Skip to main content
Log in

Developing salt tolerant plants in a new century: a molecular biology approach

  • Published:
Plant Cell, Tissue and Organ Culture Aims and scope Submit manuscript

Abstract

Soil salinity is a major abiotic stress in plant agriculture strongly, influencing plant productivity world-wide. Classical breeding for salt tolerance in crop plants has been attempted to improve field performance without success. Therefore, an alternative strategy is to generate salt tolerant plants through genetic engineering. Several species and experimental approaches have been used in order to identify those genes that are important for salt tolerance. Due to high level of salt tolerance, halophytes are good candidates to identify salt tolerance genes. However, other species such as yeast and glycophytes have also been employed. Three approaches are commonly used to identify genes important for salt tolerance. The first approach is to identify genes involved in processes known to be critical for salt tolerance (osmolyte synthesis, ion homeostasis, etc.). The second approach is to identify genes whose expression is regulated by salt stress. This is relatively simply and applicable to any plant species. Genetic amenability of some species allows the third approach, which consists in the identification of salt tolerance determinants based on functionality. At the moment, there is a large number of reports in the literature claiming that plants with increased salt tolerance have been obtained. The main problem is that different plant species, stage of development, organs, promoters and salt conditions used it is difficult to compare the degree of salt tolerance conferred by different genes. In this review, we discuss progress made towards understanding the molecular elements involved in salt stress responses that have been used in transgenic approaches to improve salt tolerance.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Albert A, Martinez-Ripoll M, Espinosa-Ruiz A, Yenush L, Culianez-Macia FA & Serrano R (2000) The X-ray structure of the FMN-binding protein AtHal3 provides the structural basis for the activity of a regulatory subunit involved in signal transduction. Struct. Fold Design 8: 961-969

    Google Scholar 

  • Allen R (1995) Dissection of oxidative stress tolerance using transgenic plants. Plant Physiol. 107: 1049-1054

    Google Scholar 

  • Amaya I, Botella MA, de la Calle M, Medina MI, Heredia A, Bressan RA, Hasegawa PM, Quesada MA & Valpuesta V(1999) Improved germination under osmotic stress of tobacco plants overexpressing a cell wall peroxidase. FEBS Lett. 457: 80-84

    Google Scholar 

  • Apse MP, Aharon GS, Snedden WA & Blumwald E (1999) Salt 1 1 tolerance conferred by overexpression of a vacuolar Na /H antiport in Arabidopsis. Science 285: 1256-1258

    Google Scholar 

  • Ashraf M (1999) Breeding for salinity tolerance proteins in plants. Crit. Rev. Plant Sci. 13: 17-42

    Google Scholar 

  • Bajaj S, Targoli J, Liu L-F, Ho TH & Wu R (1999) Transgenic approaches to increase dehydration-stress in plants. Mol. Breed. 5: 493-503

    Google Scholar 

  • Bohnert H, Ayoubi P, Borchert C, Bressan R, Burnap R, Cushman JC, Cushman MA, Deyholos M, Fisher R, Galbraith D, Hasegawa P, Jenks M, Kawasaki S, Koiwa H, Kore-eda S, Lee B-H, Michalowski C, Misawa E, Nomura M, Ozturk N, Postier B, Prad RCPS, Tanaka Y, Wang H & J-K Z (2001) A genomics approach towards salt stress tolerance. Plant Physiol. Biochem. 39: 295-311

    Google Scholar 

  • Bohnert H, Nelson D & Jensen R (1995) Adaptations to environmental stresses. Plant Cell 7: 1099-1111

    Google Scholar 

  • Bhora JS, Döoffling H & Döoffling K (1995) Salinity tolerance of rice with reference to endogenous and exogenous abscised acid. J. Agron. Crop. Sci. 174: 79-86

    Google Scholar 

  • Bordas M, Montesinos C, Dabauza M, Salvador A, Roig LA, Serrano R & Moreno V(1997) Transfer of the yeast salt tolerance gene HAL1 to Cucumis melo L. cultivars and in vitro evaluation of salt tolerance. Trans. Res. 6: 41-50

    Google Scholar 

  • Borsani O, Cuartero J, Fernandez JA, Valpuesta V & Botella MA (2001a) Identification of two loci in tomato reveals distinct mechanisms for salt tolerance. Plant Cell 13: 873-888

    Google Scholar 

  • Borsani O, Valpuesta V & Botella MA (2001b) Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol. 126: 1024-1030

    Google Scholar 

  • Boston R, Viitanen P & Vierling E (1996) Molecular chaperones and protein folding in plants. Plant Mol. Biol. 32: 191-222

    Google Scholar 

  • Botella MA, Quesada MA, Kononowicz AK, Bressan RA, Pliego F, Hasegawa PM & Valpuesta V (1994) Characterization and in situ localization of a salt-induced tomato peroxidase mRNA. Plant Mol. Biol. 25: 105-140

    Google Scholar 

  • Bray EA (1993) Molecular responses to water deficit. Plant Physiol. 103: 1035-1040

    Google Scholar 

  • Bressan RA, Zhang C, Zhang H, Hasegawa PM, Bohnert HJ & Zhu J-K (2001) Learning from the Arabidopsis experience. The next gene search paradigm. Plant Physiol. 127: 1354-1360

    Google Scholar 

  • Brewster JL, de Valoir T, Dwyer ND, Winter E & Gustin MC (1993) An osmosensing signal transduction pathway in yeast. Science 259: 1760-1763

    Google Scholar 

  • Cuartero J, Yeo AR & Flowers TJ (1992) Selection of donors for salt-tolerance in tomato using physiological traits. New Phytol. 121: 63-69

    Google Scholar 

  • Cuartero J & Fernandez-Muñoz R (1999) Tomato and salinity. Sci. Hort. 78: 83-125

    Google Scholar 

  • Espartero J, Sanchez-Aguayo I & Pardo JM (1995) Molecular characterization of glyoxalase-I from a higher plant; upregulation by stress. Plant Mol. Biol. 29: 1223-1233

    Google Scholar 

  • Flowers T, Troke P & Yeo A (1977) The mechanism of salt tolerance in halophytes. Ann. Rev. Plant Physiol. 28: 89-121

    Google Scholar 

  • Flowers TJ, Koyama ML, Flowers SA, Chinta Sudhakar KP, Shing KP & Yeo AR (2000) QTL: their place in enginnering tolerance of rice to salinity. J. Exp. Bot. 51: 99-106

    Google Scholar 

  • Foolad MR & Lin GY (1997) Genetic potential for salt tolerance during germination in Lycopersicon species. HortScience 32: 296-300

    Google Scholar 

  • Foyer C, Lelandais M, G alap C & Kunert K (1991) Effects of elevated cytosolic glutathione reductase activity on cellular glutathione pool and photosynthesis in leaves under normal and stress conditions. Plant Physiol. 97:863-872

    Google Scholar 

  • Foyer C, Descourvieres P & Kunert K (1994) Protection against oxygen radicals: an important defense mechanism studied in transgenic plants. Plant Cell Environ. 17: 507-523

    Google Scholar 

  • Frandsen G, Muller-Uri F, Nielsen M, Mundy J & Skriver K (1996) Novel plant Ca(21)-binding protein expressed in response to abscisic acid and osmotic stress. J. Biol. Chem. 271: 343-348

    Google Scholar 

  • Fukushima E, Arata Y, Endo T, Sonnewald U & Sato F (2001) Improved salt tolerance of transgenic tobacco expressing apoplastic yeast-derived invertase. Plant Cell Physiol. 42: 245-249

    Google Scholar 

  • Gisbert C, Rus AM, Bolarin MC, Lopez-Coronado JM, Arrillaga I, Montesinos C, Caro M, Serrano R & Moreno V(2000) The yeast HAL 1 gene improves salt tolerance of transgenic tomato. Plant Physiol. 123: 393-402

    Google Scholar 

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

    Google Scholar 

  • Gosti F, Beaudoin N, Serizet C, Webb AA, Vartanian N & Giraudat J (1999) ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signaling. Plant Cell 11: 1897-1910

    Google Scholar 

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

    Google Scholar 

  • Hanson A & Hitz W(1982) Metabolics responses of mesophytes to plant water deficits. Ann. Rev. Plant Physiol. 33: 163-203

    Google Scholar 

  • Hare PD, Cress WA & Van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ. 21: 535-554

    Google Scholar 

  • Hasegawa M, Bressan R & Pardo JM (2000a) The dawn of plant salt tolerance genetics. Trends Plant Sci. 5: 317-319

    Google Scholar 

  • Hasegawa M, Bressan R, Zhu J-K & Bhonert H (2000b) Plant cellular and molecular responses to high salinity. Ann. Rev. Plant Physiol. 51: 493-499

    Google Scholar 

  • Hayashi H, Alia Mustardy L, Deshnium P, Ida M & Murata N (1997) Transformation of Arabidopsis thaliana with the codA gene for choline oxidase; accumulation of glycinebetaine and enhanced tolerance to salt and cold stress. Plant J. 12: 133-142

    Google Scholar 

  • Hirayama T, Ohto C, Mizoguchi T & Shinozaki K (1995) A gene encoding a phosphatidylinositol-specific phospholipase C is induced by dehydration and salt stress in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 92: 3903-3907

    Google Scholar 

  • Holmstrom KO, Somersalo S, Mandal A, Palva TE & Welin B (2000) Improved tolerance to salinity and low temperature in transgenic tobacco producing glycine betaine. J. Exp. Bot. 51: 177-185

    Google Scholar 

  • Hong B, Barg R & Ho TH (1992) Developmental and organspecific expression of an ABA-and stress-induced protein in barley. Plant Mol. Biol. 18: 663-674

    Google Scholar 

  • Hoshida H, Tanaka Y, Hibino T, Hayashi Y, Tanaka A & Takabe T (2000) Enhanced tolerance to salt stress in transgenic rice that overexpresses chloroplast glutamine synthetase. Plant Mol. Biol. 43: 103-111

    Google Scholar 

  • Huang J, Hirji R, Adam L, Rozwadowski KL, Hammerlindl JK, Keller WA & Selvaraj G (2000) Genetic engineering of muglycinebetaine production toward enhancing stress tolerance in plants: metabolic limitations. Plant Physiol. 122: 747-756

    Google Scholar 

  • Ichimura K, Mizoguchi T, Irie K, Morris P, Giraudat J, Matsumoto K & Shinozaki K (1998) Isolation of ATMEKK1 (a MAP kinase kinase kinase)-interacting proteins and analysis of a MAP kinase cascade in Arabidopsis. Biochem. Biophys. Res. Commun. 253: 532-543

    Google Scholar 

  • Ingram J & Bartels D (1996) The molecular basis of dehydration tolerance in plants. Ann. Rev. Plant Physiol. Plant Mol. Biol. 47: 377-403

    Google Scholar 

  • Iraki N, Bressan R, Hasegawa P & Carpita N (1989) Alteration of physical and chemical structure of the primary cell wall of growth-limited plant cells adapted to osmotic stress. Plant Physiol. 91: 29-47

    Google Scholar 

  • Ishitani M, Xiong L, Stevenson B & Zhu JK (1997) Genetic analysis of osmotic and cold stress signal transduction in Arabidopsis: interactions and convergence of abscisic acid-dependent and abscisic acid-independent pathways. Plant Cell 9: 1935-1949

    Google Scholar 

  • Johnson D, Smith S & Dobrenz A (1992) Genetic and phenotypic relationships in response to NaCl at different developmental stages in alfalfa. Theor. Appl. Gen. 83: 833-838

    Google Scholar 

  • Jones RA (1986) High salt tolerance potential in Lycopersicon species during germination. Euphytica 35: 575-582

    Google Scholar 

  • Karakas B, Ozias-Akins P, Stushnoff C, Suefferheld M & Rieger M (1997) Salinity and drought tolerance of mannitol-accumulating transgenic tobacco. Plant Cell Environ. 20: 609-616

    Google Scholar 

  • Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K & Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat. Biotechnol. 17: 287-291

    Google Scholar 

  • Kishor PB, Hong Z, Miao GH, Hu CA & Verma DP (1995) Overexpression of D1-pyrroline-5-carboxylase synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol. 108: 1387-1394

    Google Scholar 

  • Klee C, Draetta M & Hubbard M (1988) Calcineurin. Adv. Enzymol. 61: 149-200

    Google Scholar 

  • Koornneef M, Leon-Kloosterziel KM, Scwartz SH & Zeevart JAD (1998) The genetic and molecular dissection of abscisic acid biosynthesis and signal transduction in Arabidopsis. Plant Physiol. Biochem. 36: 83-89

    Google Scholar 

  • Kudla J, Xu Q, Harter K, Gruissem W & Luan S (1999) Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals. Proc. Natl. Acad. Sci. USA 96: 4718-4723

    Google Scholar 

  • Lauchli A & Epstein E (1990) Plant responses to saline and sodic conditions. In: Tanji, KK (eds) Agricultural salinity assessment and management (pp. 113-137). Amer. Soc. Civil Eng., New York

    Google Scholar 

  • Leung J, Bouvier-Durand M, Morris PC, Guerrier D, Chefdor F & Giraudat J (1994) Arabidopsis ABA response gene ABI 1: features of a calcium-modulated protein phosphatase. Science 264: 1448-1452

    Google Scholar 

  • Liang Z, Ma D, Tang L, Hong Y, Luo A, Zhou J & Dai X (1997) Expression of the spinach betaine aldehyde dehydrogenase (BADH) gene in transgenic tobacco plants. Chin. J. Biotechnol. 13: 153-159

    Google Scholar 

  • Lilius G, Holmberg N & Bulow L (1996) Enhanced NaCl stress tolerance in transgenic tobacco expressing bacterial choline dehydrogenase. Biotechnology 14: 177-180

    Google Scholar 

  • Lippuner V, Cyert MS & Gasser CS (1996) Two classes of plant cDNA clones differentially complement yeast calcineurin mutants and increase salt tolerance of wild-type yeast. J. Biol. Chem. 271: 12859-12866

    Google Scholar 

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

    Google Scholar 

  • Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K & Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought-and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10: 1391-1406

    Google Scholar 

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

    Google Scholar 

  • Liu J, Ishitani M, Halfter U, Kim CS & Zhu JK (2000) The Arabidopsis thaliana SOS 2gene encodes a protein kinase that is required for salt tolerance. Proc. Natl. Acad. Sci. USA 97: 3730- 3734

    Google Scholar 

  • Lynch TJ, Polito L & Lauchli A (1989) Salinity stress increases 21 cytoplasmic Ca activity in maize root protoplast. Plant Physiol. 90: 1271-1274

    Google Scholar 

  • Luan S, Li W, Rusnak F, Assmann SM & Schreiber SL (1993) Immunosuppressants implicate protein phosphatase-regulation of 1 K+ channels in guard cells. Proc. Natl. Acad. Sci. USA 90: 2202-2206

    Google Scholar 

  • Maeda T, Wurgler-Murphy SM & Saito H (1994) A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369: 242-245

    Google Scholar 

  • Maeda T, Takekawa M & Saito H (1995) Activation of yeast PBS2 MAPKK by MAPKKKs or by binding of an SH3-containing osmosensor. Science 269: 554-558

    Google Scholar 

  • McCourt P (1999) Genetic analysis of hormone signaling. Ann. Rev. Plant Physiol. Plant Mol. Biol. 50: 219-243

    Google Scholar 

  • Mendoza I, Rubio F, Rodriguez-Navarro A & Pardo JM (1994) The protein phosphatase calcineurin is essential for NaCl tolerance of Saccharomyces cerevisiae. J. Biol. Chem. 269: 8792-8796

    Google Scholar 

  • Meyer K, Leube MP & Grill E (1994) A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science 264: 1452-1455

    Google Scholar 

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

    Google Scholar 

  • Murguia JR, Belles JM & Serrano R (1995) A salt-sensitive 3' (2'),5'-bisphosphate nucleotidase involved in sulfate activation. Science 267: 232-234

    Google Scholar 

  • Nakamura T, Liu Y, Hirata D, Namba H, Harada S, Hirokawa T & Miyakawa T (1993) Protein phosphatase type 2B (calcineurin)mediated, FK506-sensitive regulation of intracellular ions in yeast is an important determinant for adaptation to high salt stress conditions. EMBO J. 12: 4063-4071

    Google Scholar 

  • Nanjo T, Kobayashi M, Yoshiba Y, Kakubari Y, Yamaguchi-Shinozaki K & Shinozaki K (1999) Antisense suppression of proline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana. FEBS Lett. 461:205-210

    Google Scholar 

  • Narasimhan M, Bizel ML, Perez-Prat E, Chen Z, Nelson DE, Shing NK, Bressan RA & Hasegawa PM (1991) NaCl regulation of tonoplast ATPase 70-kilodalton subunit meseger RNA in tobacco cells. Plant Physiol. 97: 562-568

    Google Scholar 

  • Niu X, Bressan RA, Hasegawa PM & Pardo JM (1995) Ion homeostasis in NaCl stress enviroments. Plant Physiol. 109: 735-742

    Google Scholar 

  • Osmond C & Grace S (1995) Perspectives on photoinhibition and photorespiration in the field: quintessential inefficiencies of the light and dark reactions of photosynthesis? J. Exp. Bot. 46: 1351-1362

    Google Scholar 

  • Pardo JM, Reddy MP, Yang S, Maggio A, Huh GH, Matsumoto T, Coca MA, Paino-D'Urzo M, Koiwa H, Yun DJ, Watad AA, Bressan RA & Hasegawa PM (1998) Stress signaling through 21 Ca2+ /calmodulin-dependent protein phosphatase calcineurin mediates salt adaptation in plants. Proc. Natl. Acad. Sci. USA 95: 9681-9686

    Google Scholar 

  • Piao HL, Pih KT, Lim JH, Kang SG, Jin JB, Kim SH & Hwang I (1999) An Arabidopsis GSK 3/shaggy-like gene that complements yeast salt stress-sensitive mutants is induced by NaCl and abscisic acid. Plant Physiol. 119: 1527-1534

    Google Scholar 

  • Pilon-Smits E, Terry N, Sears T, Kim H, Zayed A, Hwang S, Van Dun K, Voodg E, Verwoerd T, Krutwagen R & Goddijn O (1998) Trehalose-producing transgenic tobacco plants show improved growth performance under drought stress. J. Plant Physiol. 152: 525-532

    Google Scholar 

  • Polle A (1997) Defense against photoxidative damage in plants. In: Scandalios, JG (ed) Oxidative stress and molecular biology of antioxidants defences (pp. 623-666). Cold Spring Harbor Laboratories

  • Popping B, Gibbons T & Watson MD (1996) The Pisum sativum MAP kinase homologue (PsMAPK) rescues the Saccharomyces cerevisiae hog1 deletion mutant under conditions of high osmotic stress. Plant Mol. Biol. 31: 355-363

    Google Scholar 

  • Price A & Hendry G (1991) Iron-catalyzed oxygen radical formation and its possible contribution to drought damage in nine native grasses and three cereals. Plant Cell Environ. 14: 477-484

    Google Scholar 

  • Quintero FJ, Garciadeblas B & Rodriguez-Navarro A (1996) The SAL 1 gene of Arabidopsis, encoding an enzyme with 39(29), 59’-bisphosphate nucleotide and inositol polyphosphate 1-phosphate activities, increases salt tolerance in yeast. Plant Cell 8: 529-537

    Google Scholar 

  • Quintero FJ, Ohta M, Shi H, Zhu J-K & Pardo JM (2002) Reconstitution in yeast of the Arabidospsis signaling pathway for Na+ homeostasis. Proc. Natl. Acad. Sci. USA 99: 9061-9066

    Google Scholar 

  • Rhodes D & Hanson AD (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Ann. Rev. Plant Physiol. Plant Mol. Biol. 44: 357-384

    Google Scholar 

  • Roberts SK (1998) Regulation of K+ channels in maize roots by water stress and abscisic acid. Plant Physiol. 116: 145-153

    Google Scholar 

  • Roberts SK & Snowman BN (2000) The effects of ABA on channel-mediated K(1) transport across higher plant roots. J. Exp. Bot. 51: 1585-1594

    Google Scholar 

  • Rock CD (2000) Pathways to abscisic acid-regulated gene expression. New Phytol. 148: 357-396

    Google Scholar 

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

    Google Scholar 

  • Roxas VP, Smith RK Jr., Allen ER & Allen RD (1997) Overexpression of glutathione S-transferase / glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nat. Biotechnol. 15: 988-991

    Google Scholar 

  • Saijo Y, Hata S, Kyozuka J, Shimamoto K & Izui K (2000) Over expression of a single Ca2+-dependent protein kinase confers both cold and salt /drought tolerance on rice plants. Plant J. 23: 319-327

    Google Scholar 

  • Sakamoto A, Alia A, Murata N & Murata A (1998) Metabolic engineering of rice leading to biosynthesis of glycinebetaine and tolerance to salt and cold. Plant Mol. Biol. 38: 1011-1019

    Google Scholar 

  • Serrano R & Glaxiola R (1994) Microbial models and salt tolerance in plants. Crit. Rev. Plant Sci. 13: 121-138

    Google Scholar 

  • Serrano R (1996) Salt tolerance in plants and microorganisms: toxicity targets and defense responses. Int. Rev. Cytol. 165: 1-52

    Google Scholar 

  • Serrano R, Culianz-Macia FA & Moreno V (1998) Genetic engineering of salt and drought tolerance with yeast regulatory genes. Sci. Hort. 78: 261-269

    Google Scholar 

  • Serrano R, Mulet JM, Rios G, Marquez JA, de Larriona IF, Leube MP, Mendizabal I, Pascual-Ahuir A, Proft MRR & Montesinos C (1999) A glimpse of the mechanism of ion homeostasis during salt stress. J. Exp. Bot. 50: 1023-1036

    Google Scholar 

  • Sheveleva E, Chmara W, Bohnert H & Jensen R (1997) Increased salt and drought tolerance by D-oninitol production in transgenic Nicotiana tabaccum L. Plant Physiol. 115: 1211-1219

    Google Scholar 

  • Shi H, Ishitani M, Kim C & Zhu JK (2000) The Arabidopsis 1 1 thaliana salt tolerance gene SOS 1 encodes a putative Na+ /H+ antiporter. Proc. Natl. Acad. Sci. USA 97: 6896-6901

    Google Scholar 

  • Shi H, Quintero FJ, Pardo JM & Zhu J-K (2002a) The putative plasma membrane Na(1)/H(1) antiporter SOS1 controls longdistance Na(1) transport in plants. Plant Cell 14: 456-477

    Google Scholar 

  • Shi H, Xiong L, Stevenson B, Lu T & Zhu JK (2002b) The Arabidopsis salt overly sensitive 4 mutants uncover a critical role for vitamin B6 in plant salt tolerance. Plant Cell 14: 575-588

    Google Scholar 

  • Smart CC & Flores S (1997) Overexpression of D-myo-inositol-3-phosphate synthase leads to elevated levels of inositol in Arabidopsis. Plant Mol. Biol. 33: 811-820

    Google Scholar 

  • Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol. 27-58

  • Stewart CR & Voetberg G (1987) Abscisic acid accumulation is not required for proline accumulation in wilted leaves. Plant Physiol. 83: 747-749

    Google Scholar 

  • Strizhov N, Abraham E, Okresz L, Blickling S, Zilberstein A, Schell J, Koncz C & Szabados L (1997) Differential expression of two P5CS genes controlling proline accumulation during saltstress requires ABA and is regulated by ABA 1ABI 1and AXR 2 in Arabidopsis. Plant J. 12: 557-569

    Google Scholar 

  • Sugino M, Hibino T, Tanaka Y, Nii N, Takabe T & Takabe T (1999) Overexpression of DnaK from a halotolerant cyanobacterium Aphanothece halophytica acquires resistance to salt stress in transgenic tobacco plants. Plant Sci. 146: 81-88

    Google Scholar 

  • Szabolcs I (1994) Soil salinization. In: Pressarkli, M (ed) Handbook of plant crop stress (pp. 3-11). Marcel Dekker, New York

    Google Scholar 

  • Tanaka Y, Hibino T, Hayashi Y, Tanaka A, Kishitani S, Takabe T, Yokota S & Takabe T (1999) Salt tolerance of transgenic rice overexpressing yeast mitochondrial Mn-SOD in chloroplasts. Plant Sci. 148: 131-138

    Google Scholar 

  • Tarczynski M, Jensen R & Bohnert H (1993) Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science 259: 508-510

    Google Scholar 

  • Taylor IB, Burbidage A & Thompson AJ (2000) Control of abscisic Engineeracid synthesis. J. Exp. Bot. 51: 1563-1574

    Google Scholar 

  • Thomas JC, Smigocki AC & Bohnert HJ (1995) Light-induced expression of ipt from Agrobacterium tumefaciens results in cytokinin accumulation and osmotic stress symptoms in transgenic tobacco. Plant Mol. Biol. 27: 225-235

    Google Scholar 

  • Thornalley PJ (1990) The glyoxalase system: new developments towards functional characterization of a metabolic pathway fundamental to biological life. Biochem. J. 269: 1-11

    Google Scholar 

  • Thornalley PJ (1993) The glyoxalase system in health and disease. Mol. Aspects Med. 14: 287-371

    Google Scholar 

  • Toone WM & Jones N (1998) Stress-activated signaling pathways in yeast. Genes Cells 3: 485-498

    Google Scholar 

  • Tsiantis MS, Bartholomew DM & Smith JA (1996) Salt regulation of transcript levels for the c subunit of a leaf vacuolar H(+)-ATPase in the halophyte Mesembryanthemum crystallinum. Plant J. 9: 729-736

    Google Scholar 

  • Urao T, Yakubov B, Satoh R, Yamaguchi-Shinozaki K, Seki M, Hirayama T & Shinozaki K (1999) A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell 11: 1743-1754

    Google Scholar 

  • Veena Reddy VS & Sopory SK (1999) Glyoxalase I from Brassica juncea: molecular cloning, regulation and its over-expression confer tolerance in transgenic tobacco under stress. Plant J. 17: 385-395

    Google Scholar 

  • Wallsgrove R, Turner J, Hall N, Kendall A & Bright S (1987) Barley mutants lacking chloroplast glutamine synthetase. Biochemical and genetic analysis. Plant Physiol. 83: 155-158

    Google Scholar 

  • Winicov I (2000) Alfin 1 transcription factor overexpression enhances plant root growth under normal and saline conditions and improves salt tolerance in alfalfa. Planta 210: 416-422

    Google Scholar 

  • Wu S-J, Ding L & Zhu JK (1996) SOS 1, a genetic locus essential for salt tolerance and potassium acquisition. Plant Cell 8: 617-627

    Google Scholar 

  • Wu Y, Kuzma J, Marechal E, Graeff R, Lee HC, Foster R & Chua NH (1997) Abscisic acid signaling through cyclic ADP-ribose in plants. Science 278: 2126-2130

    Google Scholar 

  • Xiong L, Lee B, Ishitani M, Lee H, Zhang C & Zhu JK (2001) FIERY 1 encoding an inositol polyphosphate 1-phosphatase is a negative regulator of abscisic acid and stress signaling in Arabidopsis. Genes Dev. 15: 1971-1984

    Google Scholar 

  • Xu D, Duan X, Wang B, Hong B, Ho TH & Wu R (1996) Expression of a late embryogenesis abundant protein gene, HVA 1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol. 110: 249-257

    Google Scholar 

  • Yang SX, Zhao YX, Zhang Q, He YK, Zhang H & Luo (2001) HAL 1mediate salt adaptation in Arabidopsis thaliana. Cell Res. 11: 142-148

    Google Scholar 

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

    Google Scholar 

  • Yokoi S, Quintero FJ, Cubero B, Ruiz MT, Bressan RA, Hasegawa PM & Pardo JM (2002) Differential expression and function of 1 1 Arabidopsis thaliana NHX Na+ /H+ antiporter in the salt stress response. Plant J. 30: 529-539

    Google Scholar 

  • Yoshiba Y, Kiyosue T, Katagiri T, Ueda H, Mizoguchi T, Yamaguchi-Shinozaki K, Wada K, Harada Y & Shinozaki K (1995) Correlation between the induction of a gene for delta 1-pyrroline-5-carboxylate synthetase and the accumulation of proline in Arabidopsis thaliana under osmotic stress. Plant J. 7: 751-760

    Google Scholar 

  • Zhang H, Hodson J, 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

    Google Scholar 

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

    Google Scholar 

  • Zhu JK, Hasegawa PM & Bressan RA (1997) Molecular aspects of osmotic stress. Crit. Rev. Plant Sci. 16:253-277

    Google Scholar 

  • 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

    Google Scholar 

  • Zhu JK (2000) Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol. 124: 941-948

    Google Scholar 

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

    Google Scholar 

  • Zhu JK (2002) Salt drought stress signal transduction in plants. Ann. Rev. Plant Biol. 53: 247-273

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to O. Borsani.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Borsani, O., Valpuesta, V. & Botella, M. Developing salt tolerant plants in a new century: a molecular biology approach. Plant Cell, Tissue and Organ Culture 73, 101–115 (2003). https://doi.org/10.1023/A:1022849200433

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1022849200433

Navigation