Journal of Plant Biotechnology

The Korean Society of Plant Biotechnology (한국식물생명공학회)
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Molecular Mechanism of Plant Adaption to High Salinity

식물의 고염 스트레스에 대한 반응 및 적응기작

  • Yun Dae-Jin (Division of Applied Life Science (BK21 program), and Environmental Biotechnology National Core Research Center, Gyeongsang National University)
  • 윤대진 (경상대학교 대학원 응용생명과학부)
  • Published : 2005.03.01
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Abstract

Plant responses to salinity stress is critical in determining the growth and development. Therefore, adaptability of plant to salinity stress is directly related with agriculture productivity. Salt adaptation is a result of the integrated functioning of numerous determinants that are regulated coordinately through an appropriate responsive signal transduction cascade. The cascade perceives the saline environment and exerts control over the essential mechanisms that are responsible for ion homeostasis and osmotic adjustment. Although little is known about the component elements of salt stress perception and the signaling cascade(s) in plant, the use of Arabidopsis plant as a molecular genetic tool has been provided important molecular nature of salt tolerance effectors and regulatory pathways. In this review, I summarize recent advances in understanding the molecular mechanisms of salt adaptation.

Keywords

References

  1. Alvim FC, Carolina SM, Cascardo JC, Nunes CC, Martinez CA, Otoni WC, Fontes EP (2001) Enhanced accumulation of BiP in transgenic plants confers tolerance to water stress. Plant Physiol 126: 1042-1054 https://doi.org/10.1104/pp.126.3.1042
  2. Amtmann A, Sanders D (1999) Mechanisms of Na+ uptake by plant cells. In, (eds) Advances in Botanical Research. Academic Press, pp 76-114
  3. Anderson JA, Huprikar SS, Kochian LV, Lucas WJ, Gaber RF (1992) Functional expression of a probable Arabidopsis thaliana potassium channel in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 89: 3736-3740 https://doi.org/10.1073/pnas.89.9.3736
  4. Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285: 1256-1258 https://doi.org/10.1126/science.285.5431.1256
  5. Audran C, Borel C, Frey A, Sotta B, Meyer C, Simonneau T, Marion-Poll A (1998) Expression studies of the zeaxanthin epoxidase gene in Nicotiana plumbaginifolia. Plant Physiol 118: 102-110
  6. Blumwald E, Poole RJ (1985) Na+/H+ antiport in isolated tonoplast vesicles from storage tissue of Beta vulgaris. Plant Physiol 78: 163-167 https://doi.org/10.1104/pp.78.1.163
  7. Bohnert HJ, Shen B (1999) Transformation and compatible solutes. Sci Horticult 78: 237-260
  8. 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 https://doi.org/10.1104/pp.010752
  9. Covic L, Lew RR (1996) Arabidopsis thaliana cDNA isolated by functional complementation shows homology to serine/threonine protein kinases. Biochim Biophys Acta 1305: 125-129 https://doi.org/10.1016/0167-4781(95)00233-2
  10. terization of ARAKIN (ATMEKK1): a possCovic L, Silva NF, Lew RR (1999) Functional characible mediator in an osmotic stress response pathway in higher plants. Biochim Biophys Acta 1451: 242-252 https://doi.org/10.1016/S0167-4889(99)00096-8
  11. Cramer GR, Lynch J, Luchli A, Epstein E (1987) Influx of Na+, K+, and Ca2+ into roots of salt-stressed cotton seedlings. Plant Physiol 83: 510-516 https://doi.org/10.1104/pp.83.3.510
  12. Cunningham KW, Fink GR (1996) Calcineurin inhibits VCX1-depentdent H+/Ca+ exchange and induces Ca2+ ATPases in Saccharomyces cerevisiae. Mol Cell Biol 16: 2226-2237 https://doi.org/10.1128/MCB.16.5.2226
  13. 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
  14. Dietz KJ, Tavakoli N, Kluge C, Miura T, Sharma SS, Harris GC, Chardonnens AN, Golldack, D (2001) Significance of the V-type ATPase for the adaptation to stressful growth conditions and its regulation on the molecular and biochemical level. J Exp Bot 52: 1969-1980 https://doi.org/10.1093/jexbot/52.363.1969
  15. Dreyer I, Horeu C, Lemaillet G, Zimmermann S, Bush DR, Rodriguez-Navarro A, Schachtman DP, Spalding EP, Sentenac H, Gaber RF (1999) Identification and characterization of plant transporters using heterologous expression systems. J Exptl Bot 50: 1073-1087 https://doi.org/10.1093/jexbot/50.suppl_1.1073
  16. Ellul P, RiDS G, Atares A, Roig LA, Serrano R, Moreno V (2003) The expression of the Saccharomyces cerevisiae HAL1 gene increases salt tolerance in transgenic watermelon [Citrullus lanatus (Thunb.) Matsun and Nakai]. Theor Appl Genet 107: 462-469 https://doi.org/10.1007/s00122-003-1267-3
  17. Espinosa-Ruiz A, Belles JM, Serrano R, Gulianez-Macia FA (1999) Arabidopsis thaliana AtHAL3: a flavoproteinrelated to salt and osmotic tolerance and plant growth. Plant J 20: 529-539 https://doi.org/10.1046/j.1365-313X.1999.00626.x
  18. Flowers, TJ, Troke PF, Yeo AR (1977) The mechanism of salt tolerance in halophytes. Annu Rev Plant Physiol 28: 89-121 https://doi.org/10.1146/annurev.pp.28.060177.000513
  19. Garciadeblas B, Rubio F, Quintero FJ, Bauelos MA, Haro R, Rodriguez-Navarro A (1993) Differential expession of two genes encoding isoforms of the ATPase involved in sodium efflux in Saccharomyces cerevisiae. Mol Gen Genet 236: 363-368 https://doi.org/10.1007/BF00277134
  20. 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 Natl Acad Sci USA 96: 1480-1485 https://doi.org/10.1073/pnas.96.4.1480
  21. Geisler M, Frange N, Gomes E, Martinoia E, Palmgren MG (2000). The ACA4 gene of Arabidopsis encodes a vacuolar membrane calcium pump that improves salt tolerance in yeast. Plant Physiol 124: 1814-1827 https://doi.org/10.1104/pp.124.4.1814
  22. Guern J, Mathieu Y, Kurkdjian A (1989) Regulation of vacuolar pH in plant cells. Plant Physiol 89: 27-36 https://doi.org/10.1104/pp.89.1.27
  23. Hasegawa PM, Bressa RA, Zhu J-K, Bohnert H (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51: 463-499 https://doi.org/10.1146/annurev.arplant.51.1.463
  24. Hayashi H, Mustardy L, Deshnium P, Ida M, Murata N (1997). Transformation of Arabidopsis thalianawith the coda gene for choline oxidase; accumulation of glycinebetaine and enhanced tolerance to saIt and cold stress. Plant J 12: 133-142 https://doi.org/10.1046/j.1365-313X.1997.12010133.x
  25. Himmelbach A, Yang Y, Grill E (2003) Relay and control of abscisic acid signaling. Curr Opin Plant Biol 6: 470-479 https://doi.org/10.1016/S1369-5266(03)00090-6
  26. Hirschi, KD (1999) Expression of Arabidopsis CAX1 in tobacco: altered calcium homeostasis and increased stress sensitivity. Plant Cell 11: 2113-2122 https://doi.org/10.1105/tpc.11.11.2113
  27. Hirschi, KD (2004) The calcium conundrum. Both versatile nutrient and specific signal. Plant Physiol 136: 2438-2442 https://doi.org/10.1104/pp.104.046490
  28. Hirsch RE, Lewis BD, Spalding EP, Sussman MR (1998) A role for the AKT1 postassium channel in plant nutrition. Science 280: 918-921 https://doi.org/10.1126/science.280.5365.918
  29. 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 https://doi.org/10.1093/jexbot/51.343.177
  30. Hong Z, Lakkineni ?, Zhang Z, Verma DP (2000) Removal of feedback inhibition of delta(1)-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiol 122: 1129-1136 https://doi.org/10.1104/pp.122.4.1129
  31. Inan G, Zhang Q, Li P, Wang Z, CaD Z, Zhang H, lhang C, Quist TM, Goodwin SM, lhu J, Shi H, Damsz B, Charbaji T, Gong Q, Ma S, Fredricksen M, Galbraith DW, Jenks MA, Rhodes D, Hasegawa PM, Bohnert HJ, Joly RJ, Bressan RA, Zhu J-K (2004) Salt cress. A halophyte and cryophyte Arabidopsis relative model system and its applicability to molecular genetic analyses of growth and development of extremophiles. Plant Physiol 135: 1718-1737 https://doi.org/10.1104/pp.104.041723
  32. Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu. Rev. Plant Physiol. Plant Mol Biol 48: 377-403
  33. 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 https://doi.org/10.1105/tpc.9.11.1935
  34. Iuchi, S, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2000) A stress-inducible gene for 9-cis-epoxycarotenoid dioxygenase involved in abscisic acid biosynthesis under water stress in drought-tolerant cowpea. Plant Physiol123: 553-562 https://doi.org/10.1104/pp.123.2.553
  35. Jeong MJ, Park SC, Byun MO (2001) Improvement of salt tolerance in transgenic potato plants by glyceraldehyde-3-phosphate dehydrogenase gene transfer. Mol Cell 12: 185-189
  36. Kim SA, Kwak JM, Jae SK, Wang MH, Nam HG (2001) Overexpression of the AtGluR2 gene encoding an Arabidopsis homolog of mammalian glutamate receptors impairs calcium utilization and sensitivity to ionic stress intransgenic plants. Plant Cell Physiol 42: 74-84 https://doi.org/10.1093/pcp/pce008
  37. Knight H, Trewavas AJ, Knight MR (1997) Calcium signalling in Arabidopsis thaliana responding to drought and salinity. Plant J 12: 1067-1078 https://doi.org/10.1046/j.1365-313X.1997.12051067.x
  38. 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 9: 4718-4723
  39. Leung J, Giraudat J (1998) Abscisic acid signal transduction. Annu Rev Plant Physiol Plant Mol Biol 49: 199-222 https://doi.org/10.1146/annurev.arplant.49.1.199
  40. Lippuner V, Cyert MS, Gasser CS (1996) Two classes of plant cDNA clones differentially complement yeast calcinerin mutants and increase salt tolerance of wild type yeast. J Biol Chem 271: 12859-12866 https://doi.org/10.1074/jbc.271.22.12859
  41. 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 https://doi.org/10.1073/pnas.94.26.14960
  42. Liu J, Zhu JK (1998) A calcium sensor homolog required for plant salttolerance. Science 280: 1943-1945 https://doi.org/10.1126/science.280.5371.1943
  43. Louis P, Galinski EA (1997) Characterization of genes for the biosynthesis of the compatible solute ectoine from Marinococcus halophilus and osmoregulated expression in E. coli. Microbiol 143: 1141-11 https://doi.org/10.1099/00221287-143-4-1141
  44. 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 https://doi.org/10.1126/science.7624781
  45. Maeda T, Wurgler-Murphy SM, Saito H (1994) A twocomponent system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369: 242-245 https://doi.org/10.1038/369242a0
  46. Martinez V, Luchli A (1993) Effects of Ca2+ on the salt-stress response of barley roots as observed by in-vivo 31P-nuclear magnetic resonance and in-vitro analysis. Planta 190: 519-524
  47. Matsumoto TK, Pardo JM, Takeda S, Bressan RA, Hasegawa PM (2001) Tobacco and Arabidiopsis SLT1 mediate salt tolerance of yeast. Plant Mol Biol 45: 489-500 https://doi.org/10.1023/A:1010659207604
  48. Mazel, A, Leshem, Y, Tiwari BS, Levine A (2004) Induction of salt and osmotic stress tolerance by overexpression of an intracellular vesicle trafficking protein AtRab7 (AtRabG3e). Plant Physiol 134: 118-128 https://doi.org/10.1104/pp.103.025379
  49. McCue KF, Hanson AD (1990) Drought and salt tolerance: Towards understanding and application. Biotechnol. 8: 358-362 https://doi.org/10.1038/nbt0490-358
  50. 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
  51. Mendoza I, Quintero FJ, Bressan RA, Hasegawa PM, Pardo JM (1996) Activated calcineurin confers high tolerance to ion stress and alters the budding pattern and cell morphology of yeast cells. J Biol Chem 227: 23061-23067
  52. 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
  53. Mizoguchi T, Irie K, Hirayam T, Hayashida N, Yamaguchi-Shinozaki K, Matsumoto K, Shinozaki K (1996) A gene encoding a MAP kinase kinase kinase is induced simultaneously with genes for a MAP kinase and an S6 kinase by touch, cold and water stress in Arabidopsis thaliana. Proc Natl Acad Sci USA 93: 765-769 https://doi.org/10.1073/pnas.93.2.765
  54. Mukhopadhyay A, Vij S, Tyagi AK (2004) Overexpression of a zinc-finger protein gene from rice confers tolerance tocold, dehydration, and salt stress in transgenic tobacco. Proc Natl Acad Sci USA 101: 6309-6314 https://doi.org/10.1073/pnas.0401572101
  55. Nakayama H, Yoshida K, Ono H, Murooka Y, Shinmyo A (2000) Ectoine, the compatible solute of Halomonas elongata, confers hyperosmotic tolerance in cultured tobacco cells. Plant Physiol 122: 1239-1247 https://doi.org/10.1104/pp.122.4.1239
  56. Nanjo T, Kobayashi M, Yoshiba Y, Kakubari Y, YamaguchiShinozaki K, Shinozaki K (1999) Antisense suppression of praline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana. FEBS Lett 461: 205-210 https://doi.org/10.1016/S0014-5793(99)01451-9
  57. Nelson DE, Shen B, Bohnert HJ (1998) Salinity tolerance mechanisms, models, and the metabolic engineering of complex traits. In Genetic Engineering, Principles and Methods, ed JK Setlow, pp 153-176, Vol. 20, New York: Plenum Prenum
  58. Niu X, Bressan RA, Hasegawa PM, Pardo JM (1995) Ion homeostasis in NaCl stress environments. Plant Physiol 109: 735-742 https://doi.org/10.1104/pp.109.3.735
  59. Nomura M, lshitani M, Takabe T, Rai AK, Takabe T (1995) Synechococcus sp. PCC7942 transformed with Escherichia coli bet genes produces glycine betaine from choline and acquires resistance to salt stress. Plant Physiol 107: 703-708 https://doi.org/10.1104/pp.107.3.703
  60. Nylander M, Heino P, Helenius E, Palva ET, Ronne H, Welin BV (2001) The low-temperature- and salt-induced RCl2A gene of Arabidopsis complements the sodium sensitivity caused by a deletion of the homologous yeast gene SNA1. Plant Mol Biol 45: 341-351 https://doi.org/10.1023/A:1006451914231
  61. Ono H, Sawada K, Khunajakr N, Tao T, Yamamoto M, Hiramoto M, Shinmyo A, Takano M, Murooka Y (1999) Characterization of biosynthetic enzymes for ectoine as a compatible solute in a moderately halophilic eubacterium, Halomonas elongata. J Bact 181: 91-99
  62. Pardo JM, Reddy MP, Yang S, Maggio A, Huh G-H, Matsumoto T, Coca MA, Paino-D'Urazo M, Koiwa H, Yun D-J, Watad AA, Bressan RA, Hasegawa PM (1998) Stress signalling through Ca2+/calmodulin-dependent protein phosphatase calcineurin mediates salt adaptation in plants. Proc Natl Acad Sci USA 95: 9681-9686 https://doi.org/10.1073/pnas.95.16.9681
  63. Park JM, Park CJ, Lee SB, Ham BK, Shin R, Paek KH (2001) Overexpression of the tobacco Tsi1 gene encoding an EREBP/AP2-type transcription factor enhances resistance against pathogen attack and osmotic stress in tobacco. Plant Cell 13: 1035-1046 https://doi.org/10.1105/tpc.13.5.1035
  64. Piao HL, Pih KT, Lim JH, Kang SG, Jin JB, Kim SH, Hwang I (1999) An Arabidopsis GSK3/shaggy-like gene that complements yeast salt stress-sensitive mutants in induced by NaCl and abscisic acid. Plant Physiol 119: 1527-1534 https://doi.org/10.1104/pp.119.4.1527
  65. Posas F, Camps M, Arino J (1995) The PPZ protein phosphatases are important determinants of salt tolerance in yeast cells. J Biol Chem 207: 13036-13041
  66. Qi Z, Spalding EP (2004) Protection of plasma membrane K+ transport by the salt overly sensitive1 Na+-H+ antiporter during salinity stress. Plant Physiol 136: 2548-2555 https://doi.org/10.1104/pp.104.049213
  67. Quesada, V, Ponce MR, Micol JL (2000) Genetic analysis of salt-tolerant mutants in Arabidopsis thaliana. Genetics 154: 1
  68. Qui QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci USA 99: 8436-8441 https://doi.org/10.1073/pnas.122224699
  69. Quintero FJ, Garciadeblas B, Rodriguez-Navarro A (1996) The SALl gene of Arabidopsis, encoding an enzyme with 3' (2'), 5' -bisphosphate nucleotide and inositol polyphosphate 1-phosphatase activities, increases salt tolerance in yeast. Plant Cell 8: 529-537 https://doi.org/10.1105/tpc.8.3.529
  70. Quintero FJ, Ohta M, Shi H, Zhu J-K, Pardo JM (2002) Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis. Proc Natl Acad Sci USA 99: 9061-9066 https://doi.org/10.1073/pnas.132092099
  71. Rhoades JD, Loveday J (1990) Salinity in irrigated agriculture. in American Society of Civil Engineers, Irrigation of Agricultural Crops (Steward BA and Nielsen DR eds), Am Soc Agronomists, Monograph 30, 1089-1142
  72. Romero C, Belles JM, Vaya JL, Serrano R, Culiaez-Maci FA (1997) Expression of the yeast trehalose-6-phosphate synthase gene in transgenic tobacco plants, pleiotropic phenotypes include drought tolerance, Planta 201: 293-297 https://doi.org/10.1007/s004250050069
  73. Roxas VR, Smigh JRK, Alien ER, Alien RD (1997) Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress, Nature Biotech 15: 988-991 https://doi.org/10.1038/nbt1097-988
  74. Rus A, Lee B-h, Munoz-Mayor A, Sharkhuu A, Miura K, Zhu JK, Bressan RA, Hasegawa PM (2004) AtHKT1 facilitates Na + homeostasis and K+ nutrition in Planta. Plant Physiol 136: 2500-2525 https://doi.org/10.1104/pp.104.042234
  75. Rus A, Yokoi S, Sharkhuu A, Reddy M, Lee B-h, Matsumoto TK, Koiwa H, Zhu JK, Bressan RA, Hasegawa PM (2001) AtHK1 is a salt tolerance determinant that controls Na + entry into plant roots. Proc Natl Acad Sci USA 98: 14150-14155 https://doi.org/10.1073/pnas.241501798
  76. 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
  77. Saleki R, Young P, Lefebvre DD (1993) Mutants of Arabidopsis thaliana capable of germination under saline conditions. Plant Physiol 101: 839-845 https://doi.org/10.1104/pp.101.3.839
  78. Seo M, Koiwai H, Akaba S, Komano T, Oritani T, Kamiya Y, Koshiba T (2000) Abscisic aldehyde oxidase in leaves of Arabidopsis thaliana. Plant J 23: 481-488 https://doi.org/10.1046/j.1365-313x.2000.00812.x
  79. Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative $Na^+/H^+$ antiporter. Proc Natl Acad Sci USA 97: 6896-6901 https://doi.org/10.1073/pnas.120170197
  80. Shi H, Lee BH, Wu SJ, Zhu JK (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nature Biotech 21: 81-85 https://doi.org/10.1038/nbt766
  81. Shi H, Zhu JK (2002) Regulation of expression of the vacuolar $Na^+/H^+$ antiporter gene AtNHX1 by salt stress and ABA. Plant Mol Biol 50: 543-550 https://doi.org/10.1023/A:1019859319617
  82. Shin D, Koo VD, Lee H, Baek D, Lee S, Cheon C, Kwak SS, Lee S, Yun DJ (2004) Athb-12, homeobox-Iecucin zipper domain protein from Arabidopsis thaliana, increases salt tolerance in yeast by regulating sodium exclusion. Biochem Biophys Res Commun 323: 534-540 https://doi.org/10.1016/j.bbrc.2004.08.127
  83. 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 salt-stress requires ABA and is regulated byABA1, ABI1, and AXR2 in Arabidopsis. Plant J 12: 557-569 https://doi.org/10.1046/j.1365-313X.1997.00557.x
  84. Sze H, Li X, Palmgren MG (1999) Enegrization of plant cell membranes by H+-pumping ATPases: Regulation and biosynthesis. Plant Cell 11: 677-689 https://doi.org/10.1105/tpc.11.4.677
  85. Tarczynski M, Jensen RG, Bohnert HJ (1993) Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science 259: 508-510 https://doi.org/10.1126/science.259.5094.508
  86. Tsugane K, Kobayashi K, Niwa Y, Ohba Y, Wada K, Kobayashi H (1999) A recessive Arabidopsis mutant that grows photoautotrophically under salt stress shows enhanced active oxygen detoxification. Plant Cell 11: 1195-1206 https://doi.org/10.1105/tpc.11.7.1195
  87. Urao T, Yakubov B, Satoh R, Yamaguchi-Shinozakia K, Seki B, Hirayama T, Shinozaki K (1999) A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell 11: 1743-1754 https://doi.org/10.1105/tpc.11.9.1743
  88. Villalobos MA, Bartels D, lturriaga G (2004) Stress tolerance and glucose insensitive phenotypes in Arabidopsis overexpressing the CpMYB10 transcription factor gene. Plant Physiol 135: 309-324 https://doi.org/10.1104/pp.103.034199
  89. 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 https://doi.org/10.1104/pp.120.2.473
  90. Xiong L, Gong Z, Rock CD, Subramanian S, Guo Y, Xu W, Galbraith D, Zhu JK (2001) Modulation of abscisic acid signal transduction and biosynthesis by an Sm-like protein in Arabidopsis. Dev Cell 1: 771-781 https://doi.org/10.1016/S1534-5807(01)00087-9
  91. Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14: S165-S183 https://doi.org/10.1105/tpc.010278
  92. Xiong L, Zhu JK (2002) Salt tolerace. In Somerville C, Meyerowitz E, (eds) Arabidopsis book. The American Society of Plant Biology. Rockville, MD pp1-24.
  93. Xiong L, Zhu JK (2003) Regulation of abscisic acid bio synthesis. Plant Physiol 133: 29-36 https://doi.org/10.1104/pp.103.025395
  94. Zhang HX, Blumwald E (2001) Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nature Biotechnol 19: 765-768 https://doi.org/10.1038/90824
  95. Zhu JK (2000) Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol 124: 941-948 https://doi.org/10.1104/pp.124.3.941
  96. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6: 66-71 https://doi.org/10.1016/S1360-1385(00)01838-0
  97. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53: 247-273 https://doi.org/10.1146/annurev.arplant.53.091401.143329
  98. Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6: 441-445 https://doi.org/10.1016/S1369-5266(03)00085-2

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