetic capacity of salt-sensitive species, Phaseolus vulgaris L. Planta 2:151–162
Segen JC, Stauffer J (1998) The patient’s guide to medical tests. Checkmark books, New York
Senn ME, Rubio F, Bañuelos MA, Rodríguez-Navarro (2001) Comparative functional features of plant potassium HvHAK1 and HvHAK2 transporters. J Biol Chem 276:44563–44569
Shabala S, Mackay AS (2011a) Ion transport in halophytes. In: Kader J, Delseny M (eds) Advances in botanical research. Academic, Massachusetts, pp 151–199
Shabala S, Mackay AS (2011b) Ion transport in halophytes. Adv Bot Res 57:151–199
Shabala S, Shabala L, van Volkenburgh E (2003) Effect of calcium on root development and root ion fluxes in salinised barley seedlings. Funct Plant Biol 30:507–514
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
Shi HZ, Ishitami M, Kim CS, 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
Simonis W, Urbach W (1963) Über eine Wirkung von Natriumionen auf die Phosphataufnahme und die lichtabhängige Phosphorylierung von Ankistrodesmus braunii. Arch Mikrobiol 46:265–286
Smith GS, Middleton KR, Edmonds AS (1980) Sodium nutrition of pasture plants. II. effects of sodium chloride on growth, chemical composition and reduction of nitrate nitrogen. New Phytol 84:613–622
Spalding EP, Hirsch RE, Lewis DR, Qi Z, Sussman MR, Lew BD (1999) Potassium uptake supporting plant growth in the absence of AKT1 channel activity—inhibition by ammonium and stimulation by sodium. J Gen Physiol 113:909–918
Speer M, Kaiser WM (1991) Ion relations of symplastic and apoplastic space in leaves from Spinacia oleracea L. and Pisum sativum L. under salinity. Plant Physiol 97:990–997
Stanford G, Carter JN, Westermann DT, Meisinger JJ (1977) Residual nitrate and mineralizable soil nitrogen in relation to nitrogen uptake by irrigated sugar beets. Agron J 69:303–308
Su H, Golldack D, Katsuhara M, Zhao CS, Bohnert HJ (2001) Expression and stress-dependent induction of potassium channel transcripts in the common ice plant. Plant Physiol 125:604–614
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
Subbarao GV, Mackowiak C, Wheeler RM (1999a) Recycling of Na in advanced life support: strategies based on crop production systems. Life Support Biosph Sci 6:153–160
Subbarao GV, Wheeler RM, Stutte GW, Levine LH (1999b) How far can sodium substitute for potassium in red beet? J Plant Nutr 22:1745–1761
Subbarao GV, Wheeler RM, Levine LH, Stutte GW (2001) Glycine betaine accumulation, ionic and water relations of red-beet at contrasting levels of sodium supply. J Plant Physiol 158:767–776
Subbarao GV, Ito O, Berry WL, Wheeler RM (2003) Sodium—a functional plant nutrient. Crit Rev Plant Sci 22:391–416
Sunarpi, Horie T, 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 transporter-induced Na+ unloading from xylem vessels into xylem parenchyma cells. Plant J 44:928–938
Szczerba MW, Britto DT, Ali SA, Balkos KD, Kronzucker HJ (2008) NH4 +-stimulated and -inhibited components of K+ transport in rice (Oryza sativa L.). J Exp Bot 59:3415–3423
Szulc PM, Kobierski M, Kubicki K, Keutgen N (2010) The potential of sodium fertilization for sugarbeet production. Zuckerindustrie 135:721–724
Szyroki A, Ivashikina N, Dietrich P, Roelfsema MRG, Ache P, Reintanz B, Deeken R, Godde M, Felle H, Steinmeyer R, Palme K, Hedrich R (2001) KAT1 is not essential for stomatal opening. Proc Natl Acad Sci U S A 98:2917–2921
Takahashi E, Maejima K (1998) Comparative research on sodium as a beneficial element for crop plants. Mem Fac Agr Kinki Univ 31:57–72
Takahashi R, Nishio T, Ichizen N, Takano T (2007) 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
Tavakkoli E, Rengasamy P, McDonald GK (2010) High concentrations of Na+ and Cl- ions in soil solution have simultaneous detrimental effects on growth of faba bean under salinity stress. J Exp Bot 61:4449–4459
Terry N, Ulrich A (1973) Effects of potassium deficiency on the photosynthesis and respiration of leaves of sugar beet under conditions of low sodium supply. Plant Physiol 51:1099–1101
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
Thiel G, MacRobbie EAC, Blatt MR (1992) Membrane transport in stomatal guard cells: the importance of voltage control. J Membrane Biol 126:1–18
Tinker PBH (1965) The effects of nitrogen, potassium and sodium fertilizers on sugar beet. J Agric Sci 65:207–212
Truog E, Berger KC, Attoe OJ (1953) Response of nine economic plants to fertilization with sodium. Soil Sci Soc Am J 76:41–50
Tyerman SD, Skerrett IM (1999) Root ion channels and salinity. Sci Hortic-Amsterdam 78:175–235
Ulrich A, Ohki K (1956) Chlorine, bromine and sodium as nutrients for sugar beet plants. Plant Physiol 31:171–181
Vaughn KC, Campbell WH (1988) Immunogold localization of nitrate reductase in maize leaves. Plant Physiol 88:1354–1357
Venema K, Quintero FJ, Pardo JM, Donaire JP (2002) The Arabidopsis Na+/H+ exchanger AtNHX1 catalyzes low affinity Na+ and K+ transport in reconstituted liposomes. J Biol Chem 277:2413–2418
Véry AA, Gaymard F, Bosseux C, Sentenac H, Thibaud JB (1995) Expression of a cloned plant K+ channel in Xenopus oocytes: analysis of macroscopic currents. Plant J 7:321–332
Véry AA, Robinson MF, Mansfield TA, Sander D (1998) Guard cell cation channels are involved in Na+-induced stomatal closure in a halophyte. Plant J 14:509–521
von Marilaun AK (1896) The natural history of plants. Blackie & Son Ltd, London
Walker NA, Sanders D, Maathuis FJM (1996) High-affinity potassium uptake in plants. Science 273:977–978
Wallace A, Toth SJ, Bear FE (1948) Influence of sodium on growth and composition of ranger alfalfa. Soil Sci 65:477–486
Wang SM, Zhang JL, Flowers TJ (2007) Low-affinity Na+ uptake in the halophyte Suaeda maritima. Plant Physiol 145:559–571
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
Warne TR, Hickok LG, Kinraide TB, Vogelien DL (1996) High salinity tolerance in the stl2 mutation of Ceratopteris richardii is associated with enhanced K+ influx and loss. Plant Cell Environ 19:24–32
Watad AEA, Reuveni M, Bressan RA, Hasegawa PM (1991) Enhanced net K+ uptake capacity of NaCl-adapted cells. Plant Physiol 95:1265–1269
Weber APM, von Caemmerer S (2010) Plastid transport and metabolism of C3 and C4 plants—comparative analysis and possible biotechnological exploitation. Curr Opin Plant Biol 13:257–265
Wetson AM, Flowers TJ (2010) The effect of saline hypoxia on growth and ion uptake in Suaeda maritima. Funct Plant Biol 38:1024–1025
Wheeler HJ, Adams GE (1905) Concerning the agricultural value of sodium salts. Rhode Island Agricultural Experiment Station, Kingston
Williams MC (1960) Effect of sodium and potassium salts on growth and oxalate content of Halogeton. Plant Physiol 35:500–509
Williams BP, Aubry S, Hibberd JM (2012) Molecular evolution of genes recruited into C4 photosynthesis. Trends Plant Sci 17:213–220
Wolf T, Guinot DR, Hedrich R, Dietrich P, Marten I (2005) Nucleotides and Mg2+ ions differentially regulate K+ channels and non-selective cation channels present in cells forming the stomatal complex. Plant Cell Physiol 46:1682–1689
Woolley JT (1957) Sodium and silicon as nutrients for the tomato plant. Plant Physiol 1:317–321
Wyn Jones RG, Brady CJ, Speirs J (1979) Ionic and osmotic relations in plant cells. In: Laidman DL, Wyn Jones RG (eds) Recent advances in the biochemistry of cereals. Academic Press, New York, New York, pp 63–103
Yadav S, Irfan M, Ahmad A, Hayat S (2011) Causes of salinity and plant manifestations to salt stress: a review. J Environ Biol 32:667–685
Yao X, Horie T, Xue S, Leung H-Y, Katsuhara M, Brodsky DE, Wu Y, Schroeder JI (2010) Differential sodium and potassium transport selectivities of the rice OsHKT2;1 and OsHKT2;2 transporters in plant cells. Plant Physiol 152:341–355
Yeo AR, Yeo ME, Flowers SA, Flowers TJ (1990) (1990) Screening of rice (Oryza sativa L.) genotypes for physiological characters contributing to salinity resistance, and their relationship to overall performance. Theor Appl Genet 79:377–384
Zhang HX, Blumwald E (2001) Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nature 19:765–768
Zhang JL, Flowers TJ, Wang SM (2010) Mechanisms of sodium uptake by roots of higher plants. Plant Soil 326:45–60
Zhao J, Barkla BJ, Marshall J, Pittman JK, Hirschi KD (2008) The Arabidopsis cax3 mutants display altered salt tolerance, pH sensitivity and reduced plasma membrane H+-ATPase activity. Planta 227:659–669
Zhao X, Wang YJ, Wang YL, Wang XL, Zhang X (2011) Extracellular Ca2+ alleviates NaCl-induced stomatal opening through a pathway involving H2O2-blocked Na+ influx in Vicia guard cells. J Plant Physiol 168:903–910
Zhu JK, Liu J, Xiong L (1998) Genetic analysis of salt tolerance in Arabidopsis: evidence for a critical role of potassium nutrition. Plant Cell 10:1181–1191