Trends in genetic engineering of plants with (Na⁺/H⁺) antiporters for salt stress tolerance

References

• Munns R. Genes and salt tolerance: bringing them together. New Phytol. 2005;167:645–663.
   PubMed Web of Science ®Google Scholar
• Chinnusamy V, Jagendorf A, Zhu JK. Understanding and improving salt tolerance in plants. Crop Sci. 2005;45:437–448.
   Web of Science ®Google Scholar
• Flowers TJ, Yeo AR. Breeding for salinity resistance in crop plants-where next? Aus J Plant Physiol. 1995;22:875–884.
   Google Scholar
• Vinocur B, Altman A. Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol. 2005;16:123–132.
   PubMed Web of Science ®Google Scholar
• Wang WX, Vinocur B, Shoseyov O, et al. Biotechnology of plant osmotic stress tolerance: physiological and molecular considerations. Acta Hortic. 2001;560:285–292.
   Google Scholar
• Tester M, Davenport R. Na+ tolerance and Na+ transport in higher plants. Ann Bot. 2003;91:503–527.
   PubMed Web of Science ®Google Scholar
• Sun J, Chen SL, Dai SX, et al. Ion flux profiles and plant ion homeostasis control under salt stress. Plant Signal Behav. 2009;4:261–264.
   PubMedGoogle Scholar
• Blumwald E. Sodium transport and salt tolerance in plants. Curr Opin Cell Biol. 2000;12:431–434.
   PubMed Web of Science ®Google Scholar
• Hasegawa PM, Bressan RA, Zhu JK, et al. Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol. 2000;51:463–499.
   PubMed Web of Science ®Google Scholar
• Khan MA, Duke NC. Halophytes – a resource for the future. Wetlands Ecol Manag. 2001;9:455–456.
   Google Scholar
• Shi H, Lee BH, Wu SJ, et al. Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol. 2002;21:81–85.
   Google Scholar
• Rus A, Lee BH, Munoz-Mayor A, et al. AtHKT1 facilitates Na+ homeostasis and K+ nutrition in planta. Plant Physiol. 2004;136:2500–2511.
   PubMed Web of Science ®Google Scholar
• Pardo JM, Cubero B, Leidi EO, et al. Alkali cation exchangers: roles in cellular homeostasis and stress tolerance. J Exp Bot. 2006;57:1181–1199.
   PubMed Web of Science ®Google Scholar
• Fukuda A, Nakamura A, Tanaka Y. Molecular cloning and expression of the Na+/H+ exchanger gene in Oryza sativa. Biochim Biophys Acta. 1999;1446:149–155.
   PubMed Web of Science ®Google Scholar
• Chauhan S, Forsthoefel N, Ran Y, et al. Na+/myo-inositol symporters and Na+/H+-antiport in Mesembryanthemum crystallinum. Plant J. 2000;24:511–522.
   PubMed Web of Science ®Google Scholar
• Shi H, Ishitani M, Kim C, et al. The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA. 2000;97:6896–6901.
   PubMed Web of Science ®Google Scholar
• Yokoi S, Quintero FJ, Cubero B, et al. Differential expression and function of Arabidopsis thaliana NHX Na+/H+ antiporters in the salt stress response. Plant J. 2002;30:529–539.
   PubMed Web of Science ®Google Scholar
• Yoshida K. Plant biotechnology – genetic engineering to enhance plant salt tolerance. J Biosci Bioeng. 2002;94:585–590.
   PubMed Web of Science ®Google Scholar
• Ashraf M, Akram NA. Improving salinity tolerance of plants through conventional breeding and genetic engineering: an analytical comparison. Biotechnol Adv. 2009;27:744–752.
   PubMed Web of Science ®Google Scholar
• Khan MS, Ahmad D, Khan MA. Utilization of genes encoding osmoprotectants in transgenic plants for enhanced abiotic stress tolerance. Electron J Biotechnol. Forthcoming 2015. Available from: http://dx.doi.org/10.1016/j.ejbt.2015.04.002.
   Google Scholar
• Liu J, Ishitani M, Halfter U, et al. The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc Natl Acad Sci USA. 2000;97:3730–3734.
   PubMed Web of Science ®Google Scholar
• Liu J, Zhu JK. A calcium sensor homolog required for plant salt tolerance. Science. 1998;280:1943–1945.
   PubMed Web of Science ®Google Scholar
• Wu SJ, Ding L, Zhu JK. SOS1, a genetic locus essential for salt tolerance and potassium acquisition. Plant Cell. 1996;8:617–627.
   PubMed Web of Science ®Google Scholar
• Liu JP, Zhu JK. An Arabidopsis mutant that requires increased calcium for potassium nutrition and salt tolerance. Proc Natl Acad Sci USA. 1997;94:14960–14964.
   PubMed Web of Science ®Google Scholar
• Zhu JK, Liu J, Xiong L. Genetic analysis of salt tolerance in Arabidopsis: evidence for a critical role of potassium nutrition. Plant Cell. 1998;10:1181–1191.
   PubMed Web of Science ®Google Scholar
• Zhu JK. Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol. 2000;124:941–948.
   PubMed Web of Science ®Google Scholar
• Higinbotham N. Electropotentials of plant cells. Annu Rev Plant Physiol Plant Mol Biol. 1973;24:25–46.
   Web of Science ®Google Scholar
• Apse MP, Blumwald E. Na+ transport in plants. FEBS Lett. 2007;581:2247–2254.
   PubMed Web of Science ®Google Scholar
• Garciadeblas B, Senn ME, Banuelos MA, et al. Sodium transport and HKT transporters: the rice model. Plant J. 2003;34:788–801.
   PubMed Web of Science ®Google Scholar
• Essah PA, Davenport R, Tester M. Sodium influx and accumulation in Arabidopsis. Plant Physiol. 2003;133:307–318.
   PubMed Web of Science ®Google Scholar
• Kader MA, Seidel T, Golldack D, et al. Expressions of OsHKT1, OsHKT2 and OsVHA are differently regulated under NaCl stress in salt-sensitive and salt-tolerant rice (Oryza sativa L.) cultivars. J Exp Bot. 2006;57:4257–4268.
   PubMed Web of Science ®Google Scholar
• Møller IS, Gilliham M, Jha D, et al. Shoot Na+ exclusion and increased salinity tolerance engineered by cell type-specific alteration of Na+ transport in Arabidopsis. Plant Cell. 2009;21:2163–2178.
   PubMed Web of Science ®Google Scholar
• Schachtman DP, Kumar R, Schroeder JI, et al. Molecular and functional characterization of a novel low affinity cation transporter (LCT1) in higher plants. Proc Natl Acad Sci USA. 1997;94:11079–11084.
   PubMed Web of Science ®Google Scholar
• Amtmann A, Fischer M, Marsh EL, et al. The wheat cDNA LCT1 generates hypersensitivity to sodium in a salt sensitive yeast strain. Plant Physiol. 2001;126:1061–1071.
   PubMed Web of Science ®Google Scholar
• Leng Q, Mercier RW, Hua BG, et al. Electrophysiological analysis of cloned cyclic nucleotide-gated ion channels. Plant Physiol. 2002;128:400–410.
   PubMed Web of Science ®Google Scholar
• Demidchik V, Essah PA, Tester M. Glutamate activates cation currents in the plasma membrane of Arabidopsis root cells. Planta. 2004;219:167–175.
   PubMed Web of Science ®Google Scholar
• Balague C, Lin B, Alcon C, et al. HLM1, an essential signaling component in the hypersensitive response, is a member of the cyclic nucleotide-gated channel family. Plant Cell. 2003;15:365–379.
   PubMed Web of Science ®Google Scholar
• Gobert A, Park G, Amtmann A, et al. Arabidopsis thaliana cyclic nucleotide gated channel 3 forms a non-selective ion transporter involved in germination and cation transport. J Exp Bot. 2006;57:791–800.
   PubMed Web of Science ®Google Scholar
• Li X, Borsics T, Harrington HM, et al. Arabidopsis AtCNGC10 rescues potassium channel mutants of E. coli, yeast and Arabidopsis and is regulated by calcium/calmodulin and cyclic GMP in E. coli. Funct Plant Biol. 2005;32:643–653.
   Web of Science ®Google Scholar
• Horie T, Schroeder JI. Sodium transporters in plants. Diverse genes and physiological functions. Plant Physiol. 2004;136:2457–2462.
   PubMed Web of Science ®Google Scholar
• Sze H, Padmanaban S, Cellier F, et al. Expression patterns of a novel AtCHX gene family highlight potential roles in osmotic adjustment and K+ homeostasis in pollen development. Plant Physiol. 2004;136:2532–2547.
   PubMed Web of Science ®Google Scholar
• An R, Chen QJ, Chai MF, et al. AtNHX8, a member of the monovalent cation: proton antiporter-1 family in Arabidopsis thaliana, encodes a putative Li+/H+ antiporter. Plant J. 2007;49:718–728.
   PubMed Web of Science ®Google Scholar
• Qiu QS, Barkla BJ, Vera-Estrella R, et al. Na+/H+ exchange activity in the plasma membrane of Arabidopsis. Plant Physiol. 2003;132:1041–1052.
   PubMed Web of Science ®Google Scholar
• Apse MP, Blumwald E. Engineering salt tolerance in plants. Curr Opin Biotechnol. 2002;13:146–150.
   PubMed Web of Science ®Google Scholar
• Gaxiola RA, Rao R, Sherman A, et al. The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1, can function in cation detoxification in yeast. Proc Natl Acad Sci USA. 1999;96:1480–1485.
   PubMed Web of Science ®Google Scholar
• Li HT, Liu H, Gao XH, et al. Knock-out of Arabidopsis AtNHX4 gene enhances tolerance to salt stress. Biochem Biophys Res Commun. 2009;382:637–641.
   PubMed Web of Science ®Google Scholar
• Khan MS. Role of sodium and hydrogen (Na+/H+) antiporters in salt tolerance of plants: present and future challenges. Afr J Biotechnol. 2011;10:13693–13704.
   Web of Science ®Google Scholar
• Brini F, Hanin M, Mezghani I, et al. Overexpression of wheat Na+/H+ antiporter TNHX1 and H+-pyrophosphatase TVP1 improve salt and drought stress tolerance in Arabidopsis thaliana plants. J Exp Bot. 2006;58:301–308.
   Web of Science ®Google Scholar
• Li J, Jiang G, Huang P, et al. Overexpression of the Na+/H+ antiporter gene from Suaeda salsa confers cold and salt tolerance to transgenic Arabidopsis thaliana. Plant Cell Tissue Organ Cult. 2007;90:41–48.
   Web of Science ®Google Scholar
• An BY, Luo Y, Li JR, et al. Expression of a vacuolar Na+/H+ antiporter gene of alfalfa enhances salinity tolerance in transgenic Arabidopsis. Acta Agron Sin. 2008;34:557–564.
   Google Scholar
• Zhang HX, Hodson JN, Williams JP, et al. 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. 2001;98:12832–12836.
   PubMed Web of Science ®Google Scholar
• Liu H, Wang Q, Yu M, et al. Transgenic salt-tolerant sugar beet (Beta vulgaris L.) constitutively expressing an Arabidopsis thaliana vacuolar Na+/H+ antiporter gene, AtNHX3, accumulates more soluble sugar but less salt in storage roots. Plant Cell Environ. 2008;31:1325–1334.
   PubMed Web of Science ®Google Scholar
• Wu CA, Yang GD, Meng QW, et al. The cotton GhNHX1 gene encoding a novel putative tonoplast Na+/H+ antiporter plays an important role in salt stress. Plant Cell Physiol. 2004;45:600–607.
   PubMed Web of Science ®Google Scholar
• Wang J, Zuo K, Wu W, et al. Expression of a novel antiporter gene from Brassica napus resulted in enhanced salt tolerance in transgenic tobacco plants. Biol Plant. 2004;48:509–515.
   Web of Science ®Google Scholar
• Lu SY, Jing YX, Shen SH, et al. Antiporter gene from Hordeum brevisubulatum (Trin.) link and its overexpression in transgenic tobaccos. J Integr Plant Biol. 2005;47:343–349.
   Web of Science ®Google Scholar
• Hossain GS, Waditee R, Hibino T, et al. Root specific expression of Na+/H+ antiporter gene from Synechocystis sp. PCC 6803 confers salt tolerance of tobacco plant. Plant Biotechnol. 2006;23:275–281.
   Google Scholar
• Soliman MH, Omar HS, El-Awady MA, et al. Transformation and expression of Na+/H+ antiporter vacuolar (AtNHX1) gene in tobacco plants under salt stress. Arab J Biotechnol. 2009;12:99–108.
   Google Scholar
• Zhang GH, Su Q, An LJ, et al. Characterization and expression of a vacuolar Na+/H+ antiporter gene from the monocot halophyte Aeluropus littoralis. Plant Physiol Biochem. 2008;46:117–126.
   PubMed Web of Science ®Google Scholar
• Ohta M, Hayashi Y, Nakashima A, et al. Introduction of a Na+/H+ antiporter gene from Atriplex gmelini confers salt tolerance to rice. FEBS Lett. 2002;532:279–282.
   PubMed Web of Science ®Google Scholar
• Fukuda A, Nakamura A, Tagiri A, et al. Function, intracellular localization and the importance in salt tolerance of a vacuolar Na+/H+ antiporter from rice. Plant Cell Physiol. 2004;45:146–159.
   PubMed Web of Science ®Google Scholar
• Chen H, An R, Tang JH, et al. Over-expression of a vacuolar Na+/H+ antiporter gene improves salt tolerance in an upland rice. Mol Breed. 2007;19:215–225.
   Web of Science ®Google Scholar
• Verma D, Singla-Pareek SL, Rajagopal D, et al. Functional validation of a novel isoform of Na+/H+ antiporter from Pennisetum glaucum for enhancing salinity tolerance in rice. J Biosci. 2007;32:621–628.
   PubMed Web of Science ®Google Scholar
• Wu LM, Chen W, Zhao Y, et al. Salt tolerance enhancement of transgenic rice with Na+/H+ antiporter gene driven by root specific promoter PmPgPR10. Res Papers. 2012;26:643–650.
   Google Scholar
• Xue ZY, Zhi DY, Xue GP, et al. 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. 2004;167:849–859.
   Web of Science ®Google Scholar
• Yin XY, Yang AF, Zhang KW, et al. Production and analysis of transgenic maize with improved salt tolerance by the introduction of AtNHX1 gene. Acta Bot Sin. 2004;7:12–20.
   Google Scholar
• Chen M, Chen QJ, Niu XG, et al. Expression of OsNHX1 gene in maize confers salt tolerance and promotes plant growth in the field. Plant Soil Environ. 2007;53:490–498.
   Web of Science ®Google Scholar
• Gisbert C, Rus AM, Boların MC, et al. The yeast HAL1 gene improves salt tolerance of transgenic tomato. Plant Physiol. 2000;123:393–402.
   PubMed Web of Science ®Google Scholar
• Sondergaard TE, Schulz A, Palmgren MG. Energization of transport processes in plants. Roles of the plasma membrane H+-ATPase. Plant Physiol. 2004;136:2475–2482.
   PubMed Web of Science ®Google Scholar
• Gaxiola RA, Li S, Undurraga S, et al. Drought- and salt-tolerant plants result from overexpression of the AVP1 H+-pump. Proc Natl Acad Sci USA. 2001;98:11444–11449.
   PubMed Web of Science ®Google Scholar
• Park S, Li J, Pittman JK, et al. Up-regulation of a H+-pyrophosphatase (H+-PPase) as a strategy to engineer drought-resistant crop plants. Proc Natl Acad Sci USA. 2005;102:18830–18835.
   PubMed Web of Science ®Google Scholar
• He C, Yan J, Shen G, et al. 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. 2005;46:1848–1854.
   PubMed Web of Science ®Google Scholar
• Pasapula V, Shen G, Kuppu S, et al. 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. 2011;9:88–99.
   PubMed Web of Science ®Google Scholar
• Rodríguez-Rosales MP, Jiang X, Gálvez FJ, et al. Overexpression of the tomato K+/H+ antiporter LeNHX2 confers salt tolerance by improving potassium compartmentalization. New Phytol. 2008;179:366–377.
   PubMed Web of Science ®Google Scholar
• Liu P, Yang GD, Li H, et al. Overexpression of NHX1s in transgenic Arabidopsis enhances photoprotection capacity in high salinity and drought conditions. Acta Physiol Plant. 2010;32:81–90.
   Web of Science ®Google Scholar
• Rajagopal D, Agarwal P, Tyagi W, et al. Pennisetum glaucum Na+/H+ antiporter confers high level of salinity tolerance in transgenic Brassica juncea. Mol Breed. 2007;19:137–151.
   Web of Science ®Google Scholar
• Jha B, Mishra A, Jha A, et al. Developing transgenic jatropha using the SbNHX1 gene from an extreme halophyte for cultivation in saline wasteland. PLoS One. 2013;8:e71136.
   PubMed Web of Science ®Google Scholar
• Zhang YM, Liu ZH, Wen ZY, et al. The vacuolar Na+/H+ antiport gene TaNHX2 confers salt tolerance on transgenic alfalfa (Medicago sativa). Funct Plant Biol. 2012;39:708–716.
   Web of Science ®Google Scholar
• Yadav NS, Shukla PS, Jha A, et al. The SbSOS1 gene from the extreme halophyte Salicornia brachiata enhances Na+ loading in xylem and confers salt tolerance in transgenic tobacco. BMC Plant Biol. 2012;12:188.
   PubMed Web of Science ®Google Scholar
• Xu K, Hong P, Luo L, et al. Overexpression of AtNHX1, a vacuolar Na+/H+ antiporter from Arabidopsis thaliana, in Petunia hybrida enhances salt and drought tolerance. J Plant Biol. 2009;52:453–461.
   Web of Science ®Google Scholar
• Zhao J, Zhi D, Xue Z, et al. Enhanced salt tolerance of transgenic progeny of tall fescue (Festuca arundinacea) expressing a vacuolar Na+/H+ antiporter gene from Arabidopsis. J Plant Physiol. 2007;164:1377–1383.
   PubMed Web of Science ®Google Scholar
• OGTR: risk assessment and risk management plan for DIR 102/2010: limited and controlled release of wheat and barley genetically modified for abiotic stress tolerance. The University of Adelaide. 2010 Apr. Available from: http://www.ogtr.gov.au.
   Google Scholar
• Rudelsheim PLJ, Smets G. Anticipating the environmental risk assessment of crops modified to enhance or preserve yield. COGEM Report CGM 2010-05. Available from: http://www.cogem.net/index.cfm/en/publications/categorie/research-reports.
   Google Scholar
• Xu K, Zhang H, Blumwald E, et al. A novel plant vacuolar Na+/H+ antiporter gene evolved by DNA shuffling confers improved salt tolerance in yeast. J Biol Chem. 2010;285:22999–23006.
   PubMed Web of Science ®Google Scholar
• Khan MS. The role of DREB transcription factors in abiotic stress tolerance of plants. Biotechnol Biotechnol Equip. 2011;25(3):2433–2442.
   Web of Science ®Google Scholar
• Khan MS, Yu X, Kikuchi A, et al. Genetic engineering of glycine betaine biosynthesis to enhance abiotic stress tolerance in plants. Plant Biotechnol. 2009;26:125–134.
   Web of Science ®Google Scholar
• Bassil E, Coku A, Blumwald E. Cellular ion homeostasis: emerging roles of intracellular NHX Na+/H+ antiportes in plant growth and development. J Exp Bot. 2012;63:5727–5740.
   PubMed Web of Science ®Google Scholar
• Bassil E, Ohto MA, Esumi T, et al. The Arabidopsis intracellular Na+/H+ antiporters NHX5 and NHX6 are endosome associated and necessary for plant growth and development. Plant Cell. 2011;23:224–239.
   PubMed Web of Science ®Google Scholar
• Bassil E, Tajima H, Liang YC, et al. The Arabidopsis Na+/H+ antiporters NHX1 and NHX2 control vacuolar pH and K+ homeostasis to regulate growth, flower development, and reproduction. Plant Cell. 2011;23:3482–3497.
   PubMed Web of Science ®Google Scholar
• Shabala S. Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Ann Bot. 2013;112:1209–1221.
   PubMed Web of Science ®Google Scholar