Selective transport capacity for K+ over Na+ is linked to the expression levels of PtSOS1 in halophyte Puccinellia tenuiflora
Qiang Guo A B , Pei Wang A B , Qing Ma A , Jin-Lin Zhang A , Ai-Ke Bao A and Suo-Min Wang A C
+ Author Affiliations
- Author Affiliations
A State Key Laboratory of Grassland Agro-ecosystems, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, PR China.
B These authors have contributed equally to this work.
C Corresponding author. Email: smwang@lzu.edu.cn
Functional Plant Biology 39(12) 1047-1057 https://doi.org/10.1071/FP12174
Submitted: 15 June 2012 Accepted: 19 August 2012 Published: 24 January 2012
Abstract
The plasma membrane Na+/H+ antiporter (SOS1) was shown to be a Na+ efflux protein and also involved in K+ uptake and transport. PtSOS1 was characterised from Puccinellia tenuiflora (Griseb.) Scribn. et Merr., a monocotyledonous halophyte that has a high selectivity for K+ over Na+ by roots under salt stress. To assess the contribution of PtSOS1 to the selectivity for K+ over Na+, the expression levels of PtSOS1 and Na+, K+ accumulations in P. tenuiflora exposed to different concentrations of NaCl, KCl or NaCl plus KCl were analysed. Results showed that the expression levels of PtSOS1 in roots increased significantly with the increase of external NaCl (25–150 mM), accompanied by an increase of selective transport (ST) capacity for K+ over Na+ by roots. Transcription levels of PtSOS1 in roots and ST values increased under 0.1–1 mM KCl, then declined sharply under 5–10 mM KCl. Under 150 mM NaCl, PtSOS1 expression levels in roots and ST values at 0.1 mM KCl was significantly lower than that at 5 mM KCl with the prolonging of treatment time. A significant positive correlation was found between root PtSOS1 expression levels and ST values under various concentrations of NaCl, KCl or 150 mM NaCl plus 0.1 or 5 mM KCl treatments. Therefore, it is proposed that PtSOS1 is the major component of selective transport capacity for K+ over Na+ and hence, salt tolerance of P. tenuiflora. Finally, we hypothesise a function model of SOS1 in regulating K+ and Na+ transport system in the membrane of xylem parenchyma cells by sustaining the membrane integrity; it also appears that this model could reasonably explain the phenomenon of Na+ retrieval from the xylem when plants are exposed to severe salt stress.
Additional keywords: K+, Na+, plasma membrane Na+/H+ antiporter, salt tolerance.
References
Amtmann A (2009) Learning from evolution: Thellungiella generates new knowledge on essential and critical components of abiotic stress tolerance in plants. Molecular Plant 2, 3–12.| Learning from evolution: Thellungiella generates new knowledge on essential and critical components of abiotic stress tolerance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovV2msbk%3D&md5=caaa0b670a94e03607038abb047f22f6CAS |
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 Science 176, 232–240.
| Overexpression of the Arabidopsis H+-PPase enhanced resistance to salt and drought stress in transgenic alfalfa (Medicago sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFagtbvN&md5=4d5b531a5ccd49247c3e769fa9f53a50CAS |
Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. Biochimica et Biophysica Acta 1465, 140–151.
| Sodium transport in plant cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXit1Wgtrs%3D&md5=ae76c7b66bf582f7e33a8bb7f922d29fCAS |
Brett CL, Donowitz M, Rao R (2005) Evolutionary origins of eukaryotic sodium/proton exchangers. American Journal of Physiology. Cell Physiology 288, C223–C239.
| Evolutionary origins of eukaryotic sodium/proton exchangers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhsVCks70%3D&md5=91aab1897de7db99e814042ae98abc47CAS |
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 Physiology 143, 1918–1928.
| HKT1;5-like cation transporters linked to Na+ exclusion loci in wheat, Nax2 and Kna1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksFWjurs%3D&md5=f0f7213246aef9707915ba9c62365e47CAS |
Chen J, Xiao Q, Wu FH, Dong XJ, He JX, Pei ZM, Zheng HL (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 Physiology 30, 1570–1585.
| 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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvVyiug%3D%3D&md5=80f78e58bc6b7d4ba2d559f19af2fdf0CAS |
Chomczynski P, Sacchi N (1987) Single step method of RNA isolation by acid guanidinium thiocynate-phenol-chloroform extraction. Analytical Biochemistry 162, 156–159.
| Single step method of RNA isolation by acid guanidinium thiocynate-phenol-chloroform extraction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXitFSns7Y%3D&md5=f34f7799c0f2cbd069f6f6b1ee6cc279CAS |
Clarkson DT, Hanson JB (1980) The mineral nutrition of higher plants. Annual Review of Plant Biology 31, 239–298.
Cosentino C, Fischer-Schliebs E, Bertl A, Thiel G, Homann U (2010) Na+/H+ antiporters are differentially regulated in response to NaCl stress in leaves and roots of Mesembryanthemum crystallinum. New Phytologist 186, 669–680.
| Na+/H+ antiporters are differentially regulated in response to NaCl stress in leaves and roots of Mesembryanthemum crystallinum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnsVejt7s%3D&md5=037fa4f19907c23e1ca5c7345b78fde7CAS |
Cuin TA, Bose J, Stefano G, Jha D, Tester M, Mancuso S, Shabala S (2011) Assessing the role of root plasma membrane and tonoplast Na+/H+ exchangers in salinity tolerance in wheat: in planta quantification methods. Plant, Cell & Environment 34, 947–961.
| Assessing the role of root plasma membrane and tonoplast Na+/H+ exchangers in salinity tolerance in wheat: in planta quantification methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXos1Sgtbw%3D&md5=0bf364eccc98d80c9e39bd8497c7d4e4CAS |
Demidchik V, Cuin TA, Svistunenko D, Smith SJ, Miller AJ, Shabala S, Sokolik A, Yurin V (2010) Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. Journal of Cell Science 123, 1468–1479.
| Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnt1KmtL0%3D&md5=9760101d29a57e595ee89346dec09645CAS |
Donaldson L, Ludidi N, Knight MR, Gehring C, Denby K (2004) Salt and osmotic stress cause rapid increases in Arabidopsis thaliana cGMP levels. FEBS Letters 569, 317–320.
| Salt and osmotic stress cause rapid increases in Arabidopsis thaliana cGMP levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlt1amu7g%3D&md5=112e6f7f51b70c01f08751c432383dbbCAS |
Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytologist 179, 945–963.
| Salinity tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWqur%2FE&md5=72b4deb297e7aba3822bd35460a0cbe9CAS |
Flowers TJ, Yeo AR (1995) Breeding for salinity resistance in crop plants: where next? Australian Journal of Plant Physiology 22, 875–884.
| Breeding for salinity resistance in crop plants: where next?Crossref | GoogleScholarGoogle Scholar |
Garciadeblás B, Haro R, Benito B (2007) Cloning of two SOS1 transporters from the seagrass Cymodocea nodosa. SOS1 transporters from Cymodocea and Arabidopsis mediate potassium uptake in bacteria. Plant Molecular Biology 63, 479–490.
| Cloning of two SOS1 transporters from the seagrass Cymodocea nodosa. SOS1 transporters from Cymodocea and Arabidopsis mediate potassium uptake in bacteria.Crossref | GoogleScholarGoogle Scholar |
Gaymard F, Pilot G, Lacombe B, Bouchez D, Bruneau D, Boucherez J, Michaux-Ferriere N, Thibaud JB, Sentenac H (1998) Identification and disruption of a plant shaker-like outward channel involved in K+ release into the xylem sap. Cell 94, 647–655.
| Identification and disruption of a plant shaker-like outward channel involved in K+ release into the xylem sap.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmtVWksrs%3D&md5=a27b1401c17d354c675922892ec15219CAS |
Guo KM, Babourina O, Rengel Z (2009) Na+/H+ antiporter activity of the SOS1 gene: lifetime imaging analysis and electrophysiological studies on Arabidopsis seedlings. Physiologia Plantarum 137, 155–165.
| Na+/H+ antiporter activity of the SOS1 gene: lifetime imaging analysis and electrophysiological studies on Arabidopsis seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtF2qs7jF&md5=55a696a87e19afd2981950716d5af150CAS |
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 & Environment 33, 552–565.
| 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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXltV2hurY%3D&md5=f2fcd0ef7f68d02ec06ec4ec8198e33cCAS |
Horie T, Hauser F, Schroeder JI (2009) HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants. Trends in Plant Science 14, 660–668.
| HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsV2mtr7J&md5=8b5093747e84e25562335820492a11a6CAS |
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. Proceedings of the National Academy of Sciences of the United States of America 103, 18816–18821.
| The plasma membrane Na+/H+ antiporter SOS1 interacts with RCD1 and functions in oxidative stress tolerance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlahtbzF&md5=9c837304f9c60d8cc082a6bf07cd32a7CAS |
Kinclová O, Ramos J, Potier S, Sychrová H (2001) Functional study of the Saccharomyces cerevisiae Nha1p C-terminus. Molecular Microbiology 40, 656–668.
| Functional study of the Saccharomyces cerevisiae Nha1p C-terminus.Crossref | GoogleScholarGoogle Scholar |
Kronzucker HJ, Britto DT (2011) Sodium transport in plants: a critical review. New Phytologist 189, 54–81.
| Sodium transport in plants: a critical review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltlGhug%3D%3D&md5=2cc2408d47529fcd441cdde872cd9c02CAS |
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 Physiology 32, 4–13.
| Sodium chloride improves photosynthesis and water status in the succulent xerophyte Zygophyllum xanthoxylum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjsVCmt7Y%3D&md5=55013dc4800a754c35c16b041d26322bCAS |
Maathuis FJ (2006) cGMP modulates gene transcription and cation transport in Arabidopsis roots. The Plant Journal 45, 700–711.
| cGMP modulates gene transcription and cation transport in Arabidopsis roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjt1SjtrY%3D&md5=3fc8f933d864e56d422601482c0e611bCAS |
Maathuis FJM, Sanders D (2001) Sodium uptake in Arabidopsis roots is regulated by cyclic nucleotides. Plant Physiology 127, 1617–1625.
| Sodium uptake in Arabidopsis roots is regulated by cyclic nucleotides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtVWmsw%3D%3D&md5=04312724d9b9033f0f969cde2ca4e04aCAS |
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 Physiology 143, 1001–1012.
| Conservation of the salt overly sensitive pathway in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhvFWnt7s%3D&md5=9c35dc5b14fe7410f7ab984079987736CAS |
Maughan PJ, Turner TB, Coleman CE (2009) Characterization of salt overly sensitive 1 (SOS1) gene homoeologs in quinoa (Chenopodium quinoa Willd.). Genome 52, 647–657.
| Characterization of salt overly sensitive 1 (SOS1) gene homoeologs in quinoa (Chenopodium quinoa Willd.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVSjsrvM&md5=4fb54fadfddb8a10f04162296f72269cCAS |
Niu X, Bressan RA, Hasegawa PM, Pardo JM (1995) Ion homeostasis in NaCl stress environments. Plant Physiology 109, 735–742.
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. Journal of Integrative Plant Biology 49, 1484–1496.
| Sodium stress in the halophyte Thellungiella halophila and transcriptional changes in a thsos1-RNA interference line.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1WmsrzI&md5=5d99e0836e13844272d975d0b5504ac7CAS |
Oh DH, Leidi E, Zhang Q, Li YZ, Ma WY, Yun DJ, Bressan RA, Bohnert HJ (2009) Loss of halophytism by interference with SOS1 expression. Plant Physiology 151, 210–222.
| Loss of halophytism by interference with SOS1 expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFOjsbzL&md5=6c379f595dba9f2868e46abe7d9ad0b6CAS |
Oh DH, Lee SY, Bressan RA, Yun DJ, Bohnert HJ (2010) Intracellular consequences of SOS1 deficiency during salt stress. Journal of Experimental Botany 61, 1205–1213.
| Intracellular consequences of SOS1 deficiency during salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXis1Wnsbo%3D&md5=317477c036d58e3e03b970b6706093b7CAS |
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 & Environment 32, 904–916.
| The plasma membrane Na+/H+ antiporter SOS1 is essential for salt tolerance in tomato and affects the partitioning of Na+ between plant organs.Crossref | GoogleScholarGoogle Scholar |
Pardo JM, Cubero B, Leidi EO, Quintero FJ (2006) Alkali cation exchangers: roles in cellular homeostasis and stress tolerance. Journal of Experimental Botany 57, 1181–1199.
| Alkali cation exchangers: roles in cellular homeostasis and stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1Gls78%3D&md5=6555c7c2c3eb973656c90dc74cfe27ffCAS |
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+. Journal of Experimental Botany 55, 939–949.
| Alkali grass resists salt stress through high [K+] and an endodermis barrier to Na+.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXisF2ls7Y%3D&md5=0eee95b67bca84c3d44722c46b3a1c33CAS |
Qi Z, Spalding EP (2004) Protection of plasma membrane K+ transport by the salt overlay sensitive Na+/H+ antiporter during salinity stress. Plant Physiology 136, 2548–2555.
| Protection of plasma membrane K+ transport by the salt overlay sensitive Na+/H+ antiporter during salinity stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvFOruro%3D&md5=b6993a57942ca3b3b7fcec48aa41d7acCAS |
Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proceedings of the National Academy of Sciences of the United States of America 99, 8436–8441.
| Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvVGntrg%3D&md5=a333a77ef895f268299b27efbda1bbd2CAS |
Quintero FJ, Ohta M, Shi H, Zhu JK, Pardo JM (2002) Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis. Proceedings of the National Academy of Sciences of the United States of America 99, 9061–9066.
| Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltF2hu70%3D&md5=d961ef19936db53173b6440b633e9112CAS |
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. Nature Genetics 37, 1141–1146.
| A rice quantitative trait locus for salt tolerance encodes a sodium transporter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVCntL%2FJ&md5=8d06ab35399af7295afd1fdee45197a4CAS |
Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogentic trees. Molecular Biology and Evolution 4, 406–425.
Shabala L, Cuin TA, Newman IA, Shabala S (2005) Salinity induced ion flux patterns from the excised roots of Arabidopsis sos mutants. Planta 222, 1041–1050.
| Salinity induced ion flux patterns from the excised roots of Arabidopsis sos mutants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Gqsr7O&md5=5ca185a6b887f05bd0f473db8805661cCAS |
Shabala S, Shabala S, Cuin TA, Pang JY, Percey W, Chen ZH, Conn S, Eing C, Wegner LH (2010) Xylem ionic relations and salinity tolerance in barley. The Plant Journal 61, 839–853.
| Xylem ionic relations and salinity tolerance in barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjsFaktr0%3D&md5=d91727639c8e29c8d35bced6c22bcb27CAS |
Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proceedings of the National Academy of Sciences of the United States of America 97, 6896–6901.
| The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktFahtrs%3D&md5=b9467cede7bb4ca2a98b16c9c16e4573CAS |
Shi H, Quintero FJ, Pardo JM, Zhu JK (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. The Plant Cell 14, 465–477.
| The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XisVKgur0%3D&md5=b9e79961135fe6e6169000e386c1056cCAS |
Shi H, Lee BH, Wu SJ, Zhu JK (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nature Biotechnology 21, 81–85.
| Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhvVyr&md5=7ef8ea2024ada988af65931f119612cfCAS |
Sunarpi HT, Motoda J, Kubo M, Yang H, Yoda K, Horie R, Chan WY, Leung HY, Hattori K, Konomi M, Osumi M, Yamagami M, Schroeder JI, Uozumi N (2005) Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na+ unloading from xylem vessels to xylem parenchyma cells. The Plant Journal 44, 928–938.
| Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na+ unloading from xylem vessels to xylem parenchyma cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjslGlsw%3D%3D&md5=4544d7cc5a0a2e8ac45aea020ff220e8CAS |
Takahashi R, Liu SK, Takano T (2009) Isolation and characterization of plasma membrane Na+/H+ antiporter genes from salt-sensitive and salt-tolerant reed plants. Journal of Plant Physiology 166, 301–309.
| Isolation and characterization of plasma membrane Na+/H+ antiporter genes from salt-sensitive and salt-tolerant reed plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitV2lu74%3D&md5=489694ab92f1d0e7b2cc552183e7e2baCAS |
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599.
| MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVGrsL8%3D&md5=172d8627ecb5a96c5c6c395d1a5ce15aCAS |
Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Annals of Botany 91, 503–527.
| Na+ tolerance and Na+ transport in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjsVyisbk%3D&md5=74c60da106de125747711c854ea8fcabCAS |
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.
| The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntFyntQ%3D%3D&md5=a0c7e54e30d37bd2fa3a93d66e591a25CAS |
Wang SM, Zhao GQ, Gao YS, Tang ZC, Zhang CL (2005) Puccinellia tenuiflora exhibits stronger selectivity for K+ over Na+ than wheat. Journal of Plant Nutrition 27, 1841–1857.
| Puccinellia tenuiflora exhibits stronger selectivity for K+ over Na+ than wheat.Crossref | GoogleScholarGoogle Scholar |
Wang SM, Zhang JL, Flowers TJ (2007) Low affinity Na+ uptake in the halophyte Suaeda maritima. Plant Physiology 145, 559–571.
| Low affinity Na+ uptake in the halophyte Suaeda maritima.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1SjsLvP&md5=72f0543cd795f5055279bb3826f9924fCAS |
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 & Environment 32, 486–496.
| Puccinellia tenuiflora maintains a low Na+ level under salinity by limiting unidirectional Na+ influx resulting in a high selectivity for K+ over Na+.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvVantbk%3D&md5=9d1dce159d283eecec9c3cd64f04d611CAS |
Wang X, Yang R, Wang BC, Liu GF, Yang CP, Cheng YX (2011) Functional characterization of a plasma membrane Na+/H+ antiporter from alkali grass (Puccinellia tenuiflora). Molecular Biology Reports 38, 4813–4822.
| Functional characterization of a plasma membrane Na+/H+ antiporter from alkali grass (Puccinellia tenuiflora).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtV2htb%2FN&md5=2e747820c9aded07060e85aef95538bbCAS |
Wegner LH, De Boer AH (1997) Properties of two outward rectifying channels in root xylem parenchyma cells suggest a role in K+ homeostasis and long-distance signaling. Plant Physiology 115, 1707–1719.
Wegner LH, Raschke K (1994) Ion channels in the xylem parenchyma of barley roots. Plant Physiology 105, 799–813.
Wu SJ, Ding L, Zhu JK (1996) SOS1, a genetic locus essential for salt tolerance and potassium acquisition. The Plant Cell 8, 617–627.
Wu YS, Ding N, Zhao X, Zhao MG, Chang ZQ, Liu JQ, Zhang LX (2007) Molecular characterization of PeSOS1: the putative Na+/H+ antiporter of Populus euphratica. Plant Molecular Biology 65, 1–11.
| Molecular characterization of PeSOS1: the putative Na+/H+ antiporter of Populus euphratica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXovFSqsrk%3D&md5=ff8a93071fdfe7f4dbe0300edd1519e6CAS |
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. Journal of Plant Physiology 168, 758–767.
| The ZxNHX gene encoding tonoplast Na+/H+ antiporter from the xerophyte Zygophyllum xanthoxylum plays important roles in response to salt and drought.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXktFKjt7o%3D&md5=a8f2d1c94f668e54d60d06bdfcf4bc60CAS |
Xu HX, Jiang XY, Zhan KH, Cheng XY, Cheng XJ, Pardo JM, Cui D (2008) Functional characterization of a wheat plasma membrane Na+/H+ antiporter in yeast. Archives of Biochemistry and Biophysics 473, 8–15.
| Functional characterization of a wheat plasma membrane Na+/H+ antiporter in yeast.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksleisL0%3D&md5=b5d14e93480c15d69cbc4fded63565adCAS |
Zhang JL, Flowers TJ, Wang SM (2010) Mechanisms of sodium uptake by roots of higher plants. Plant and Soil 326, 45–60.
| Mechanisms of sodium uptake by roots of higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFGrt7vO&md5=5b3062a5bf96ff732befeb90ddd4b616CAS |
Zhu JK (2003) Regulation of ion homeostasis under salt stress. Current Opinion in Plant Biology 6, 441–445.
| Regulation of ion homeostasis under salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntVKhsbs%3D&md5=27b752d80d81bec98f48487722232aa1CAS |
Zhu JK, Liu J, Xiong L (1998) Genetic analysis of salt tolerance in Arabidopsis: evidence for a role of potassium nutrition. The Plant Cell 10, 1181–1191.
