Journal of Plant Biotechnology

The Korean Society of Plant Biotechnology (한국식물생명공학회)
권호 표지

Salt Tolerance in Plants - Transgenic Approaches

  • Sangam S. (Department of Genetics, Osmania University) ;
  • Jayasree D. (Department of Genetics, Osmania University) ;
  • Reddy K.Janardhan (Department of Botany, Osmania University) ;
  • Chari P.V.B. (Department of Genetics, Osmania University) ;
  • Sreenivasulu N. (Institute of Plant Genetics and Crop Plant Research (IPK)) ;
  • Kishor P.B.Kavi (Department of Genetics, Osmania University)
  • Published : 2005.03.01
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Abstract

Salinity is one of the major limiting factors for agricultural productivity. In plants, accumulation of osmolytes plays a pivotal role in abiotic stress tolerance. Likewise, exclusion or compartmentation of $Na^+$ ions into vacuoles provides an efficient mechanism to avert deleterious effects of $Na^+$ in the cytosol. Both vacuolar and plasma membrane sodium transporters and $H^+-ATPases$ can provide the necessary ion homeostasis. A variety of crop plants were engineered with respect to the synthesis of osmoprotectants and ion-compartmentation, but there are other cellular pathways involved in the salinity responses that are still not completely explored. Genomics approaches are increasingly used to identify genes and pathway changes involved in salt-tolerance. The new knowledge may be used via guided genetic engineering of multiple genes to create crop plants with significantly increased productivity in saline soils. This review surveys how plants deal with high salt conditions and how salt tolerance can be improved by transgenic approaches.

Keywords

References

  1. Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar $Na^+$/$H^+$ anti port in Arabidopsis. Science 285: 1256-1258 https://doi.org/10.1126/science.285.5431.1256
  2. Apse MP, Blumwald E (2002) Engineering salt tolerance in plants. Curr Opinion Biotech 13: 146-150 https://doi.org/10.1016/S0958-1669(02)00298-7
  3. Babu RC, Zhang J, Blum A, David Ho T-H, Wu R, Nguyen HT (2004) HVA1, a LEA gene from barley confers dehydration tolerance in transgenic rice (Oryza sativa L.) via cell membrane protection. Plant Sci 166: 855-862 https://doi.org/10.1016/j.plantsci.2003.11.023
  4. Badawi GH, Yamauchi Y, Shimada E, Sasaki R, Kawano N, Tanaka K, Tanaka K (2004) Enhanced tolerance to salt stress and water deficit by overexpressing superoxide dismutase in tobacco (Nicotiana tabacum) chloroplasts. Plant Sci 166: 919-928 https://doi.org/10.1016/j.plantsci.2003.12.007
  5. Balnokin-Yu V, Popova L (1994) The ATP-driven $Na^+$ pump in the plasma membrane of the marine unicellular algae, Platymonas viridis. FEBS Lett 343: 61-64 https://doi.org/10.1016/0014-5793(94)80607-1
  6. Barkla BJ, Pantoja O (1996) Physiology of ion transport across the tonoplast of higher plants. Ann Rev Plant Physiol Mol Biol 47:159-184 https://doi.org/10.1146/annurev.arplant.47.1.159
  7. Barkla BJ, Vera-Estrella R, Camacho-Emiterio J, Pantoja O (2002) $Na^+$/$H^+$ exchange in the halophyte Mesembryanthemum crystallinum is associated with cellular sites of $Na^+$ storage. Functional Plant Biol 9: 1017-1024 https://doi.org/10.1071/FP02045
  8. Barthakur S, Babu V, Bansal KC (2001) Over-expression of osmotin induces proline accumulation and confers tolerance to osmotic stress in transgenic tobacco. J Plant Biochem Biotech 10: 31-37 https://doi.org/10.1007/BF03263103
  9. Binzel ML (1995) NaCI-induced accumulation of tonoplast and plasma membrane $H^+$-ATPase in tomato. Physiol Plant 94: 722-728 https://doi.org/10.1111/j.1399-3054.1995.tb00990.x
  10. Bohnert HJ, Ayoubi P, Borchert C, Bressan RA, Burnap RL, Cushman JC, Cushman MA, Deyholos M, Fischer R, Galbraith DW, Hasegawa PM, Jenks M, Kawasaki S, Koiwa H, Kore-eda S, Lee BH, Michalowski CB, Misawa E, Nomura M, Ozturk N, Postier B, Prade R, Song CP, Tanaka Y, Wang H, Zhu JK (2001) A genomics approach towards salt stress tolerance. Plant Physiol Biochem 39: 295-311 https://doi.org/10.1016/S0981-9428(00)01237-7
  11. Bowler C, Siooten L, Vanden branden S, De Rycke R, Botterman J, Sybesma C, Van Montagu M, Inze D (1991) Manganese superoxide dismutase can reduce cellular damage mediated by oxygen radicals in transgenic plants. EMBO J 10: 1723-1732
  12. Bray EA (1997) Plant responses to water deficit. Trends Plant Sci 2: 48-54 https://doi.org/10.1016/S1360-1385(97)82562-9
  13. Bryan, JK (1990) A Comprehensive Treatise. Miflin B J, Lea P J (eds), Academic Press, Inc., San Diego, CA, in The Biochemistry of Plants 16 : 197-282
  14. Cheng ZQ, Targolli J, Huang XQ, Wu R (2002) Wheat LEA genes, PMA80 and PMA1959, enhance dehydration tolerance of transgenic rice (Oryza sativa L.). Molecular Breed 10: 71-82 https://doi.org/10.1023/A:1020329401191
  15. Churin Y, Schilling S, Borner T (1999) A gene family encoding glutathione peroxidase homologues in Hordeum vulgare (barley). FEBS Lett 459: 33-38 https://doi.org/10.1016/S0014-5793(99)01208-9
  16. Cooper S, Lerner HR, Reinhold L (1991) Evidence for a highly specific $K^+$/$H^+$ anti porter in membrane vesicles from the oil-seed rape hypocotyls. Plant Physiol 95: 1212-1220 https://doi.org/10.1104/pp.97.3.1212
  17. Crowe JH, Carpenter JF, Crowe LM (1998) The role of vitrification in anhydrobiosis. Ann Rev Physiol 60:73-103 https://doi.org/10.1146/annurev.physiol.60.1.73
  18. Czenpinski K, Zimmermann S, Ehrhardt T, Muller Rober B (1997) New structure and function in plant $K^+$ channels: KCI, an outward rectifier with a steep $Ca^{2+}$ dependency. EMBO J 16: 2565-2575 https://doi.org/10.1093/emboj/16.10.2565
  19. Datta K, Velazhahan R, Oliva N, ana I, Mew T, Khush GS, Muthukrishnan S, Datta SK (1999) Over-expression of the cloned rice thaumatin-like protein (PR-5) gene in transgenic rice plants enhances environmental friendly resistance to Rhizoctonia solani causing sheath blight disease. Theor Appl Genet 98: 1138-1145 https://doi.org/10.1007/s001220051178
  20. Delauney AJ, Hu C-M, Kavi Kishor PB, Verma DPS (1993) Cloning of ornithine ${\delta}$-aminotransferase cDNA from Vigna aconitifolia by trans-complementation in Escherichia coli and regulation of proline biosynthesis. J Biol Chem 268: 18673-18678
  21. Delauney AJ, Verma DPS (1990) A soybean gene encoding $\Delta^{1}$ -pyrroline-5-carboxylate reductase was isolated by functional complementation in Escherichia coli and is found to be osmoregulated. Mol Gen Genet 221: 299-305 https://doi.org/10.1007/BF00259392
  22. Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4: 215-223 https://doi.org/10.1046/j.1365-313X.1993.04020215.x
  23. De Ronde JA, Spreeth MH, Cress WA (2000) Effect of antisense 1-pyrroline-5-carboxylate reductase transgenic soybean plants subjected to osmotic and drought stress. Plant Growth Reg 32: 13-26 https://doi.org/10.1023/A:1006338911617
  24. Dure L (1993) Structural motifs in LEA proteins. In: CloseTJ, Bray EA, (eds), Plant responses to cellular dehydration during environmental stress, American Society of Plant Physiologists, pp 91-104
  25. 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 https://doi.org/10.1093/pcp/pce027
  26. Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Nat Acad Sd USA 99: 15898-15903 https://doi.org/10.1073/pnas.252637799
  27. Gaxiola RA, Li J, Undurraga S, Dang LM, Allen GJ, Alper SI, Fink GR (2001) Drought- and salt-tolerant plants result from overexpression of the AVP1 $H^+$ - pump. Proc Nat Acad Sci USA 98: 11444-11449 https://doi.org/10.1073/pnas.191389398
  28. 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 Nat Acad Sci USA 98: 11444-11449 https://doi.org/10.1073/pnas.191389398
  29. Gaxiola R, deLarrinoa FI, Villalba JM, Serrano R (1992) A novel and conserved salt induced protein is an important determinant of salt tolerance in yeast. EMBO J 11: 3157-3164
  30. Glaser H-U, Thomas D, Gaxiola R, Montrichard F, SurdinKerjan Y, Serrano R (1993) Salt tolerance and methionine biosynthesis in Saccharomyces cerevisiae involve a putative phosphatase gene. EMBO J 12: 3105-3110
  31. Glenn E, Brown JJ, Blumwald E (1999) Salt tolerant mechanism and crop potential of halophytes. Critical Rev Plant Sci 18: 227-255 https://doi.org/10.1016/S0735-2689(99)00388-3
  32. Goldschmidt EE, Tsang MLS, Schiff JA (1975) Studies of sulfate utilization by algae. Plant Sci Lett 4: 293-299 https://doi.org/10.1016/0304-4211(75)90101-7
  33. Greenway H, Munns R (1980) Mechanisms of salt tolerance in non-halophytes. Ann Rev Plant Physiol 31: 149-190 https://doi.org/10.1146/annurev.pp.31.060180.001053
  34. Gueta-Dahan Y, Yaniv Z, Zillinskas BA, Ben-Hayyim G (1997) Salt and oxidative stress: similar and specific responses and their relation to salt tolerance in citrus. Planta 203: 460-469 https://doi.org/10.1007/s004250050215
  35. Hassidim M, Braun Y, Lernaer 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 https://doi.org/10.1104/pp.94.4.1795
  36. 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 glycine betaine and enhanced tolerance to salt and cold stress. Plant J 12: 133-142 https://doi.org/10.1046/j.1365-313X.1997.12010133.x
  37. Hernandez AJ, Jimenez A, Mullineaux P, Sevilla F (2000) Tolerance of pea (Pisum sativum) to long-term salt stress is associated with induction of antioxidant defences. Plant Cell Envron 23: 853-862 https://doi.org/10.1046/j.1365-3040.2000.00602.x
  38. Holmstrom K, Somersalo S, Mandai A, Paiva TE and Welin B (2000) Improved tolerance to salinity and low temparature in transgenic tobacco producing glycine betaine. J Exp Bot 51: 177-185 https://doi.org/10.1093/jexbot/51.343.177
  39. Hong SW, Vierling E (2000) Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proc Nat Acad Sci 97: 4392-4397 https://doi.org/10.1073/pnas.97.8.4392
  40. Huang J, Hirji R, Adam L, Rozwadowski KL, Hammerlindl JK, Keller WA, Selvaraj G (2000) Genetic engineering of glycinebetaine production toward enhancing stress tolerance in plants: Metabolic limitations. Plant Physiol 122: 747-756 https://doi.org/10.1104/pp.122.3.747
  41. Jia ZP, McCullough N, Martel R, Hemmingsen S, Young PG (1992) Gene amplification at a locus encoding a putative $Na^+$/$H^+$ anti porter confers sodium and lithium tolerance in fission yeast. EMBO J 11: 1631-1640
  42. Kavi Kishor PB, Sangam S, Amrutha RN, Sri Laxmi P, Naidu KR, Rao KRSS, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: Its implications in plant growth and abiotic stress tolerance. Curr Sci 88: 424-438
  43. Kavi Kishor PB, Hong Z, Miao G, Hu C, Verma DPS (1995) Over expression of ${\Delta}^{1}$-pyrroline-5-carboxylate synthetase increases proline overproduction and confers osmotolerance in transgenic plants. Plant Physiol 108: 1387-1394 https://doi.org/10.1104/pp.108.4.1387
  44. Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert HJ (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13: 889-905 https://doi.org/10.1105/tpc.13.4.889
  45. Kleines M, Elster RC, Rodrigo MJ, Blervacq AS, Salmini F, Bartels D (1999) Isolation and expression analysis of twostress responsive sucrose-synthase genes from the resurrection plant Craterostigma platagineum (Hochst.). Planta 209: 13-24 https://doi.org/10.1007/s004250050602
  46. Ko CH, Gaber RF (1991) TRK1 and TRK2 encode structurally related $K^+$ transporters in Saccharomyces cerevisiae. Mol Cell Biol 11: 4266-4273 https://doi.org/10.1128/MCB.11.8.4266
  47. Laurie S, Feeney KA, Maathuis FJM, Heard PJ, Brown SJ, Leigh RA (2002) A role for HKT1 in sodium uptake by wheat roots. Plant J 32: 139-149 https://doi.org/10.1046/j.1365-313X.2002.01410.x
  48. Lehr A, Kirsch M, Viereck R, Schiemann, Rausch T (1999) cDNA and genomic cloning of sugar beet V-type $H^+$ATPase subunit A and C isoforms: evidence for coordinated expression during plant development and coordinated induction in response to high salinity. Plant Mol Biol 39: 463-475 https://doi.org/10.1023/A:1006158310891
  49. Leprince O, Harren FJM, Buitink J, Alberda M, Hoekstra FA (2000) Metabolic dysfunction and unabated respiration precede the loss of membrane integrity during dehydration of germinating radicles. Plant Physiol 122: 597-608 https://doi.org/10.1104/pp.122.2.597
  50. Liu JP, Ishitani M, Halfter U, Kim CS, Zhu JK (2000) The Arabidopsis thaliana $SOS_2$ gene encodes a protein kinase that is required for salt tolerance. Proc Nat Acad Sci USA 97: 3730-3734 https://doi.org/10.1073/pnas.060034197
  51. Liu J, Zhu JK (1998) A calcium sensor homolog required for plant salt tolerance. Science 280: 1943-1945 https://doi.org/10.1126/science.280.5371.1943
  52. Matsumura T, Tabayashi N, Kamagata Y, Souma C, Saruyama H (2002) Wheat catalase expressed in transgenic rice can improve tolerance against low temperature stress. Physiol Plant 116: 317-327 https://doi.org/10.1034/j.1399-3054.2002.1160306.x
  53. Mani S, Van de Cotte B, Van Montagu M, Verbruggen N (2002) Altered levels of proline dehydrogenase cause hypersensitivity to proline and its analogs in Arabidopsis. Plant Physiol 128: 73-83 https://doi.org/10.1104/pp.010572
  54. McKersie BD, Bowley SR, Harjanto E, Leprince O (1996) Water deficit tolerance and field performance of transgenic alfalfa overexpressing superoxide dismutase. Plant Physiol 111: 1177-1181 https://doi.org/10.1104/pp.111.4.1177
  55. Mohanty A, Kathuria H, Ferjani A, Sakamoto A, Mohanty P, Murata N, Tyagi AK (2002) Transgenics of an elite Indica rice variety Pusa Basmati-1 harbouring the codA gene are highly tolerant to salt stress. Theor Appl Genet 106: 51-57 https://doi.org/10.1007/s00122-002-1063-5
  56. Murguia JR, Belles JM, Serrano R (1995) A salt sensitive 3' (2'), 5' -bisphosphate nucleotidase involved in sulphate activation. Science 267:232-234 https://doi.org/10.1126/science.7809627
  57. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Ann Rev Plant Physiol 39: 1269-1280
  58. Oberschall A, Deak M, Torok K, Sass L, Vass I, Kovacs I, Feher A, Dudits D, Horvath GV (2000) A novel aldosel aldehyde reductase protects transgenic plants against lipid peroxidation under chemical and drought stresses. Plant J 24: 437-446 https://doi.org/10.1046/j.1365-313x.2000.00885.x
  59. Ozturk ZN, Talame V, Oeyholos M, Michalowski CB, Galbraith OW, Gozukirmizi N, Tuberosa R, Bohnert HJ (2002) Monitoring large-scale changes in transcript abundance in drought- and salt-stressed barley. Plant Mol Biol 48: 551-573 https://doi.org/10.1023/A:1014875215580
  60. Pardo JM, Reddy MP, Yang SL, Maggio A, Huh GH, Matsumoto T, Coca MA, Paino-D' Urzo M, Koiwa H, Yun OJ, Watad AA, Bressan RA, Hasegawa PM (1998) Stress signaling through $Ca^{2+}$ /calmodulin-dependent protein phosphatase calcineurin mediates salt adaptation in plants. Proc Nat Acad Sci USA 95: 9681-9686 https://doi.org/10.1073/pnas.95.16.9681
  61. Park SY, Seo SB, Lee SJ, Na JG, Kim Y J (2001) Mutation in PMR1, a $Ca^{2+}$ -ATPase in Golgi, confers salt tolerance in Saccharomyces cerevisiae by inducing expression of PMR2, an $Na^+$-ATPase in plasma membrane. J Biol Chem 276: 28694-28699 https://doi.org/10.1074/jbc.M101185200
  62. Peng Z, Verma OPS (1995) A rice HAL2-like gene encodes a $Ca^{2+}$ sensitive 3' (2') 5' - diphospho nucleoside 3' (2' )phospho hydrolase and complements yeast met22 and Escherichia coli cys Q mutations. J Biol Chem 270: 29105-29110 https://doi.org/10.1074/jbc.270.49.29105
  63. Piao HL, Lim JH, Kim SJ, Cheong GW, Hwang I (2001) Constitutive over-expression of AtGSK1 induces NaCI stress responses in the absence of NaCI stress and results in enhanced NaCI tolerance in Arabidopsis. Plant J 27: 305-314 https://doi.org/10.1046/j.1365-313x.2001.01099.x
  64. Pilon-Smits EA, Terry N, Sears T, Kim H, Zayed A, Hawang S, Van Dun K, Voogd E, Berwoerd TC, Krutwagen RWHH, Godijn OJM (1998) Trehalose - producing transgenic tobacco plants show improved performance under drought conditions. J Plant Physiol 152: 525-532 https://doi.org/10.1016/S0176-1617(98)80273-3
  65. Prabhavathi V, Yadav JS, Kumar PA, Rajam MV (2002) Abiotic stress tolerance in transgenic eggplant (Solanum melongena L.) by introduction of bacterial mannitol phosphodehydrogenase gene. Molecular Breed 9: 137-147 https://doi.org/10.1023/A:1026765026493
  66. Quintero FJ, Garciadeblas B and Rodriguez-Navarro A (1996) The SAL1 gene of Arabidopsis, encoding an enzyme with 3' (2'), 5' -bisphosphate nucleotide and inositol polyphosphate 1-phosphate activities increase salt tolerance in yeast. Plant Cell 8: 529-537 https://doi.org/10.1105/tpc.8.3.529
  67. Rawson HM, Richards RA, Munns R (1988) An examination of selection criteria for salt tolerance in wheat, barley and triticale genotypes. Aust J Agri Res 39: 759-772 https://doi.org/10.1071/AR9880759
  68. Rehman S, Harris PJC, Bourne WF (1998) The effect of sodium chloride on the $Ca^{2+}$ , $K^+$, and $Na^+$ concentrations of the seed coat and embryo of Acacia totilis and A.coriacea. Ann Appl Biol 133: 269-279 https://doi.org/10.1111/j.1744-7348.1998.tb05827.x
  69. Rohila JS, Jain RK, Wu R (2002) Genetic improvement of Basmati rice for salt and drought tolerance by regulated expression of a barley HVA1 cDNA. Plant Sci 163: 525-532 https://doi.org/10.1016/S0168-9452(02)00155-3
  70. Roxas VP, Smith RK, Allen ER, Allen RO (1997) Overex-pression of glutathione S-transferase, glutathione peroxidase enhance the growth of transgenic tobacco seedlings during stress. Nature Biotech 15: 988-991 https://doi.org/10.1038/nbt1097-988
  71. Roxas VP, Lodhi SA, Garrett OK, Mahan JR, Allen RO (2000) Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidase. Plant Cell Physiol 41: 1229-1234 https://doi.org/10.1093/pcp/pcd051
  72. Rus A, Yokai S, Sharkhu A, Reddy M, Lee B, Matasumoto TK, Kolwa H, Zhu JK, Bressan RA, Hasegawa PM (2001). AtHKT1 is a salt tolerance determinant that controls $Na^+$ entry into plant roots. Proc Nat Acad Sci USA 98: 14150-14155 https://doi.org/10.1073/pnas.241501798
  73. Russell BL, Rathinasabapathi B, Hanson AD (1998) Osmotic stress induces expression of choline monooxygenase in sugar beet and amaranth. Plant Physiol 116: 859-865 https://doi.org/10.1104/pp.116.2.859
  74. Saijo Y, Hata S, Kyozuka J, Shimamoto K, Izui K (2000) Over-expression of a single $Ca^{2+}$ -dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J 23: 319-327 https://doi.org/10.1046/j.1365-313x.2000.00787.x
  75. Sakamoto A, Murata N (2002) The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant Cell Environ 25: 163-171 https://doi.org/10.1046/j.0016-8025.2001.00790.x
  76. Sawahel WA, Hassan AH (2002) Generation of transgenic wheat plants producing high levels of the osmoprotectant proline. Biotech Lett 24: 721-725 https://doi.org/10.1023/A:1015294319114
  77. Sheveleva E, Chmara W, Bohnert HJ, Jensen RG (1997) Increased salt and drought tolerance by O-ononitol production in transgenic Nicotiana tabacum L. Plant Physiol 115: 1211-1219 https://doi.org/10.1104/pp.115.3.1211
  78. Shi HZ, Ischitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative $Na^+$/$H^+$antiporter. Proc Nat Acad Sci USA 97: 6896-6901 https://doi.org/10.1073/pnas.120170197
  79. Shi HZ, Xiong LM, Stevenson B, Lu TG, Zhu JK (2002) The Arabidopsis salt overly sensitive 4 mutants uncover a critical role for vitamin B6 in plant salt tolerance. Plant Cell 14: 575-588 https://doi.org/10.1105/tpc.010417
  80. Singh BG, Verma OPS (2001) Glutathione-an antioxidant to withstand oxidative stress in transgenic lines of tobacco. Ind J Plant Physiol 6: 229-232
  81. Sivamani E, Bahieldin A, Wraith JM, AI-Niemi T, Dyer WE, Ho THO, Qu RO (2000) Improved biomass productivity and water use efficiency under water deficit conditions in transgenic wheat constitutively expressing the barley HVA1 gene. Plant Sci 155: 1-9 https://doi.org/10.1016/S0168-9452(99)00247-2
  82. Smart CC, Flores HE (1997) Overexpression of D-myoinositol-3-phsphate synthase leads to elevated levels of inositol in Arabidopsis. Plant Mol Biol 33: 814-820 https://doi.org/10.1023/A:1005754425440
  83. Sreenivasulu N, Ramanjulu S, Ramachandra-Kini K, Prakash HS, Shetty HS. Savithri HS, Sudhakar C (1999) Total peroxidase activity and peroxidase isoforms as modified by salt stress in two cultivars of fox-tail millet with differential salt tolerance. Plant Sci 141: 1-9 https://doi.org/10.1016/S0168-9452(98)00204-0
  84. Sreenivasulu N, Grimm B, Wobus U, Weschke W (2000) Differential response of antioxidant compounds to salinity stress in salt-tolerant and salt-sensitive seedlings of foxtail millet (Setaria italica). Physiol Plant 109: 435-442 https://doi.org/10.1034/j.1399-3054.2000.100410.x
  85. Sreenivasulu N, Kavi Kishor PB, Varshney RK, Altschmied L (2002a) Mining functional information from cereal genomes - the utility of expressed sequence tags. Current Sci 83: 965-973
  86. Sreenivasulu N, Altschmied L, Panitz R, Hahnel U, Michalek W, Weschke W, Wobus U (2002b) Identification of genes specifically expressed in maternal and filial tissues of barley caryopses: A cDNA array analysis. Mol Genet Genomics 266: 758-767 https://doi.org/10.1007/s00438-001-0614-9
  87. Sreenivasulu N, Miranda M, Prakash HS, Wobus U, Weschke W (2004) Transcriptome changes in foxtail millet genotypes at high salinity: Identification and characterization of a PHGPX gene specifically up-regulated by NaCI in a salt-tolerant line. J Plant Physiol 161: 467-477 https://doi.org/10.1078/0176-1617-01112
  88. 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 https://doi.org/10.1016/S0168-9452(99)00086-2
  89. Sun WN, Bernard C, van de Cotte B, Van Montagu M, Verbruggen N (2001) At-HSP17.6A, encoding a small heat-shock protein in Arabidopsis, can enhance osmotolerance upon overexpression. Plant J 27: 407-415 https://doi.org/10.1046/j.1365-313X.2001.01107.x
  90. Suprasanna P (2003) Building stress tolerance through overproducing trehalose in transgenic plants. Trends Plant Sci 8: 355-357 https://doi.org/10.1016/S1360-1385(03)00159-6
  91. Tarczynski MC, Jensen RG, Bohnert HJ (1993) Stress protection of the osmolyte mannitol. Science 259: 508-510 https://doi.org/10.1126/science.259.5094.508
  92. Tepperman JM, Dunsmuir P (1990) Transformed plants with elevated levels of chloroplastic SOD are not more resistant to superoxide toxicity. Plant Mol Biol 14: 501-511 https://doi.org/10.1007/BF00027496
  93. Tsugane K, Kobayashi K, Niwa Y, Ohba Y, Wada K, Kobayashi H (1999) A recessive Arabidopsis mutant that grows photoautotrophically under salt stress enhanced active oxygen detoxification. Plant Cell 11: 1195-1206 https://doi.org/10.1105/tpc.11.7.1195
  94. Wang J, Zhang H, Allen RD (1999) Overexpression of an Arabidopsis peroxisomal ascorbate peroxidase gene in tobacco increases protection against oxidative stress. Plant Cell Physiol 40: 725-732 https://doi.org/10.1093/oxfordjournals.pcp.a029599
  95. Xu DP, Duan XL, Wang BY, Hong BM, Ho THO, Wu R (1996) Expression of a late embryogenesis abundant protein gene, HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol 110: 249-257 https://doi.org/10.1104/pp.110.1.249
  96. Yang SX, Zhao YX, Zhang Q, He YK, Zhang H, Luo D (2001) HAL1 mediated salt adaptation in Arabidopsis thaliana. Cell Research 11: 142-148 https://doi.org/10.1038/sj.cr.7290079
  97. Yeo ET, Kwon HB, Han SE, Lee JT, Ryu JC, Byu MO (2000) Genetic engineering of drought resistant potato plants by introduction of the trehalose-6-phosphate synthase (TPS1) gene from Saccharomyces cerevisiae. Mol Cells 10: 263-268
  98. Zhang HX, Hodson IN, 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 Nat Acad Sci USA 98: 12832-12836 https://doi.org/10.1073/pnas.231476498
  99. Zhang HX, Blumwald E (2001) Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nature Biotech 19: 765-768 https://doi.org/10.1038/90824
  100. Zhu JK, Shi J, Bressan RA, Hasegawa PM (1993) Expression of an Atriplex nummularia gene encoding a protein homologous to the bacterial molecular chaperone DNA J. Plant Cell 5: 341-349 https://doi.org/10.1105/tpc.5.3.341
  101. Zhu JK, Hasegawa PM, Bressan RA (1997) Molecular aspects of osmotic stress in plants. Crit. Rev. Plant Sci 16: 253-277 https://doi.org/10.1080/713608147
  102. 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: 1181-1192 https://doi.org/10.1105/tpc.10.7.1181
  103. Zhu BC, Su J, Chan MC, Verma DPS, Fan YL, Wu R (1998) Overexpression of a ${\Delta}^1$-pyrroline-5-carboxylate synthetase gene and analysis of tolerance to water- and salt-stress in transgenic rice. Plant Sci 139: 41-48 https://doi.org/10.1016/S0168-9452(98)00175-7
  104. Zhu JK (2002) Salt and drought stress signal transduction in plants. Ann Rev Plant Biol 53: 247-273 https://doi.org/10.1146/annurev.arplant.53.091401.143329