Transgenic approaches for abiotic stress tolerance in plants: Retrospect and prospects

Plant Cell Reports

Volumn 27, Issue 3, 2008, Pages 411-424

  Bhatnagar Mathur, Pooja ^a   Vadez, V ^a   Sharma, Kiran K ^a  

^a INTERNATIONAL CROPS RESEARCH INSTITUTE FOR THE SEMI ARID TROPICS ICRISAT   (India)

Author keywords

Abiotic stress; Drought tolerance; Genetic engineering; Transcription factors; Transpiration efficiency

Indexed keywords

ADAPTATION; EVAPOTRANSPIRATION; GENE EXPRESSION REGULATION; GENETIC ENGINEERING; GENETIC TRANSCRIPTION; GENETICS; METHODOLOGY; PHYSIOLOGY; REVIEW; TRANSGENIC PLANT;

ADAPTATION, PHYSIOLOGICAL; GENE EXPRESSION REGULATION, PLANT; GENETIC ENGINEERING; PLANT TRANSPIRATION; PLANTS, GENETICALLY MODIFIED; TRANSCRIPTION, GENETIC;

EID: 43049173527     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-007-0474-9     Document Type: Review

References (154)

1. Abebe T, Guenzi AC, Martin B, Cushman JC (2003) Tolerance of Mannitol-accumulating transgenic wheat to water stress and salinity. Plant Physiol 131:1748-1755
2. Aharoni A, Dixit S, Jetter R, Thoenes E, van Arkel G, Pereira A (2004) The SHINE clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. Plant Cell 16:2463-2480
3. Alia H, Sakamoto A, Murata N (1998) Enhancement of tolerance of Arabidopsis to high temperature by genetic engineering of the synthesis of glycine betaine. Plant J 16:155-161
4. Alia H, Kondo Y, Sakamoto A, Nonaka H, Hayashi H, Pardha Saradhi P, Chen THH, Norio M (1999) Enhanced tolerance to light stress of transgenic Arabidopsis plants that express the codA gene for a bacterial choline oxidase. Plant Mol Biol 40:279-288
5. Allen RD (1995) Dissection of oxidative stress tolerance using transgenic plants. Plant Physiol 107:1049-1054
6. Anderson SE, Bastola DR, Minocha SC (1998) Metabolism of polyamines in transgenic cells of carrot expressing a mouse ornithine decarboxylase cDNA. Plant Physiol 116:299-307
7. Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vascoular Na+/H+ antiport in Arabidopsis. Science 285:1256-1258
8. Bajaj S, Targolli J, Liu L-F, Ho TH, Wu R (1999) Transgenic approaches to increase dehydration stress tolerance in plants. Mol Breed 5:493-503
9. Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 21:1-36
10. Behnam B, Kikuchi A, Celebi-Toprak F, Yamanaka S, Kasuga M, Yamaguchi-Shinozaki K, Watanabe KN (2006) The Arabidopsis DREB1A gene driven by the stress-inducible rd29A promoter increases salt-stress tolerance in proportion to its copy number in tetrasomic tetraploid potato (Solanum tuberosum). Plant Biotech 23:169-177
11. Bhatnagar-Mathur P, Devi M J, Serraj R, Yamaguchi-Shinozaki K, Vadez V, Sharma KK (2004) Evaluation of transgenic groundnut lines under water limited conditions. Int Arch Newsl 24:33-34
12. Bhatnagar-Mathur P, Devi M J, Reddy DS, Vadez V, Yamaguchi-Shinozaki K, Sharma KK (2006) Overexpression of Arabidopsis thaliana DREB1A in transgenic peanut (Arachis hypogaea L.) for improving tolerance to drought stress (poster presentation). In: Arthur M. Sackler Colloquia on "From Functional Genomics of Model Organisms to Crop Plants for Global Health", April 3-5, 2006. National Academy of Sciences, Washington, DC
13. Bohnert HJ, Shen B (1999) Transformation and compatible solutes. Sci Hort 78:237-260
14. Bohnert HJ, Nelson DF, Jenson RG (1995) Adaptation to environmental stresses. Plant Cell 7:1099-1111
15. Bordás 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. Transgenic Res 5:1-10
16. Bowler C, Slooten L, Vandenbranden S, Rycke RD, 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
17. Bray EA (1993) Molecular responses to water deficit. Plant Physiol 103:1035-1040
18. Burke EJ, Brown SJ, Christidis N (2006) Modeling the recent evolution of global drought and projections for the twenty-first century with the Hadley centre climate model. J Hydrometeor 7:1113-1125
19. Capell T, Escobar C, Lui H, Burtin H, Lepri O, Christou P (1998) Overexpression of the oat arginine decarboxylase cDNA in transgenic rice (Oryza sativa L.) affects normal development patterns in vitro and results in putrescine accumulation in transgenic plants. Theor Appl Genet 97:246-254
20. Capell T, Bassie L, Christou P (2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc Natl Acad Sci USA 101:9909-9914
21. Chen TH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5:250-257
22. Cheng WH, Endo A, Zhou L, Penney J, Chen HC, Arroyo A, Leon P, Nambara E, Asami T, Seo M (2002) A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. Plant Cell 14:2723-2743
23. Chinnusamy V, Jagendorf A, Zhu JK (2005) Understanding and improving salt tolerance in plants. Crop Sci 45:437-448
24. Cortina C, Culiá n ez-Maciá F (2005) Tomato abiotic stress enhanced tolerance by trehalose biosynthesis. Plant Sci 169:75-82
25. Cutler S, Ghassemian M, Bonetta D, Cooney S, McCourt P (1996) A protein farnesyl transferase involved in abscisic acid signal transduction in Arabidopsis. Science 273:1239-1241
26. Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4:215-223
27. Diamant S, Eliahu N, Rosenthal D, Goloubinoff P (2001) Chemical chaperones regulate molecular chaperones in vitro and in cells under combined salt and heat stresses. J Biol Chem 276:39586-39591
28. Dure L III (1993) A repeating 11-mer amino acid motif and plant desiccation. Plant J 3:363-369
29. Dure L III, Crouch M, Harada J, Ho T-HD, Mundy J (1989) Common amino acid sequence domains among the LEA proteins of higher plants. Plant Mol Biol 12:475-486
30. FAO (Food, Agriculture Organization of the United Nations) (2004) FAO production yearbook. FAO, Rome
31. Fukai S, Cooper M (1995) Developing resistant cultivars using physiomorphological traits in rice. Field Crops Res 40:67-86
32. Galau GA, Bijaisoradat N, Hughes DW (1987) Accumulation kinetics of cotton late embryogenesis-abundent (Lea) mRNAs and storage protein mRNAs: coordinate regulation during embryogenesis and role of abscisic acid. Dev Biol 123:198-212
33. Gao M, Sakamoto A, Miura K, Murata N, Sugiura A, Tao R (2000) Transformation of Japanese persimmon (Diospyros kaki Thunb.) with a bacterial gene for choline oxidase. Mol Breed 6:501-510
34. Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YC, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci USA 99:15898-15903
35. Gisbert C, Rus AM, Bolarin MC, Lopez-Coronado M, Arrillaga I, Montesinos C, Caro M, Serrano R, Moreno V (2000) The yeast HAL1 gene improves salt tolerance of transgenic tomato. Plant Physiol 123:393-402
36. Goyal K, Walton LJ, Tunnacliffe A (2005) LEA proteins prevent protein aggregation due to water stress. Biochem J 388:151-157
37. Grover A, Minhas D (2000) Towards production of abiotic stress tolerant transgenic rice plants: issues, progress and future research needs. Proc Indian Natl Sci Acad B Rev Tracts. Biol Sci 66:13-32
38. Grover A, Sahi C, Sanan N, Grover A (1999) Taming abiotic stresses in plants through genetic engineering: current strategies and perspective. Plant Sci 143:101-111
39. Grover A, Kapoor A, Satya Lakshmi O, Agrawal S, Sahi C, Katiyar-Agarwal S, Agarwal M, Dubey H (2001) Understanding molecular alphabets of the plant abiotic stress responses. Curr Sci 80:206-216
40. Guiltinan MJ, Marcotte WR, Quatrano RS (1990) A plant leucine zipper protein that recognizes an abscisic acid response element. Science 250:267-271
41. Haake V, Cook D, Riechmann JL, Pineda O, Thomashow MF, Zhang JZ (2002) Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol 130:639-648
42. Hare PD, Cress WA, Van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21:535-553
43. Hayashi H, 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
44. Hayashi H, Alia, Sakamoto A, Nonaka H, Chen THH, Murata N (1998) Enhanced germination under high-salt conditions of seeds of transgenic Arabidopsis with a bacterial gene (codA) for choline oxidase. J Plant Res 111:357-362
45. Holmstrom KO, Manty E, Welin B, Palva ET (1996) Drought tolerance in tobacco. Nature 379:683-684
46. Holmstrom KO, Somersalo S, Mandal A, Palva ET, Welin B (2000) Improved tolerance to salinity and low temperature in transgenic tobacco producing glycine betaine. J Expt Bot 51:177-185
47. Hsieh TH, Lee JT, Charng YY, Chan MT (2002) Tomato plants ectopically expressing Arabidopsis CBF1 show enhanced resistance to water deficit stress. Plant Physiol 130:618-626
48. Ishitani M, Xiong L, Stevenson B, Zhu J-K (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
49. Iwasaki T, Kiyosue T, Yamaguchi-Shinozaki K (1997) The dehydration-inducible rd17 (cor47) gene and its promoter region in Arabidopsis thaliana. Plant Physiol 115:128
50. Jaglo KR, Kleff KL, Amundsen X, Zhang V, Haake JZ, Zhang T, Thomashow MF (2001) Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Plant Physiol 127:910-917
51. Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces cor genes and enhances freezing tolerance. Science 280:104-106
52. Kagaya Y, Hobo T, Murata M, Ban A, Hattori T (2002) Abscisic acidinduced transcription is mediated by phosphorylation of an abscisic acid response element binding factor, TRAB1. Plant Cell 14:3177-3189
53. 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
54. Kasuga M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2004) A combination of the Arabidopsis DREB1A gene and stress-inducible rd29A promoter improved drought- and low-temperature stress tolerance in tobacco by gene transfer. Plant Cell Physiol 45:346-350
55. Katiyar-Agarwal S, Agarwal M, Grover A (1999) Emerging trends in agricultural biotechnology research: use of abiotic stress induced promoter to drive expression of a stress resistance gene in the transgenic system leads to high level stress tolerance associated with minimal negative effects on growth. Curr Sci 77:1577-1579
56. Katiyar-Agarwal S, Agarwal M, Grover A (2003) Heat-tolerant basmati rice engineered by over-expression of hsp101. Plant Mol Biol 51:677-686
57. Kimpel JA, Key JL (1985) Heat shock in plants. Trends Biochem Sci 10:353-357
58. Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci USA 97:2940-2945
59. Kumria R, Rajam MV (2002) Ornithine decarboxylase transgene in tobacco affects polyamines, in vitro-morphogenesis and response to salt stress. J Plant Physiol 159:983-990
60. Lee JH, Hubel A, Schoffl F (1995) Derepression of activity of genetically engineered heat-shock factor causes constitutive synthesis of heat shock proteins and increased thermotolerance in transgenic Arabidopsis. Plant J 8:603-612
61. Lee JH, van Montagu M, Verbruggen N (1999) A highly conserved kinase is an essential component for stress tolerance in yeast and plant cells. Proc Natl Acad Sci USA 96:5873-5877
62. Lee H, Xiong L, Gong Z, Ishitani M, Stevenson B, Zhu JK (2001) The Arabidopsis HOS1 gene negatively regulates cold signal transduction and encodes a RING-finger protein that displays cold-regulated nucleo-cytoplasmic partitioning. Gene Dev 15:912-924
63. Lee SS, Cho HS, Yoon GM, Ahn JW, Kim HH, Pai HS (2003) Interaction of NtCDPK1 calcium-dependent protein kinase with NtRpn3 regulatory subunit of the 26S proteasome in Nicotiana tabacum. Plant J 33:825-840
64. Li HY, Chang CS, Lu LS, Liu CA, Chan MT, Chang YY (2003) Over-expression of Arabidopsis thaliana heat shock factor gene (AtHsfA1b) enhances chilling tolerance in transgenic tomato. Bot Bull Acad Sin 44:129-140
65. Lilius G, Holmberg N, Bülow L (1996) Enhanced NaCl stress tolerance in transgenic tobacco expressing bacterial choline dehydrogenase. Biotechnol 14:177-180
66. Lindquist S (1986) The heat-shock response. Annu Rev Biochem 55:1151-1191
67. 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
68. Malik MK, Solvin JP, Hwang CH, Zimmerman JL (1999) Modified expression of a carrot small heat-shock protein gene, Hsp 17.7 results in increased or decreased thermotolerance. Plant J 20:89-99
69. Maliro MFA, McNeil D, Kollmorgen J, Pittock C, Redden B (2004) Screening chickpea (Cicer arietinum L.) and wild relatives germplasm from diverse sources for salt tolerance. New directions for a diverse planet: Proceedings of the 4th International Crop Science Congress, Brisbane, Australia, 26 Sep to 1 Oct 2004
70. 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
71. McNeil SD, Nuccio ML, Hanson AD (1999) Betaines and related osmoprotectants. Targets for metabolic engineering of stress resistance. Plant Physiol 120:945-949
72. McNeil SD, Nuccio ML, Rhodes D, Shachar-Hill Y, Hanson AD (2000) Radiotracer and computer modeling evidence that phosphobase methylation is the main route of choline synthesis in tobacco. Plant Physiol 123:371-380
73. Miroshnichenko S, Tripp J, Nieden UZ, Neumann D, Conrad U, Manteuffel R (2005) Immunomodulation of function of small heat shock proteins prevents their assembly into heat stress granules and results in cell death at sublethal temperatures. Plant J 41:269-281
74. Mundy J, Chua N-H (1988) Abscisic acid and water-stress induce the expression of a novel rice gene. EMBO J 7:2279-2286
75. Mundy J, Yamaguchi-Shinozaki K, Chua NH (1990) Nuclear proteins bind conserved elements in the abscisic acid-responsive promoter of a rice rab gene. Proc Natl Acad Sci USA 87:406-410
76. Munns R, Husain S, Rivelli AR, James RA, Condon AG, Lindsay MP, Lagudah ES, Schachtman DP, Hare RA (2002) Avenues for increasing salt tolerance of crops, and the role of physiologically based selection traits. Plant Soil 247:93-105
77. Murakami Y, Tsuyama M, Kobayashi Y, Kodama H, Iba K (2000) Trienoic fatty acids and plant tolerance of high temperature. Science 287:476-479
78. Murata N, Ishizaki-Nishizawa O, Higashi S, Hayashi S, Tasaka Y, Nishida I (1992) Genetically engineered alteration in the chilling sensitivity of plants. Nature 356:710-713
79. Nanjo T, Kobayashi M, Yoshiba Y, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (1999a) Antisense supression of proline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana. FEBS Lett 461:205-210
80. Nordin K, Heino P, Palva ET (1991) Separate signal pathways regulate the expression of a low-temperature-induced gene in Arabidopsis thaliana (L.) Heynh. Plant Mol Biol 115:875-879
81. Oberschall A, Deak M, Torok K, Sass L, Vass I, Kovacs I, Feher A, Dudits D, Hovarth GV (2000) A novel aldose/aldehyde reductase protects transgenic plants against lipid peroxidation under chemical and drought stress. Plant J 24:437-446
82. Ozturk ZN, Talame V, Deyholos M, Michalowski CB, Galbraith DW, 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
83. Passioura J (1977) Physiology of grain yield in wheat growing on stored water. Aust J Plant Physiol 3:559-565
84. Passioura J (2007) The drought environment: physical, biological and agricultural perspectives. J Exp Bot 58:113-117
85. 2+/Calmodulin dependent protein phosphatase calcineurin mediates salt adaptation in plants. Proc Natl Acad Sci USA 95:9681-9683
86. Pei ZM, Ghassemian M, Kwak CM, McCourt P, Schroeder JI (1998) Role of farnesyltransferase in ABA regulation of guard cell anion channels and plant water loss. Science 282:287-290
87. Pellegrineschi A, Reynolds M, Pacheco M, Brito R M, Almeraya R, Yamaguchi-Shinozaki K, Hoisington D (2004) Stress-induced expression in wheat of the Arabidopsis thaliana DREB1A gene delays water stress symptoms under greenhouse conditions. Genome 47:493-500
88. Perl A, Perl-Treves R, Galili S, Aviv D, Shalgi E, Malkin S, Galun E (1993) Enhanced oxidative stress defense in transgenic potato expressing tomato Cu, Zn superoxide dismutases. Theor Appl Genet 85:568-576
89. Pilon-Smits EAH, Ebskamp MJM, Paul MJ, Jeuken JW, Weisbeek, Smeekens SCM (1995) Improved performance of transgenic fructan-accumulating tobacco under drought stress. Plant Physiol 107:125-130
90. Pilon-Smits EAH, Ebskamp MJM, Jeuken MJW, van der Meer IM, Visser RGF, Weisbeek PJ, Smeekens JCM (1996) Microbial fructan production in transgenic potato plants and tubers. Ind Crops Prod 5:35-46
91. Pilon-Smits EAH, Terry N, Sears T, Kim H, Zayed A, Hwang S, Van Dun K, Voogd E, Verwoerd TC, Krutwagen RWHH, Giddijn JM (1998) Trehalose-producing transgenic tobacco plants show improved growth performance under drought stress. J Plant Physiol 152:525-532
92. Pilon-Smits EAH, Terry N, Sears T, van Dun K (1999) Enhanced drought resistance in fructan-producing sugar beet. Plant Physiol Biochem 37:313-317
93. Quimlo CA, Torrizo LB, Setter TL, Ellis M, Grover A, Abrigo EM, Oliva NP, Ella ES, Carpena AL, Ito O, Peacock WJ, Dennis E, Datta SK (2000) Enhancement of submergence tolerance in transgenic rice plants overproducing pyruvate decarboxylase. J Plant Physiol 156:516-521
94. Quintero FJ, Blatt MR, Pardo JM (2000) Functional conservation between yeast and plant endosomal Na(+)/H(+) antiporters. FEBS Lett 471:224-228
95. Ritchie GA (1982) Carbohydrate reserves and root growth potential in Douglas-fir seedlings before and after cold storage. Can J For Res 12:905-912
96. 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
97. Romero C, Belles JM, Vaya JL, Serrano R, Culianez-Macia FA (1997) Expression of the yeast trehalose-6-phosphate synthase gene in transgenic tobacco plants: pleiotropic phenotypes include drought tolerance. Planta 201:293-297
98. 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
99. Roy M, Wu R (2001) Arginine decarboxylase transgene expression and analysis of environmental stress tolerance in transgenic rice. Plant Sci 160:869-875
100. Roy M, Wu R (2002) Overexpression of S-adenosylmethionine decarboxylase gene in rice increases polyamine level and enhances sodium chloride-stress tolerance. Plant Sci 163:987-992
101. Rubio MC, González EM, Minchin FR, Webb KJ, Arrese-Igor C, Ramos J, Becana M (2002) Effects of water stress on antioxidant enzymes of leaves and nodules of transgenic alfalfa overexpressing superoxide dismutases. Physiol Plant 115:531-540
102. Sakamoto A, Alia, Murata N (1998) Metabolic engineering of rice leading to biosynthesis of glycine betaine and tolerance to salt and cold. Plant Mol Biol 38:1011-1019
103. Sakamoto A, Valverde R, Alia, Chen TH, Murata N (2000) Tranformation of Arabidopsis with the codA gene for choline oxidase enhances freezing tolerance of plants. Plant J 22:449-453
104. Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in droughtresponsive gene expression. The Plant Cell 18:1292-1309
105. Schobert B, Tschesche H (1978) Unusual solution properties of proline and its interaction with proteins. Biochem Biophys Acta 541:270-277
106. Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi- Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K (2001) Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA Microarray. Plant Cell 13:61-72
107. Sen Gupta A, Heinen JL, Holady AS, Burke JJ, Allen RD (1993) Increased resistance to oxidative stress in transgenic plants that over-express chloroplastic Cu/Zn superoxide dismutase. Proc Nat Acad Sci USA 90:1629-1633
108. Serraj R, Sinclair TR (2002) Osmolyte accumulation: can it really help increase crop under drought conditions? Plant Cell Environ 25:333-341
109. Shen B, Jensen RG, Bohnert HJ (1997) Increased resistance to oxidative stress in transgenic plants by targeting mannitol biosynthesis to chloroplasts. Plant Physiol 113:1177-1183
110. Shi H, Ishitani 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
111. Shinozaki K, Yamaguchi-Shinozaki K (1997) Gene expression and signal transduction in water-stress response. Plant Physiol 115:327-334
112. Shinozaki K, Yamaguchi-Shinozaki K (1999) Molecular responses to drought stress. In: Shinozaki K, Yamaguchi-Shinozaki K (eds) Molecular responses to cold, drought, heat and salt stress in higher plants. R.G. Landes Co., Austin, pp 11-28
113. Shinwari ZK (1999) Function and regulation of genes that are induced by dehydration stress. Biosci Agric 5:39-47
114. Shinwari ZK, Nakashima K, Miura S, Kasuga M, Seki M, Yamaguchi-Shinozaki K, Shinozaki K (1998) An Arabidopsis gene family encoding DRE/CRT binding proteins involved in low-temperature-responsive gene expression. Biochem Biophys Res Commun 50:161-170
115. Shou H, Bordallo P, Wang K (2004) Expression of the Nicotiana protein kinase (NPK1) enhanced drought tolerance in transgenic maize. J Exp Bot 55:1013-1019
116. Simpson SD, Nakashima K, Narusaka Y, Seki M, Shinozaki K, Yamaguhci-Shinozaki K (2003) Two different novel cis-acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence. Plant J 33:259-270
117. Sinclair TR, Ludlow MM (1986) Influence of soil water supply on the plant water balance of four tropical grain legumes. Aust J Plant Physiol 13:329-341
118. Sinclair BJ, Jaco Klok C, Chown SL (2004) Metabolism of the sub-Antarctic caterpillar Pringleophaga marioni during cooling, freezing and thawing. J Exp Biol 207:1287-1294
119. Sivamani E, Bahieldin A, Wraith JM, Al-Niemi T, Dyer WE, Ho THD, Qu R (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
120. Skriver K, Mundy J (1990) Gene expression in response to abscisic acid and osmotic stress. Plant Cell 5:503-512
121. Slooten L, Capiau K, Van Camp W, Montagu MV, Sybesma C, Inzé D (1995) Factors affecting the enhancement of oxidative stress tolerance in transgenic tobacco overexpressing manganese superoxide dismutase in the chloroplasts. Plant Physiol 107:737-775
122. Sun W, Bernard C, van de Cotte B, Montagu MV, Verbruggen N (2001) At-HSP17.6A, encoding a small heat-shock protein in Arabidopsis, can enhance osmotolerance upon overexpression. Plant J 27:407-415
123. Tarczynski MC, Jensen RG, Bohnert HJ (1993) Stress protection of transgenic tobacco by production of osmolyte mannitol. Science 259:508-510
124. Thomashow M F (1998) Role of cold responsive genes in plant freezing tolerance. Plant Physiol 118:1-7
125. Turner NC, Shahal A, Berger JD, Chaturvedi SK, French RJ, Ludwig C, Mannur DM, SJ Singh SJ, Yadava HS (2007) Osmotic adjustment in chickpea (Cicer arietinum L.) results in no yield benefit under terminal drought. J Exp Bot 58:187-194
126. Umezawa T, Yoshida R, Maruyama K, Yamaguchi-Shinozaki K, Shinozaki K (2004) SRK2C, a SNF1-related protein kinase 2, improves drought tolerance by controlling stress-responsive gene expression in Arabidopsis thaliana. Proc Natl Acad Sci USA.101:17306-17311
127. Umezawa T, Fujita M, Fujita Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr Opin Biotechnol 17:113-122
128. Vadez V, Krishnamurthy L, Gaur PM, Upadhyaya HD, Hoisington DA, Varshney RK, Turner NC, Siddique KHM (2006) Tapping the large genetic variability for salinity tolerance in chickpea. Proceeding of the Australian Society of Agronomy meeting (10-14 Sept 2006) http://www.agronomy.org.au
129. Vadez V, Krishnamurthy L, Serraj R, Gaur PM, Upadhyaya HD, Hoisington DA, Varshney RK, Turner NC, Siddique KHM (2007) Large variation in salinity tolerance in chickpea is explained by differences in sensitivity at the reproductive stage. Field Crop Res (in press)
130. Van Camp W, Capiau K, Van Montagu M, Inzé D, Slooten L (1996) Enhancement of oxidative stress tolerance in transgenic tobacco plants overproducing Fe-superoxide dismutase in chloroplasts. Plant Physiol 112:1703-1714
131. Vierling E (1991) The roles of heat shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42:579-620
132. Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:123-132
133. Voetberg GS, Sharp RE (1991) Growth of the maize primary root tip at low water potentials. III. Role of increased proline deposition in osmotic adjustment. Plant Physiol 96:1125-1130
134. Vranova E, Inze D, Van Breusegem F (2002) Signal transduction during oxidative stress. J Exp Bot 53:1227-1236
135. Waie B, Rajam MV (2003) Effect of increased polyamine biosynthesis on stress responses in transgenic tobacco by introduction of human S-adenosylmethionine gene. Plant Sci 164:727-734
136. Wang Y, Ying J, Kuzma M, Chalifoux M, Sample A, McArthur C, Uchacz T, Sarvas C, Wan J, Dennis DT et al (2005) Molecular tailoring of farnesylation for plant drought tolerance and yield protection. Plant J 43:413-424
137. Waters ER, Lee GJ, Vierling E (1996) Evolution, structure and function of the small heat shock proteins in plants. J Exp Bot 47:325-338
138. Winicov I, Bastola DR (1997) Salt tolerance in crop plants: new approaches through tissue culture and gene regulation. Acta Physiol Plant 19:435-449
139. Winicov I, Bastola DR (1999) Transgenic overexpression of the transcription factor Alfin1 enhances expression of the endogenous MsPRP2 gene in alfalfa and improves salinity tolerance of the plants. Plant Physiol 120:473-480
140. Xiong L, Zhu JK (2001) Plant abiotic stress signal transduction: molecular and genetic perspectives. Physiol Plant 112:152-166
141. Xiong L, Ishitani M, Zhu J-K (1999) Interaction of osmotic stress, temperature, and abscisic acid in the regulation of gene expression in Arabidopsis. Plant Physiol 119:205-211
142. Xu D, Duan X, Wang B, Hong B, Ho T-HD, 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
143. Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R (2006) Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442:705-708
144. Yamada M, Morishita H, Urano K, Shiozaki N, Yamaguchi-Shinozaki K, Shinozaki K, Yoshiba Y (2005) Effects of free proline accumulation in petunias under drought stress. J Exp Bot 56:1975-1981
145. Yamaguchi-Shinozaki K, Shinozaki K (1993) Characterisation of the expression of a dessication-responsive rd29 gene of Arabidopsis thaliana and analysis of its promoter in transgenic plants. Mol Gen Genet 236:331-340
146. Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Kiyosue T, Shinozaki K (1994) Function and regulation of genes that are induced by dehydration stress in Arabidopsis thaliana. JIRCAS J 1:69-79
147. Yang G, Rhodes D, Joly RJ (1996) Effects of high temperature on membrane stability and chlorophyll fluorescence in glycine betaine-deficient and glycine betaine containing maize lines. Aust J Plant Physiol 23:437-443
148. Zhang H-X, Blumwald E (2001) Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat Biotechnol 19:765-768
149. Zhang JZ, Creelman RA, Zhu JK (2004) From laboratory to field. Using information from Arabidopsis to engineer salt, cold, and drought tolerance in crops. Plant Physiol 135:615-621
150. Zhang JY, Broeckling CD, Blancaflor EB, Sledge MK, Sumner LW, Wang ZY (2005) Overexpression of WXP1, a putative Medicago truncatula AP2 domain-containing transcription factor gene, increases cuticular wax accumulation and enhances drought tolerance in transgenic alfalfa (Medicago sativa). Plant J 42:689-707
151. Zhao HW, Chen YJ, Hu YL, Gao Y, Lin ZP (2000) Construction of a trehalose-6-phosphate synthase gene driven by drought responsive promoter and expression of drought-resistance in transgenic tobacco. Acta Bot Sinica 42:616-619
152. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Physiol Plant Mol Biol 53:247-273
153. Zhu B, Su J, Chang M, Verma DPS, Fan YL, Wu R (1998) Overexpression of delta1-pyrroline-5-carboxylate synthase gene and analysis of tolerance to water and salt stress in transgenic rice. Plant Sci 199:41-48
154. Zhu L, Tang GS, Hazen SP, Kim HS, Ward RW (1999) RFLP-based genetic diversity and its development in Shaanxi wheat lines. Acta Bot Boreali Occident Sin 19:13