Physiological and molecular mechanisms of plant salt tolerance

Photosynthesis Research - Tập 115 Số 1 - Trang 1-22 - 2013
Jin‐Lin Zhang1, Huazhong Shi2
1State Key Laboratory of Grassland Agro-ecosystems, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou, China
2Department of Chemistry and Biochemistry, Center for Chemical Biology, Texas Tech University, Lubbock, USA

Tóm tắt

Từ khóa


Tài liệu tham khảo

Agarie S, Shimoda T, Shimizu Y, Baumann K, Sunagawa H, Kondo A, Ueno O, Nakahara T, Nose A, Cushman JC (2007) Salt tolerance, salt accumulation, and ionic homeostasis in an epidermal bladder-cell-less mutant of the common ice plant Mesembryanthemum crystallinum. J Exp Bot 58:1957–1967

Al-Aghabary K, Zhu Z, Shi QH (2004) Influence of silicon supply on chlorophyll content, chlorophyll fluorescence, and antioxidative enzyme activities in tomato plants under salt stress. J Plant Nutr 27:2101–2115

Alemán F, Nieves-Cordones M, Martínez 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

Alemán F, Nieves-Cordones M, Martínez 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

Ali Z, Park HC, Ali A, Oh D-H, Aman R, Kropornicka A, Hong H, Choi W, Chung WS, Kim W-Y, Bressan RA, Bohnert HJ, Lee SY, Yun D-J (2012) TsHKT1;2, a HKT1 homolog from the extremophile Arabidopsis relative Thellungiella salsuginea, shows K+ specificity in the presence of NaCl. Plant Physiol 158:1463–1474

Allen GJ, Wyn Jones RG, Leigh RA (1995) Sodium transport measured in plasma membrane vesicles isolated from wheat genotypes with differing K+/Na+ discrimination traits. Plant Cell Environ 18:105–115

Amarasinghe V, Watson L (1989) Variation in salt secretory activity of microhairs in grasses. Aust J Plant Physiol 16:219–229

An R, Chen QJ, Chai MF, Lu PL, Su Z, Qin ZX, Chen J, Wang XC (2007) AtNHX8, a member of the monovalent cation: proton antiporter-1 family in Arabidopsis thaliana, encodes a putative Li/H antiporter. Plant J 49:718–728

Anil VS, Krishnamurthy P, Kuruvilla S, Sucharitha K, Thomas G, Mathew MK (2005) Regulation of the uptake and distribution of Na+ in shoots of rice (Oryza sativa) variety Pokkali: role of Ca2+ in salt tolerance response. Physiol Plantarum 124:451–464

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

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

Ardie SW, Xie L, Takahashi R, Liu S, Takano T (2009) Cloning of a high-affinity K+ transporter gene PutHKT2;1 from Puccinellia tenuiflora and its functional comparison with OsHKT2;1 from rice in yeast and Arabidopsis. J Exp Bot 60:3491–3502

Ardie SW, Liu S, Takano T (2010) Expression of the AKT1-type K+ channel gene from Puccinellia tenuiflora PutAKT1, enhances salt tolerance in Arabidopsis. Plant Cell Rep 29:865–874

Ardie SW, Nishiuchi S, Liu S, Takano T (2011) Ectopic expression of the K+ channel β subunits from Puccinellia tenuiflora (KPutB1) and rice (KOB1) alters K+ homeostasis of yeast and Arabidopsis. Mol Biotechnol 48:76–86

Ayala F, O’Leary JW, Schumaker KS (1996) Increased vacuolar and plasma membrane H+-ATPase activities in Salicornia bigelovii Torr. in response to NaCl. J Exp Bot 47:25–32

Baek D, Jiang J, Chung JS, Wang B, Chen J, Xin Z, Shi H (2011) Regulated AtHKT1 gene expression by a distal enhancer element and DNA methylation in the promoter plays an important role in salt tolerance. Plant Cell Physiol 52:149–161

Balnokin YV, Kurkova EB, Khalilova LA, Myasoedov NA, Yusufov AG (2007) Pinocytosis in the root cells of a salt-accumulating halophyte Suaeda altissima and its possible involvement in chloride transport. Russ J Plant Physiol 54:797–805

Balsamo RA, Adams ME, Thomson WW (1995) Electrophysiology of the salt glands of Avicennia germinans. Int J Plant Sci 156:658–667

Banjara M, Zhu L, Shen G, Payton P, Zhang H (2012) Expression of an Arabidopsis sodium/proton antiporter gene (AtNHX1) in peanut to improve salt tolerance. Plant Biotechnol Rep 6:59–67

Bao AK, Wang SM, Wu GQ, Xi JJ, Zhang JL, Wang CM (2009) Overexpression of the Arabidopsis H+-PPase enhanced resistance to salt and drought stress in transgenic alfalfa (Medicago sativa L.). Plant Sci 176:232–240

Bartels D, Nelson D (1994) Approaches to improve stress tolerance using molecular genetics. Plant Cell Environ 17:659–667

Baumeister VW, Kloos G (1974) Salt secretion in Halimione portulacoides (L.) Aellen. Flora 163:310–326

Baumeister W, Ziffus G (1981) Salt secretion by the salt glands of Armeria maritima L. J Plant Physiol 102:273–278

Bayat F, Shiran B, Belyaev DV (2011) Overexpression of HvNHX2, a vacuolar Na+/H+ antiporter gene from barley, improves salt tolerance in Arabidopsis thaliana. Aust J Crop Sci 5:428–432

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

Bhaskaran S, Savithramma DL (2011) Co-expression of Pennisetum glaucum vacuolar Na+/H+ antiporter and Arabidopsis H+-pyrophosphatase enhances salt tolerance in transgenic tomato. J Exp Bot 62:5561–5570

Blom-Zandstra M, Vogelzang S, Veen B (1998) Sodium fluxes in sweet pepper exposed to varying sodium concentrations. J Exp Biol 49:1863–1868

Blumwald E, Poole RJ (1985) Na+/H+ antiport in isolated tonoplast vesicles from storage tissue of Beta vulgaris. Plant Physiol 78:163–167

Bowers K, Levi BP, Patel FI, Stevens TH (2000) The sodium/proton exchanger NHX1 is required for endosomal protein trafficking in the yeast Saccharomyces cerevisiae. Mol Biol Cell 11:4277–4294

Brini F, Gaxiola RA, Berkowitz GA, Masmoudi K (2005) Cloning and characterization of a wheat vacuolar cation/proton antiporter and pyrophosphatase proton pump. Plant Physiol Bioch 43:347–354

Brini F, Hanin M, Mezghani I, Berkowitz GA, Masmoudi K (2007) Overexpression of wheat Na+/H+ antiporter TNHX1 and H+-pyrophosphatase TVP1 improve salt- and drought-stress tolerance in Arabidopsis thaliana plants. J Exp Bot 58:301–308

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

Cao Y, Jin X, Huang H, Derebe MG, Levin EJ, Kabaleeswaran V, Pan Y, Punta M, Love J, Weng J, Quick M, Ye S, Kloos B, Bruni R, Martinez-Hackert E, Hendrickson WA, Rost B, Javitch JA, Rajashankar KR, Jiang Y, Zhou M (2011) Crystal structure of a potassium ion transporter, TrkH. Nature 471:336–340

Chai Q, Shao X, Zhang J (2010) Silicon effects on Poa pratensis responses to salinity. HortSci 45:1876–1881

Chang-Qing Z, Shunsaku N, Shenkui L, Tetsuo T (2008) Characterization of two plasma membrane protein 3 genes (PutPMP3) from the alkali grass, Puccinellia tenuiflora, and functional comparison of the rice homologues, OsLti6a/b from rice. BMB Rep 41:448–454

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

Chen H, An R, Tang JH, Cui XH, Hao FS, Chen J, Wang XC (2007) Over-expression of a vacuolar Na+/H+ antiporter gene improves salt tolerance in an upland rice. Mol Breed 19:215–225

Chen LH, Zhang B, Xu ZQ (2008) Salt tolerance conferred by overexpression of Arabidopsis vacuolar Na+/H+ antiporter gene AtNHX1 in common buckwheat (Fagopyrum esculentum). Transgenic Res 17:121–132

Chen J, Xiao Q, Wu F, Dong X, He J, Pei Z, Zheng H (2010) Nitric oxide enhances salt secretion and Na+ sequestration in a mangrove plant, Avicennia marina, through increasing the expression of H+-ATPase and Na+/H+ antiporter under high salinity. Tree Physiol 30:1570–1585

Chung JS, Zhu JK, Bressan RA, Hasegawa PM, Shi H (2008) Reactive oxygen species mediate Na+-induced SOS1 mRNA stability in Arabidopsis. Plant J 53:554–565

Clipson NJW, Tomos AD, Flowers TJ, Wyn Jones RG (1985) Salt tolerance in the halophyte Suaeda maritima L. Dum. Planta 165:392–396

Cotsaftis O, Plett D, Shirley N, Tester M, Hrmova M (2012) A two-staged model of Na+ exclusion in rice explained by 3D modeling of HKT transporters and alternative splicing. PLOS One 7:e39865

Cuin TA, Bose J, Stefano G, Jha D, Tester M, Mancuso S, Shabala S (2009) Assessing the role of root plasma membrane and tonoplast Na+/H+ exchangers in salinity tolerance in wheat: in planta quantification methods. Plant Cell Environ 34:947–961

Dassanayake M, Oh DH, Haas JS, Hernandez A, Hong H, Ali S, Yun DJ, Bressan RA, Zhu JK, Bohnert HJ, Cheeseman JM (2011) The genome of the extremophile crucifer Thellungiella parvula. Nat Genet 43:913–918

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

Davenport R, James RA, Zakrisson-Plogander A, Tester M, Munns R (2005) Control of sodium transport in durum wheat. Plant Physiol 137:807–818

Davenport RJ, Muñoz-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

Drew MC, Lauchli A (1987) The role of the mesocotyl in sodium exclusion from the shoot of Zea manys L. (cv. Pioneer 3906). J Exp Biol 38:409–418

Duan XG, Yang AF, Gao F, Zhang SL, Zhang JR (2007) Heterologous expression of vacuolar H+-PPase enhances the electrochemical gradient across the vacuolar membrane and improves tobacco cell salt tolerance. Protoplasma 232:87–95

DuPont FM (1992) Salt induced changes in ion transport: regulation of primary pumps and secondary transporters. In: Clarkson DT, Cooke DT (eds) Transport and receptor proteins of plant membranes. molecular structure and function. Plenum, New York, pp 91–100

Fahn A (1988) Secretory tissues in vascular plants. New Phytol 108:229–257

Faiyue B, Al-Azzawi MJ, Flowers TJ (2010a) The role of lateral roots in bypass flow in rice (Oryza sativa L.). Plant Cell Environ 33:702–716

Faiyue B, Vijayalakshmi C, Nawaz S, Nagato Y, Taketa S, Ichii M, Al-Azzawi MJ, Flowers T (2010b) Studies on sodium bypass flow in lateral rootless mutants lrt1 and lrt2, and crown rootless mutant crl1 of rice (Oryza sativa L.). Plant Cell Environ 33:687–701

Feki K, Quintero F, Pardo J, Masmoudi K (2011) Regulation of durum wheat Na+/H+ exchanger TdSOS1 by phosphorylation. Plant Mol Biol 76:545–556

Ferjani A, Segami S, Horiguchi G, Muto Y, Maeshima M, Tsukaya H (2011) Keep an eye on PPi: the vacuolar-type H+-pyrophosphatase regulates postgerminative development in Arabidopsis. Plant Cell 23:2895–2908

Fitzgerald MA, Orlovich DA, Allaway WG (1992) Evidence that abaxial leaf glands are the sites of salt secretion in leaves of the mangrove Avicennia marina (Forsk.) Vierh. New Phytol 120:1–7

Flowers TJ (1972) Salt tolerance in Suaeda maritima (L) Dum. The effect of sodium chloride on growth respiration and soluble enzymes in a comparative study with Pisum sativum L. J Exp Bot 23:310–321

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

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

Flowers TJ, Flowers SA, Hajibagheri MA, Yeo AR (1990) Salt tolerance in the halophytic wild rice, Porteresia coarctata Tateoka. New Phytol 114:675–684

Fukuda A, Nakamura A, Tanaka Y (1999) Molecular cloning and expression of the Na+/H+ exchanger gene in Oryza sativa. BBA Gene Struct Exp 1446:149–155

Fukuda A, Chiba K, Maeda M, Nakamura A, Maeshima M, Tanaka Y (2004) Effect of salt and osmotic stresses on the expression of genes for the vacuolar H+-pyrophosphatase, H+-ATPase subunit A, and Na+/H+ antiporter from barley. J Exp Bot 55:585–594

Gao F, Gao Q, Duan XG, Yue G, Yang AF, Zhang JR (2006) Cloning of an H+-PPase gene from Thellungiella halophila and its heterologous expression to improve tobacco salt tolerance. J Exp Bot 57:3259–3270

Gao F, Zhou Y, Huang L, He D, Zhang G (2008) Proteomic analysis of long-term salinity stress-responsive proteins in Thellungiella halophila leaves. Chinese Sci Bull 53:3530–3537

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

Gaxiola RA, Rao R, Sherman A, Grisafi P, Alper SL, Fink GR (1999) The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1, can function in cation detoxification in yeast. Proc Natl Acad Sci USA 96:1480–1485

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

Gaxiola RA, Palmgren MG, Schumacher K (2007) Plant proton pumps. FEBS Lett 581:2204–2214

Genc Y, Oldach K, Verbyla A, Lott G, Hassan M, Tester M, Wallwork H, McDonald G (2010) Sodium exclusion QTL associated with improved seedling growth in bread wheat under salinity stress. Theor Appl Genet 121:877–894

Glenn EP, Brown JJ, Blumwald E (1999) Salt tolerance and crop potential of halophytes. Crit Rev Plant Sci 18:227–255

Gong QQ, Li PH, Ma SS, Rupassara SI, Bohnert HJ (2005) Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. Plant J 44:826–839

Gong HJ, Randall DP, Flowers TJ (2006) Silicon deposition in the root reduces sodium uptake in rice (Oryza sativa L.) seedlings by reducing bypass flow. Plant Cell Environ 29:1970–1979

Gouiaa S, Khoudi H, Leidi EO, Pardo JM, Masmoudi K (2012) Expression of wheat Na+/H+ antiporter TNHXS1 and H+- pyrophosphatase TVP1 genes in tobacco from a bicistronic transcriptional unit improves salt tolerance. Plant Mol Biol 79:137–155

Guan B, Hu Y, Zeng Y, Wang Y, Zhang F (2010) Molecular characterization and functional analysis of a vacuolar Na+/H+ antiporter gene (HcNHX1) from Halostachys caspica. Mol Biol Rep 38:1889–1899

Gunes A, Inal A, Bagci EG, Coban S (2007a) Silicon-mediated changes on some physiological and enzymatic parameters symptomatic of oxidative stress in barley grown in sodic-B toxic soil. J Plant Physiol 164:807–811

Gunes A, Inal A, Bagci EG, Pilbeam DJ (2007b) Silicon-mediated changes of some physiological and enzymatic parameters symptomatic for oxidative stress in spinach and tomato grown in sodic-B toxic soil. Plant Soil 290:103–114

Guo Y, Qiu QS, Quintero FJ, Pardo JM, Ohta M, Zhang C, Schumaker KS, Zhu JK (2004) Transgenic evaluation of activated mutant alleles of SOS2 reveals a critical requirement for its kinase activity and C-terminal regulatory domain for salt tolerance in Arabidopsis thaliana. Plant Cell 16:435–449

Guo SL, Yin HB, Zhang X, Zhao FY, Li PH, Chen SH, Zhao YX, Zhang H (2006) Molecular cloning and characterization of a vacuolar H+-pyrophosphatase gene, SsVP, from the halophyte Suaeda salsa and its overexpression increases salt and drought tolerance of Arabidopsis. Plant Mol Biol 60:41–50

Guo Q, Wang P, Ma Q, Zhang JL, Bao AK, Wang SM (2012) Selective transport capacity for K+ over Na+ is linked to the expression levels of PtSOS1 in halophyte Puccinellia tenuiflora. Funct Plant Biol 39:1047–1057

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

Hamada A, Shono M, Xia T, Ohta M, Hayashi Y, Tanaka A, Hayakawa T (2001) Isolation and characterization of a Na+/H+ antiporter gene from the halophyte Atriplex gmelini. Plant Mol Biol 46:35–42

Hassidim M, Braun Y, Lerner HR, Reinhold L (1990) Na+/H+ and K+/H+ antiport in root membrane-vesicles isolated from the halophyte Atriplex and the glycophyte cotton. Plant Physiol 94:1795–1801

He C, Yan J, Shen G, Fu L, 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

Hernández A, Jiang X, Cubero B, Nieto PM, Bressan RA, Hasegawa PM, Pardo JM (2009) Mutants of the Arabidopsis thaliana cation/H+ antiporter AtNHX1 conferring increased salt tolerance in yeast: the endosome/prevacuolar compartment is a target for salt toxicity. J Biol Chem 284:14276–14285

Hill AE, Hill BS (1976) Elimination processes by glands: mineral ions. In: Luttge U, Pitman MG (eds) Encyclopedia plant physiol new series 2B. Springer, Berlin, pp. 225–243

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

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

Horie T, Hauser F, Schroeder JI (2009) HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants. Trends Plant Sci 14:660–668

Huang S, 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

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

Ishitani M, Liu J, Halfter U, Kim CS, Shi W, Zhu JK (2000) SOS3 function in plant salt tolerance requires N-myristoylation and calcium binding. Plant Cell 12:1667–1678

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

James RA, Blake C, Byrt CS, Munns R (2011) Major genes for Na+ exclusion, Nax1 and Nax2 (wheat HKT1;4 and HKT1;5), decrease Na+ accumulation in bread wheat leaves under saline and waterlogged conditions. J Exp Bot 62:2939–2947

Janz D, Polle A (2012) Harnessing salt for woody biomass production. Tree Physiol 32:1–3

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

Jha A, Joshi M, Yadav N, Agarwal P, Jha B (2011) Cloning and characterization of the Salicornia brachiata Na+/H+ antiporter gene SbNHX1 and its expression by abiotic stress. Mol Biol Rep 38:1965–1973

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 57:4257–4268

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

Khoudi H, Maatar Y, Gouiaa S, Masmoudi K (2012) Transgenic tobacco plants expressing ectopically wheat H+-pyrophosphatase (H+-PPase) gene TaVP1 show enhanced accumulation and tolerance to cadmium. J Plant Physiol 169:98–103

Kobayashi H, Masaoka Y (2008) Salt secretion in Rhodes grass (Chloris gayana Kunth) under conditions of excess magnesium. Soil Sci Plant Nutr 54:393–399

Kobayashi S, Abe N, Yoshida K, Liu S, Takano T (2012) Molecular cloning and characterization of plasma membraneand vacuolar-type Na+/H+ antiporters of an alkaline-salt-tolerant monocot, Puccinellia tenuiflora. J Plant Res 125:587–594

Kramer D (1983) The possible role of transfer cells in the adaptation of plants to salinity. Physiol Plantarum 58:549–555

Krishnamurthy P, Ranathunge K, Franke R, Prakash H, Schreiber L, Mathew M (2009) The role of root apoplastic transport barriers in salt tolerance of rice (Oryza sativa L.). Planta 230:119–134

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, 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

Lerchl J, König S, Zrenner R, Sonnewald U (1995) Molecular cloning, characterization and expression analysis of isoforms encoding tonoplast-bound proton-translocating inorganic pyrophosphatase in tobacco. Plant Mol Biol 29:833–840

Li J, Yang H, Peer WA, Richter G, Blakeslee J, Bandyopadhyay A, Titapiwantakun B, Undurraga S, Khodakovskaya M, Richards EL, Krizek BA, Murphy AS, Gilroy S, Gaxiola RA (2005) Arabidopsis H+-PPase AVP1 regulates auxin-mediated organ development. Science 310:121–125

Li WY, Wong FL, Tsai SN, Phang TH, Shao GH, Lam HM (2006) Tonoplast-located GmCLC1 and GmNHX1 from soybean enhance NaCl tolerance in transgenic bright yellow (BY)-2 cells. Plant Cell Environ 29:1122–1137

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 Org 90:41–48

Li B, Wei A, Song C, Li N, Zhang JR (2008a) Heterologous expression of the TsVP gene improves the drought resistance of maize. Plant Biotechnol J 6:146–159

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

Li ZG, Baldwin M, Hu Q, Liu HB, Luo H (2010) Heterologous expression of Arabidopsis H+-pyrophosphatase enhances salt tolerance in transgenic creeping bentgrass (Agrostis stolonifera L.). Plant Cell Environ 33:272–289

Li W, Zhang C, Lu Q, Wen X, Lu C (2011) The combined effect of salt stress and heat shock on proteome profiling in Suaeda salsa. J Plant Physiol 168:1743–1752

Liang YC, Zhang WH, Chen Q, Ding RX (2005) Effects of silicon on H+-ATPase and H+-PPase activity, fatty acid composition and fluidity of tonoplast vesicles from roots of salt-stressed barley (Hordeum vulgare L.). Environ Exp Bot 53:29–37

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

Liphschitz N, Waisel Y (1974) Existence of salt glands in various genera of the Gramineae. New Phytol 73:507–513

Liphschitz N, Waisel Y (1982) Adaptation of plants to saline environments: salt excretion and glandular structure. In: Sen DN, Rajpurohit KS (eds) Tasks for vegetation science, contributions to the ecology of halophytes. Dr W Junk, The Hague, pp 197–214

Liphschitz N, Shomer-Ilan A, Eshel A, Waisel Y (1974) Salt glands on leaves of Rhodes grass (Chloris gayana Kth.). Ann Bot 38:459–462

Liu J, Zhu JK (1997) Proline accumulation and salt-stress-induced gene expression in a salt-hypersensitive mutant of Arabidopsis. Plant Physiol 114:591–596

Liu J, Zhu JK (1998) A calcium sensor homolog required for plant salt tolerance. Science 280:1943–1945

Liu J, Ishitani M, Halfter U, Kim CS, Zhu JK (2000) The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc Natl Acad Sci USA 97:3730–3734

Liu H, Zhang X, Takano T, Liu S (2009) Characterization of a PutCAX1 gene from Puccinellia tenuiflora that confers Ca2+ and Ba2+ tolerance in yeast. Biochem Biophys Res Commun 383:392–396

Liu SP, Zheng LQ, Xue YH, Zhang Q, Wang L, Shou HX (2010) Overexpression of OsVP1 and OsNHX1 increases tolerance to drought and salinity in rice. J Plant Biol 53:444–452

Liu L, Zeng Y, Pan X, Zhang F (2012) Isolation, molecular characterization, and functional analysis of the vacuolar Na+/H+ antiporter genes from the halophyte Karelinia caspica. Mol Biol Rep 39:7193–7202

Lu SY, Jing YX, Shen SH, Zhao HY, Ma LQ, Zhou XJ, Ren Q, Li YF (2005) Antiporter gene from Hordum brevisubulatum (Trin.) link and its overexpression in transgenic tobaccos. J Integr Plant Biol 47:343–349

Lü SY, Jing YX, Pang XB, Zhao HY, Ma LQ, Li YF (2005) cDNA cloning of a vacuolar H+-pyrophosphatase and its expression in Hordeum brevisubulatum (Trin.) link in response to salt stress. Agr Sci China 4:247–251

Lux A, Martinka M, Vaculik M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37

Lv SL, Zhang KW, Gao Q, Lian LJ, Song Y, Zhang J (2008) Overexpression of an H+-PPase gene from Thellungiella halophila (TsVP) in cotton enhances salt tolerance and improves growth and photosynthetic performance. Plant Cell Physiol 49:1150–1164

Lv SL, Lian LJ, Tao PL, Li ZX, Zhang KW, Zhang JR (2009) Overexpression of Thellungiella halophila H+-PPase (TsVP) in cotton enhances drought stress resistance of plants. Planta 229:899–910

Ma JF, Goto S, Tamai K, Ichii M (2001) Role of root hairs and lateral roots in silicon uptake by rice. Plant Physiol 127:1773–1780

Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M, Ishiguro M, Murata Y, Yano M (2006) A silicon transporter in rice. Nature 440:688–691

Ma JF, Yamaji N, Mitani N, Tamai K, Konishi S, Fujiwara T, Katsuhara M, Yano M (2007) An efflux transporter of silicon in rice. Nature 448:209–212

Ma Q, Yue LJ, Zhang JL, Wu GQ, Bao AK, Wang SM (2012) Sodium chloride improves photosynthesis and water status in the succulent xerophyte Zygophyllum xanthoxylum. Tree Physiol 32:4–13

Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158

Marcum KB (1999) Salinity tolerance mechanisms of grasses in the subfamily Chloridoideae. Crop Sci 39:1153–1160

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

Maruyama C, Tanaka Y, Takeyasu K, Yoshida M, Sato MH (1998) Structural studies of the vacuolar H+-pyrophosphatase: sequence analysis and identification of the residues modified by fluorescent cyclohexylcarbodiimide and maleimide. Plant Cell Physiol 39:1045–1053

Mäser P, Eckelman B, Vaidyanathan R, Horie T, Firbairn 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 AtHKT1. FEBS Lett 531:157–161

Matsushita N, Matoh T (1992) Function of the shoot base of salt-tolerant reed (Phragmites communis Trinius) Plants for Na+ exclusion from the shoots. Soil Sci Plant Nutr 38:565–571

McWhorter CG, Paul RN, Ouzts JC (1995) Bicellular trichomes of johnsongrass (Sorghum halepense) leaves: morphology, histochemistry, and function. Weed Sci 43:201–208

Mennen H, Jacoby B, Marschner H (1990) Is sodium proton antiport ubiquitous in plant cells. J Plant Physiol 137:180–183

Mian A, Oomen RJ, Isayenkov S, Sentenac H, Maathuis FJ, Véry AA (2011) Over-expression of an Na+- and K+-permeable HKT transporter in barley improves salt tolerance. Plant J 68:468–479

Miao BH, Han XG, Zhang WH (2010) The ameliorative effect of silicon on soybean seedlings grown in potassium-deficient medium. Ann Bot 105:967–973

Møller IS, Gilliham M, Jha D, Mayo GM, Roy SJ, Coates JC, Haseloff J, Tester M (2009) Shoot Na+ exclusion and increased salinity tolerance engineered by cell type-specific alteration of Na+ transport in Arabidopsis. Plant Cell 21:2163–2178

Mozafar A, Goodin JR (1970) Vesiculated hairs: a mechanism for salt tolerance in Atriplex halimus L. Plant Physiol 45:62–65

Munns R, Husain S, Rivelli AR, James RA, Condon AG, Lindsay MP, Lagudah ES, Schachtman DP, Hare RA (2002) Avenues for increasing salt tolerance of crops, and the role of physiologically based selection traits. Plant Soil 247:93–105

Munns R, James RA, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57:1025–1043

Munns R, James RA, Xu B, Athman A, Conn SJ, Jordans C, Byrt CS, Hare RA, Tyerman SD, Tester M, Plett D, Gilliham M (2012) Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene. Nat Biotechnol 30:360–364

Nah G, Pagliarulo CL, Mohr PG, Luo M, Sisneros N, Yu Y, Collura K, Currie J, Goicoechea JL, Wing RA, Schumaker KS (2009) Comparative sequence analysis of the salt overly sensitive1 orthologous region in Thellungiella halophila and Arabidopsis thaliana. Genomics 94:196–203

Naidoo G, Naidoo Y (1998) Salt tolerance in Sporobolus virginicus: the importance of ion relations and salt secretion. Flora 193:337–344

Naidoo G, Naidoo Y, Govender TG (1997) The role of salt secretion in salt tolerance in Sporobolus virginicus. Plant Physiol 114:306

Nakanishi Y, Maeshima M (1998) Molecular cloning of vacuolar H+-pyrophosphatase and its developmental expression in growing hypocotyl of mung bean. Plant Physiol 116:589–597

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 4:1484–1496

Oh DH, Leidi E, Zhang Q, Hwang SM, Li Y, Quintero FJ, Jiang X, D’Urzo MP, Lee SY, Zhao Y, Bahk JD, Bressan RA, Yun DJ, Pardo JM, Bohnert HJ (2009) Loss of halophytism by interference with SOS1 expression. Plant Physiol 151:210–222

Oh DH, Lee SY, Bressan RA, Yun DJ, Bohnert HJ (2010a) Intracellular consequences of SOS1 deficiency during salt stress. J Exp Bot 61:1205–1213

Oh DH, Dassanayake M, Haas JS, Kropornika A, Wright C, d’Urzo MP, Hong H, Ali S, Hernandez A, Lambert GM, Inan G, Galbraith DW, Bressan RA, Yun DJ, Zhu JK, Cheeseman JM, Bohnert HJ (2010b) Genome structures and halophyte-specific gene expression of the extremophile Thellungiella parvula in comparison with Thellungiella salsuginea (Thellungiella halophila) and Arabidopsis. Plant Physiol 154:1040–1052

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

Olías R, Eljakaoui Z, Li J, De Morales PA, 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

Pang Q, Chen S, Dai S, Chen Y, Wang Y, Yan X (2010) Comparative proteomics of salt tolerance in Arabidopsis thaliana and Thellungiella halophila. J Proteome Res 9:2584–2599

Pang Q, Guo J, Chen S, Chen Y, Zhang L, Fei M, Jin S, Li M, Wang Y, Yan X (2012) Effect of salt treatment on the glucosinolate-myrosinase system in Thellungiella salsuginea. Plant Soil 355:363–374

Pardo JM, Cubero B, Leidi EO, Quintero FJ (2006) Alkali cation exchangers: roles in cellular homeostasis and stress tolerance. J Exp Bot 57:1181–1199

Park S, Li J, Pittman JK, Berkowitz GA, Yang H, Undurraga S, Morris J, Hirschi KD, Gaxiola RA (2005) Up-regulation of a H+-pyrophosphatase (H+-PPase) as a strategy to engineer drought-resistant crop plants. Proc Natl Acad Sci USA 102:18830–18835

Parks GE, Dietrich MA, Schumaker KS (2002) Increased vacuolar Na+/H+ exchange activity in Salicornia bigelovii Torr. in response to NaCl. J Exp Bot 53:1055–1065

Pasapula V, Shen G, Kuppu S, Paez-Valencia J, Mendoza M, Hou P, Chen J, Qiu X, Zhu L, Zhang X, Auld D, Blumwald E, Zhang H, Gaxiola R, Payton P (2011) Expression of an Arabidopsis vacuolar H+-pyrophosphatase gene (AVP1) in cotton improves drought- and salt tolerance and increases fibre yield in the field conditions. Plant Biotechnol J 9:88–99

Pei L, Wang J, Li K, Li Y, Li B, Gao F, Yang A (2012) Overexpression of Thellungiella halophila H+-pyrophosphatase gene improves low phosphate tolerance in maize. PLOS One 7:e43501

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

Pollak G, Waisel Y (1970) Salt secretion in Aeluropus litoralis (Willd.) Parl. Ann Bot 34:879–888

Porat R, Pavoncello D, Ben-Hayyim G, Lurie S (2002) A heat treatment induced the expression of a Na+/H+ antiport gene (cNHX1) in citrus fruit. Plant Sci 162:957–963

Qiao WH, Zhao XY, Li W, Luo Y, Zhang XS (2007) Overexpression of AeNHX1, a root-specific vacuolar Na+/H+ antiporter from Agropyron elongatum, confers salt tolerance to Arabidopsis and Festuca plants. Plant Cell Rep 26:1663–1672

Qiu NW, Chen M, Guo JR, Bao HY, Ma XL, Wang BS (2007) Coordinate up-regulation of V-H+-ATPase and vacuolar Na+/H+ antiporter as a response to NaCl treatment in a C-3 halophyte Suaeda salsa. Plant Sci 172:1218–1225

Quintero FJ, Ohta M, Shi H, 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

Quintero FJ, Martinez-Atienza J, Villalta I, Jiang X, Kim WY, Ali Z, Fujii H, Mendoza I, Yun DJ, Zhu JK, Pardo JM (2011) Activation of the plasma membrane Na/H antiporter salt-overly-sensitive 1 (SOS1) by phosphorylation of an auto-inhibitory C-terminal domain. Proc Natl Acad Sci USA 108:2611–2616

Rahnama A, James RA, Poustini K, Munns R (2010) Stomatal conductance as a screen for osmotic stress tolerance in durum wheat growing in saline soil. Funct Plant Biol 37:255–263

Rajagopal D, Agarwal P, Tyagi W, Singla-Pareek SL, Reddy MK, Sopory SK (2007) Pennisetum glaucum Na+/H+ antiporter confers high level of salinity tolerance in transgenic Brassica juncea. Mol Breed 19:137–151

Ramadan T (1998) Ecophysiology of salt excretion in the xero-halophyte Reaumuria hirtella. New Phytol 139:273–281

Ramadan T (2001) Dynamics of salt secretion by Sporobolus spicatus (Vahl) Kunth from sites of differing salinity. Ann Bot 87:259–266

Ramati A, Liphschitz N, Waisel Y (1976) Ion localization and salt secretion in Sporobolus arenarius (Gou.) Duv-Jouv. New Phytol 76:289–294

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

Rodríguez-Rosales MP, Gálvez FJ, Huertas R, Aranda MN, Baghour M, Cagnac O, Venema K (2009) Plant NHX cation/proton antiporters. Plant Signal Behav 4:265–276

Rozema J, Gude H, Pollack G (1981) An ecophysical study of the salt secretion of four halophytes. New Phytol 89:207–217

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

Rus A, Lee BH, Muñoz-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

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 Genet 2:e210

Sakakibara Y, Kobayashi H, Kasamo K (1996) Isolation and characterization of cDNAs encoding vacuolar H+-pyrophosphates isoforms from rice (Oryza sativa L.). Plant Mol Biol 31:1029–1038

Sarafian V, Kim Y, Poole RJ, Rea PA (1992) Molecular cloning and sequence of cDNA encoding the pyrophosphate-energized vacuolar membrane proton pump of Arabidopsis thaliana. Proc Natl Acad Sci USA 89:1775–1779

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

Shabala S, Shabala S, Cuin TA, Pang J, Percey W, Chen Z, Conn S, Eing C, Wegner LH (2010) Xylem ionic relations and salinity tolerance in barley. Plant J 61:839–853

Shi H, Zhu JK (2002) Regulation of expression of the vacuolar Na+/H+ antiporter gene AtNHX1 by salt stress and abscisic acid. Plant Mol Biol 50:543–550

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 USA 97:6896–6901

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

Shi H, Lee BH, Wu SJ, Zhu JK (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol 21:81–85

Shi LY, Li HQ, Pan XP, Wu GJ, Li MR (2008) Improvement of Torenia fournieri salinity tolerance by expression of Arabidopsis AtNHX5. Funct Plant Biol 35:185–192

Sobrado MA (2004) Influence of external salinity on the osmolality of xylem sap, leaf tissue and leaf gland secretion of the mangrove Laguncularia racemosa (L.) Gaertn. Trees-Struct Funct 18:422–427

Sottosanto JB, Gelli A, Blumwald E (2004) DNA array analyses of Arabidopsis thaliana lacking a vacuolar Na+/H+ antiporter: impact of AtNHX1 on gene expression. Plant J 40:752–771

Stepien P, Johnson GN (2009) Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis and the halophyte Thellungiella: role of the plastid terminal oxidase as an alternative electron sink. Plant Physiol 149:1154–1165

Sun Z, Qi X, Li P, Wu C, Zhao Y, Zhang H, Wang Z (2008) Overexpression of a thellungiella halophila cbl9 homolog, thcbl9, confers salt and osmotic tolerances in transgenic Arabidopsis thaliana. J Plant Biol 51:25–34

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 to xylem parenchyma cells. Plant J 44:928–938

Taji T, Komatsu K, Katori T, Kawasaki Y, Sakata Y, Tanaka S, Kobayashi M, Toyoda A, Seki M, Shinozaki K (2010) Comparative genomic analysis of 1047 completely sequenced cDNAs from an Arabidopsis-related model halophyte Thellungiella halophila. BMC Plant Biol 10:261

Takahashi R, Liu S, Takano T (2007a) Cloning and functional comparison of a high-affinity K+ transporter gene PhaHKT1 of salt-tolerant and salt-sensitive reed plants. J Exp Bot 58:4387–4395

Takahashi R, Nishio T, Ichizen N, Takano T (2007b) Salt-tolerant reed plants contain lower Na+ and higher K+ than salt-sensitive reed plants. Acta Physiol Plant 29:431–438

Tanaka Y, Chiba K, Maeda M, Maeshima M (1993) Molecular cloning of cDNA for vacuolar membrane proton-translocating inorganic pyrophosphatase in Hordeum vulgare. Biochem Biophys Res Commun 190:1110–1114

Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 9:503–527

Tian LM, Huang CL, Yu R, Liang RF, Li ZL, Zhang LS, Wang YQ, Zhang XH, Wu ZY (2006) Overexpression AtNHX1 confers salt-tolerance of transgenic tall fescue. Afr J Biotechnol 5:1041–1044

Tuna AL, Kaya C, Higgs D, Murillo-Amador B, Aydemir S, Girgin AR (2008) Silicon improves salinity tolerance in wheat plants. Environ Exp Bot 62:10–16

Venema L, Quintero FJ, Pardo JM, Donaire JP (2002) The Arabidopsis Na+/H+ exchanger catalyzes low affinity Na+ and K+ transport in reconstituted vesicles. J Biol Chem 277:2413–2418

Verma D, Singla-Pareek SL, Rajagopal D, Reddy MK, Sopory SK (2007) Functional validation of a novel isoform of Na+/H+ antiporter from Pennisetum glaucum for enhancing salinity tolerance in rice. J Biosciences 32:621–628

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

Waisel Y (1991) The glands of Tamarix aphylla: a system for salt secretion or for carbon concentration. Physiol Plantarum 83:506–510

Waisel Y, Eshel A, Agami M (1986) Salt balance of leaves of the mangrove Avicennia marina. Physiol Plantarum 67:67–72

Wang XS, Han JG (2007) Effects of NaCl and silicon on ion distribution in the roots, shoots and leaves of two alfalfa cultivars with different salt tolerance. Soil Sci Plant Nutr 53:278–285

Wang TB, Gassmann W, Rubio F, Schroeder JI, Glass AD (1998) Rapid Up-regulation of HKT1, a high-affinity potassium transporter gene, in roots of barley and wheat following withdrawal of potassium. J Plant Physiol 118:651–659

Wang BS, Luttge U, Ratajczak R (2001) Effects of salt treatment and osmotic stress on V-ATPase and V- PPase in leaves of the halophyte Suaeda salsa. J Exp Bot 52:2355–2365

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

Wang J, Zuo KJ, Wu WS, Song J, Sun XF, Lin J, Li XF, Tang KX (2003) Molecular cloning and characterization of a new Na+/H+ antiporter gene from Brassica napus. DNA Seq 14:351–358

Wang J, Zuo K, Wu W, Song J, Sun X, Lin J, Li X, Tang K (2004a) Expression of a novel antiporter gene from Brassica napus resulted in enhanced salt tolerance in transgenic tobacco plants. Biol Plant 48:509–515

Wang SM, Wan CG, Wang YR, Chen H, Zhou ZY, Fu H, Sosebee RE (2004b) 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

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

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

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

Wang X, Yang R, Wang B, Liu G, Yang C, Cheng Y (2011) Functional characterization of a plasma membrane Na+/H+ antiporter from alkali grass (Puccinellia tenuiflora). Mol Biol Rep 38:4813–4822

Ward J (2001) Identification of novel families of membrane proteins from the model plant Arabidopsis thaliana. Bioinformatics 17:560–563

Watad AA, Pesci P, Reinhold L, Lerner HR (1986) Proton fluxes as a response to external salinity in wild type and NaCl-adapted Nicotiana cell lines. Plant Physiol 81:454–459

Wilson C, Shannon MC (1995) Salt-induced Na+/H+ antiport in root plasma membrane of a glycophytic and halophytic species of tomato. Plant Sci 107:147–157

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

Wu CA, Yang GD, Meng QW, Zheng CC (2004) The cotton GhNHX1 gene encoding a novel putative tonoplast Na+/H+ antiporter plays an important role in salt stress. Plant Cell Physiol 45:600–607

Wu YY, Chen QJ, Chen M, Chen J, Wang XC (2005) Salt-tolerant transgenic perennial ryegrass (Lolium perenne L.) obtained by Agrobacterium tumefaciens-mediated transformation of the vacuolar Na+/H+ antiporter gene. Plant Sci 169:65–73

Wu C, Gao X, Kong X, Zhao Y, Zhang H (2009) Molecular cloning and functional analysis of a Na+/H+ antiporter gene ThNHX1 from a halophytic plant Thellungiella halophila. Plant Mol Biol Rep 27:1–12

Wu GQ, Xi JJ, Wang Q, Bao AK, Ma Q, Zhang JL, Wang SM (2011) The ZxNHX gene encoding tonoplast Na+/H+ antiporter from the xerophyte Zygophyllum xanthoxylum plays important roles in response to salt and drought. J Plant Physiol 168:758–767

Wu HJ, Zhang Z, Wang JY, Oh DH, Dassanayake M, Liu B, Huang Q, Sun HX, Xia R, Wu Y, Wang YN, Yang Z, Liu Y, Zhang W, Zhang H, Chu J, Yan C, Fang S, Zhang J, Wang Y, Zhang F, Wang G, Lee SY, Cheeseman JM, Yang B, Li B, Min J, Yang L, Wang J, Chu C, Chen SY, Bohnert HJ, Zhu JK, Wang XJ, Xie Q (2012) Insights into salt tolerance from the genome of Thellungiella salsuginea. Proc Natl Acad Sci USA 109:12219–12224

Xia T, Apse MP, Aharon GS, Blumwald E (2002) Identification and characterization of a NaCl-inducible vacuolar Na+/H+ antiporter in Beta vulgaris. Physiol Plantarum 116:206–212

Xiong L, Zhu JK (2002) Salt tolerance. In: Somerville CR, Meyerowitz EM (eds) The Arabidopsis book. The American Society of Plant Biologists, Rockville, pp 1–23

Xu H, Jiang X, Zhan K, Cheng X, Chen X, Pardo JM, Cui D (2008) Functional characterization of a wheat plasma membrane Na+/H+ antiporter in yeast. Arch Biochem Biophys 473:8–15

Xue ZY, Zhi DY, Xue G, Zhang H, Zhao Y, Xia G (2004) Enhanced salt tolerance of transgenic wheat (Tritivum aestivum L.) expressing a vacuolar Na+/H+ antiporter gene with improved grain yields in saline soils in the field and a reduced level of leaf Na+. Plant Sci 167:849–859

Yamaguchi T, Fukuda-Tanaka S, Inagaki Y, Saito N, Yonekura-Sakakibara K, Tanaka Y, Kusumi T, Iida S (2001) Genes encoding the vacuolar Na+/H+ exchanger and flower coloration. Plant Cell Physiol 142:451–461

Yamaguchi T, Aharon GS, Sottosanto JB, Blumwald E (2005) Vacuolar Na+/H+ antiporter cation selectivity is regulated by calmodulin from within the vacuole in a Ca2+- and pH-dependent manner. Proc Natl Acad Sci USA 102:16107–16112

Yang QC, Wu MS, Wang PQ, Kang JM, Zhou XL (2005) Cloning and expression analysis of a vacuolar Na+/H+ antiporter gene from Alfalfa. DNA Seq 16:352–357

Yang H, Knapp J, Koirala P, Rajagopal D, Peer WA, Silbart LK, Murphy A, Gaxiola RA (2007) Enhanced phosphorus nutrition in monocots and dicots over-expressing a phosphorus-responsive type I H+-pyrophosphatase. J Plant Biotechnol 5:735–745

Yao M, Zeng Y, Liu L, Huang Y, Zhao E, Zhang F (2012) Overexpression of the halophyte Kalidium foliatum H+-pyrophosphatase gene confers salt and drought tolerance in Arabidopsis thaliana. Mol Biol Rep 39:7989–7996

Ye CY, Zhang HC, Chen JH, Xia XL, Yin WL (2009) Molecular characterization of putative vacuolar NHX-type Na+/H+ exchanger genes from the salt-resistant tree Populus euphratica. Physiol Plantarum 137:166–174

Yeo A (1998) Molecular biology of salt tolerance in the context of whole-plant physiology. J Exp Bot 49:915–929

Yeo AR, Läuchli A, Kramer D (1977) Ion measurements by X-ray microanalysis in unfixed, frozen, hydrated plant cells of species differing in salt tolerance. Planta 134:35–38

Yeo AR, Flowers SA, Rao G, Welfare K, Senanayake N, Flowers TJ (1999) Silicon reduces sodium uptake in rice (Oryza sativa L.) in saline conditions and this is accounted for by a reduction in the transpirational bypass flow. Plant Cell Environ 22:559–565

Yin XY, Yang AF, Zhang KW, Zhang JR (2004) Production and analysis of transgenic maize with improved salt tolerance by the introduction of AtNHX1 gene. Acta Bot Sin 46:854–861

Yu JN, Huang J, Wang ZM, Zhang JS, Chen SY (2007) An Na+/H+ antiporter gene from wheat plays an important role in stress tolerance. J Biosci 32:1153–1161

Yu J, Chen S, Zhao Q, Wang T, Yang C, Diaz C, Sun G, Dai S (2011) Physiological and proteomic analysis of salinity tolerance in Puccinellia tenuiflora. J Proteome Res 10:3852–3870

Yue LJ, Li SX, Ma Q, Zhou XR, Wu GQ, Bao AK, Zhang JL, Wang SM (2012) NaCl stimulates growth and alleviates water stress in the xerophyte Zygophyllum xanthoxylum. J Arid Environ 87:153–160

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

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

Zhang QF, Li YY, Pang CH, Lu CM, Wang BS (2005) NaCl enhances thylakoid-bound SOD activity in the leaves of C-3 halophyte Suaeda salsa L. Plant Sci 168:423–430

Zhang H, Shen G, Kuppu S, Gaxiola R, Payton P (2011) Creating drought- and salt-tolerant cotton by overexpressing a vacuolar pyrophosphatase gene. Plant Signal Behav 6:861–863

Zhang YM, Liu ZH, Wen ZY, Zhang HM, Yang F, Guo XL (2012) The vacuolar Na+-H+ antiport gene TaNHX2 confers salt tolerance on transgenic alfalfa (Medicago sativa). Funct Plant Biol 39:708–716

Zhao FY, Zhang XJ, Li PH, Zhao YX, Zhang H (2006) Co-expression of the Suaeda salsa SsNHX1 and Arabidopsis AVP1 confer greater salt tolerance to transgenic rice than the single SsNHX1. Mol Breeding 17:341–353

Zhu JK (2001) Cell signaling under salt, water and cold stresses. Curr Opin Plant Biol 4:401–406

Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445

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

Zhu ZJ, Wei GQ, Li J, Qian QQ, Yu JQ (2004) Silicon alleviates salt stress and increases antioxidant enzymes activity in leaves of salt-stressed cucumber (Cucumis sativus L.). Plant Sci 167:527–533

Zorb C, Noll A, Karl S, Leib K, Yan F, Schubert S (2005) Molecular characterization of Na+/H+ antiporters (ZmNHX) of maize (Zea mays L.) and their expression under salt stress. J Plant Physiol 162:55–66