Salt and drought stress signal transduction in plants

Annual Review of Plant Biology

Volumn 53, Issue , 2002, Pages 247-273

  Zhu, Jian Kang ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

Abscisic acid; Calcium signaling; Gene expression; Osmotic stress; Phospholipid; Protein kinase; SOS

Indexed keywords

ABSCISIC ACID; PROTEIN KINASE; SODIUM CHLORIDE; WATER;

BIOSYNTHESIS; HOMEOSTASIS; METABOLISM; OSMOTIC PRESSURE; PHYSIOLOGY; PLANT; REVIEW; SIGNAL TRANSDUCTION;

ABSCISIC ACID; HOMEOSTASIS; OSMOTIC PRESSURE; PLANTS; PROTEIN KINASES; SIGNAL TRANSDUCTION; SODIUM CHLORIDE; WATER;

EID: 0036999615     PISSN: 15435008     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.arplant.53.091401.143329     Document Type: Review

References (123)

1. Abel H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K. 1997. Role of Arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. Plant Cell 9:1859-68
2. + uptake by plant cells. Adv. Bot. Res. 29:75-112
3. +-antiport in Arabidopsis. Science 285:1256-58
4. Bastola DR, Pethe VV, Winicov I. 1998. Alfin1, a novel zinc-finger protein in alfalfa roots that binds to promoter elements in the salt-inducible MsPRP2 gene. Plant Mol. Biol. 38:1123-35
5. Berridge MJ, Irvine RF. 1989. Inositol phosphate and cell signaling. Nature 341:197-205
6. Boyer JS. 1982. Plant productivity and environment. Science 218:443-48
7. Bray EA. 1993. Molecular responses to water deficit. Plant Physiol. 103:1035-40
8. Burssens S, Himanen K, van de Cotte B, Beeckman T, van Montagu M. 2000 Expression of cell cycle regulatory genes and morphological alterations in response to salt stress in Arabidopsis thaliana. Planta 211:632-40
9. Chen HH, Li PH, Brenner ML. 1983. Involvement of abscisic acid in potato cold acclimation. Plant Physiol. 71:362-65
10. Choi HI, Hong JH, Ha JO, Kang JY, Kim SY. 2000. ABFs, a family of ABA-responsive element binding factors. J. Biol. Chem. 275:1723-30
11. DeWald DB, Torabinejad J, Jones CA, Shope JC, Cangelosi AR, et al. 2001. Rapid accumulation of phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate correlates with calcium mobilization in salt-stressed Arabidopsis. Plant Physiol. 126:759-69
12. Dove SK, Cooke FT, Douglas MR, Sayers LG, Parker PJ, Michell RH. 1997. Osmotic stress activates phosphatidylinositol-3,5-bisphosphate synthesis. Nature 390:187-92
13. Drobak BK, Watkins PA. 2000. Inositol (1,4,5)trisphosphate production in plant cells: an early response to salinity and hyperosmotic stress. FEBS Lett. 481:240-44
14. Droillard MJ, Thibivilliers S, Cazale AC, Barbier-Brygoo H, Lauriere C. 2000. Protein kinases induced by osmotic stresses and elicitor molecules in tobacco cell suspensions: two crossroad MAP kinases and one osmoregulation-specific protein kinase. FEBS Lett. 474:217-22
15. Einspahr KJ, Maeda M, Thompson GA Jr. 1988. Concurrent changes in Dunaliella salina ultrastructure and membrane phospholipid metabolism after hyperosmotic shock. J. Cell Biol. 107:529-38
16. El Maarouf H, Zuily-Fodil Y, Gareil M, d'Arcy-Lameta A, Pham-Thi AT. 1999. Enzymatic activity and gene expression under water stress of phospholipase D in two culitivars of Vigna unguiculata L. Walp. differing in drought tolerance. Plant Mol. Biol. 39:1257-65
17. English D. 1996. Phosphatidic acid: a lipid messenger involved in intracellular and extracellular signaling. Cell. Signal. 8:341-47
18. Epstein E, Norlyn JD, Rush DW, Kingsbury RW, Kelly DB, et al. 1980. Saline culture of crops: a genetic approach. Science 210:399-404
19. Finkelstein RR, Lynch TJ. 2000. The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcriptional factor. Plant Cell 12:599-609
20. Frank W, Munnik T, Kerkmann K, Salamini F, Bartels D. 2000. Water deficit triggers phospholipase D activity in the resurrection plant Craterostigma plantagineum. Plant Cell 12:111-23
21. Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF. 1998. Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J. 16:433-42
22. Guiltinan MJ, Marcotte WR, Quatrano RS. 1990. A plant leucine zipper protein that recognizes an abscisic acid response element. Science 250:267-71
23. Guo Y, Halfter U, Ishitani M, Zhu JK. 2001. Molecular characterization of functional domains in the protein kinase SOS2 that is required for plant salt tolerance. Plant Cell 13:1383-400
24. Gustin MC, Albertyn J, Alexander M, Davenport K. 1998. MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 62:1264-300
25. 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 97:3730-34
26. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ. 2000. Plant cellular and molecular responses to high salinity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51:463-99
27. Heilmann I, Perera IY, Gross W, Boss WF. 1999. Changes in phosphoinositide metabolism with days in culture affect signal transduction pathways in Galdieria suphuraria. Plant Physiol. 119:1331-39
28. 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 92:3903-7
29. Hobo T, Kowyama Y, Hattori T. 1999. A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proc. Natl. Acad. Sci. USA 96:15348-53
30. Hong SW, Jon JH, Kwak JM, Nam HG. 1997. Identification of a receptor-like protein kinase gene rapidly induced by abscisic acid, dehydration, high salt, and cold treatments in Arabidopsis thaliana. Plant Physiol. 113:1203-12
31. Hoyos ME, Zhang S. 2000. Calcium-independent activation of salicylic acid-induced protein kinase and a 40-kilodalton protein kinase by hyperosmotic stress. Plant Physiol. 122:1355-63
32. Ichimura K, Mizoguchi T, Yoshida R, Yuasa T, Shinozaki K. 2000. Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant J. 24:655-65
33. Ingram J, Bartels D. 1996. The molecular basis of dehydration tolerance in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:377-403
34. Ishitani M, Liu J, Halfter U, Kim CS, Wei M, Zhu JK. 2000. SOS3 function in plant salt tolerance requires myristoylation and calcium-binding. Plant Cell. 12:1667-77
35. Ishitani M, Xiong L, Stevenson B, Zhu JK. 1997. Genetic analysis of osmotic and cold stress signal transduction in Arabidopsis thaliana: interactions and convergence of abscisic acid-dependent and abscisic acid-independent pathways. Plant Cell 9:1935-49
36. Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, et al. 2001. Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J. 27:325-33
37. Jacob T, Ritchie S, Assmann SM, Gilroy S. 1999. Abscisic acid signal transduction in guard cells is mediated by phospholipase D activity. Proc. Natl. Acad. Sci. USA 96:12192-97
38. Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF. 1998. Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104-6
39. Jonak C, Kiegerl S, Ligterink W, Barker PJ, Huskisson NS, Hirt H. 1996. Stress signaling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought. Proc. Natl. Acad. Sci. USA 93:11274-79
40. 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. 17:287-91
41. Katagiri T, Takahashi S, Shinozaki K. 2001. Involvement of a novel Arabidopsis phospholipase D, AtPLD delta, in dehydration-inducible accumulation of phosphatidic acid in stress signaling. Plant J. 26:595-605
42. Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, et al. 2001. Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13:889-906
43. Kiegerl S, Cardinale F, Siligan C, Gross A, Baudouin E, et al. 2000. SIMKK, a mitogen-activated protein kinase (MAPK) kinase, is a specific activator of the salt stress-induced MAPK, SIMK. Plant Cell 12:2247-58
44. Knight H, Trewavas AJ, Knight MR. 1997. Calcium signaling in Arabidopsis thaliana responding to drought and salinity. Plant J. 12:1067-78
45. Koornneef M, Léon-Kloosterziel KM, Schwartz SH, Zeevaart JAD. 1998. The genetic and molecular dissection of abscisic acid biosynthesis and signal transduction in Arabidopsis. Plant Physiol. Biochem. 36:83-89
46. 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 97:2940-45
47. Krochko JE, Abrams GD, Loewen MK, Abrams SR, Culter AJ. 1998. (+)-abscisic acid 8′-hydroxylase is a cytochrome P450 monooxygenase. Plant Physiol. 118:849-60
48. Lang V, Mantyla E, Welin B, Sundberg B, Palva ET. 1994. Alterations in water status, endogenous abscisic acid content, and expression of rab18 gene during the development of freezing tolerance in Arabidopsis thaliana. Plant Physiol. 104:1341-49
49. 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. 15:912-24
50. Lee Y, Choi YB, Suh J, Lee J, Assmann SM, et al. 1996. Abscisic acid-induced phosphoinositide turnover in guard cell protoplasts of Vicia faba. Plant Physiol. 110:987-96
51. Lemtiri-Chlieh F, MacRobbie EAC, Brearley CA. 2000. Inositol hexakisphosphate is a physiological signal regulating the K+-inward rectifying conductance in guard cells. Proc. Natl. Acad. Sci. USA 97:8687-92
52. Leng Q, Mercier RW, Yao W, Berkowitz GA. 1999. Cloning and first functional chracterization of a plant cyclic nucleotide-gated cation channel. Plant Physiol. 121:753-61
53. Leung J, Giraudat J. 1998. Abscisic acid signal transduction. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49:199-222
54. Liotenberg S, North H, Marion-Poll A. 1999. Molecular biology and regulation of abscisic acid biosynthesis in plants. Plant Physiol. Biochem. 37:341-50
55. Liu J, Ishitani M, Halfter U, Kim CS, Zhu JK. 2000. The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc. Natl. Acad. Sci. USA 97:3735-40
56. Liu J, Zhu JK. 1997. Proline accumulation and salt-stress-induced gene expression in a salt-hypersensitive mutant of Arabidopsis. Plant Physiol. 114:591-96
57. Liu J, Zhu JK. 1998. A calcium sensor homolog required for plant salt tolerance. Science 280:1943-45
58. Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, et al. 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 10:1391-406
59. Liu Y, Zhang S, Klessig DF. 2000. Molecular cloning and characterization of a tobacco MAP kinase kinase that interacts with SIPK. Mol. Plant Microbe Interact. 13:118-24
60. Llorente F, Oliveros JC, Martinez-Zapater JM, Salinas J. 2000. A freezing-sensitive mutant of Arabidopsis, frs1, is a new aba3 allele. Planta 211:648-55
61. Maathuis F, Sanders D. 2001. Sodium uptake in Arabidopsis roots is regulated by cyclic nucleotides. Plant Physiol. In press
62. Majerus PW. 1992. Inositol phosphate biochemistry. Annu. Rev. Biochem. 61: 225-50
63. Marin E, Nussaume L, Quesada A, Gonneau M, Sotta B, et al. 1996. Molecular identification of zeaxanthin epoxidase of Nicotiana plumbaginifolia, a gene involved in abscisic acid biosynthesis and corresponding to the ABA locus of Arabidopsis thaliana. EMBO J. 15:2331-42
64. Meijer HJG, Divecha N, van den Ende H, Musgrave A, Munnik T. 1999. Hyperosmotic stress induces rapid synthesis of phosphatidyl-D-inositol 3,5-bisphosphate in plant cells. Planta 208:294-98
65. Mikami K, Katagiri T, Luchi S, Yamaguchi-Shinozaki K, Shinozaki K. 1998. A gene encoding phosphatidylinositol 4-phosphate 5-kinase is induced by water stress and abscisic acid in Arabidopsis thaliana. Plant J. 15:563-68
66. Mikolajczyk M, Olubunmi SA, Muszynska G, Klessig DF, Dobrowolska G. 2000. Osmotic stress induces rapid activation of a salicylic acid-induced protein kinase and a homolog of protein kinase ASK1 in tobacco cells. Plant Cell 12:165-78
67. Mizoguchi T, Ichimura K, Yoshida R, Shinozaki K. 2000. MAP kinase cascades in Arabidopsis: their roles in stress and hormone responses. Results Probl. Cell Differ. 27:29-38
68. Munnik T, Irvine RF, Musgrave A. 1998. Phospholipid signaling in plants. Biochim. Biophys. Acta 1389:222-72
69. Munnik T, Ligterink W, Meskiene I, Calderini O, Beyerly J, et al. 1999. Distinct osmosensing protein kinase pathways are involved in signalling moderate and severe hyperosmotic stress. Plant J. 20:381-88
70. Munnik T, Meijer HJG. 2001. Osmotic stress activates distinct lipid and MAPK signaling pathways in plants. FEBS Lett. 498:172-78
71. Munnik T, Meijer HJG, ter Riet B, Frank W, Bartels D, Musgrave A. 2000. Hyperosmotic stress stimulates phospholipase D activity and elevates the levels of phosphatidic acid and diacylglycerol pyrophosphate. Plant J. 22:147-54
72. Nakagawa H, Ohmiya K, Hattori T. 1996. A rice bZIP protein, designated OSBZ8, is rapidly induced by abscisic acid. Plant J. 9:217-27
73. Nakashima K, Shinwari ZK, Sakuma Y, Seki M, Miura S, et al. 2000. Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration- and high-salinity-responsive gene expression. Plant Mol. Biol. 42:657-65
74. Nantel A, Quatrano RS. 1996. Characterization of three rice basic/leucine zipper factors, including two inhibitors of EmBP-1 DNA binding activity. J. Biol. Chem. 271:31296-305
75. Ng CK, Carr K, McAinsh MR, Powell B, Hetherington AM. 2001. Drought-induced guard cell signal transduction involves sphingosine-1-phosphate. Nature 410:596-99
76. Oeda K, Salinas J, Chua NH. 1991. A tobacco bZip transcription activator (TAF-1) binds to a G-box-like motif conserved in plant genes. EMBO J. 10:1793-802
77. Ozcan S, Dover J, Johnston M. 1998. Glucose sensing and signaling by two glucose receptors in the yeast Saccharomyces cerevisiae. EMBO J. 17:2566-73
78. Posas F, Chambers JR, Heyman JA, Hoeffler JP, de Nada E, Arino J. 2000. The transcriptional response of yeast to salt stress. J. Biol. Chem. 275:17249-55
79. Qin X, Zeevaart JAD. 1999. The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proc. Natl. Acad. Sci. USA 96:15354-61
80. + exchanger in Arabidopsis thaliana. Abstr. Int. Workshop Plant Membr. Biol., 12th, Madison, Wis., pp. 235
81. Quintero FJ, Garciadeblas B, Rodriguez-Navarro A. 1996. The SAL1 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 8:529-37
82. Rep M, Krantz M, Thevelein JM, Hohmann S. 2000. The transcriptional response of Saccharomyces cerevisiae to osmotic shock. J. Biol. Chem. 275:8290-300
83. + entry into plant roots. Proc. Natl. Acad. Sci. USA. 98:14150-55
84. Sanchez JP, Chua NH. 2001. Arabidopsis PLC1 is required for secondary responses to abscisic acid signals. Plant Cell 13:1143-54
85. Sanders D, Brownlee C, Harper JF. 1999. Communicating with calcium. Plant Cell 11:691-706
86. Sang Y, Cui D, Wang X. 2001. Phospholipase D and phosphatidic acid-mediated generation of superoxide in Arabidopsis. Plant Physiol. 126:1449-58
87. Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D. 2001. Guard cell signal transduction. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52:627-58
88. 2+ from vacuolar membrane vesicles of oat roots. J. Biol. Chem. 262:3944-46
89. Schuppler U, He PH, John PCL, Munns R. 1998. Effects of water stress on cell division and cell-division-cycle-2-like cell-cycle kinase activity in wheat leaves. Plant Physiol. 117:667-78
90. Seo M, Peeters AJM, Koiwai H, Oritani T, Marion-Poll A, et al. 2000. The Arabidopsis aldehyde oxidase 3 (AAO3) gene product catalyzes the final step in abscisic acid biosynthesis in leaves. Proc. Natl. Acad. Sci. USA 97:12908-13
91. Seo S, Okamoto M, Seto H, Ishizuka K, Sano H, Ohashi Y. 1995. Tobacco MAP kinase: a possible mediator in wound signal transduction pathways. Science 270:1988-92
92. Shears SB. 1992. Metabolism of inositol phosphates. Adv. Second Messenger Phosphoprot. Res. 26:63-92
93. 2+ dependent protein kinases and stress signal transduction in plants. Science 274:1900-2
94. + antiporter. Proc. Natl. Acad. Sci. USA 97: 6896-901
95. + transport in plants. Plant Cell. In press
96. Shi H, Xiong L, Stevenson B, Lu T, Zhu J-K. 2002. The Arabidopsis salt overly sensitive 4 mutants uncover a critical role for vitamin B6 in plant salt tolerance. Plant Cell. In press
97. Shinozaki K, Yamaguchi-Shinozaki K. 1997. Gene expression and signal transduction in water-stress response. Plant Physiol. 115:327-34
98. Shinwari ZK, Nakashima K, Miura S, Kasuga M, Seki M, et al. 1998. An Arabidopsis gene family encoding DRE/JCRT binding proteins involved in low-temperature-responsive gene expression. Biochem. Biophys. Res. Commun. 250:161-70
99. Stockinger EJ, Gilmour SJ, Thomashow MF. 1997. Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc. Natl. Acad. Sci. USA 94:1035-40
100. Takahashi S, Katagiri T, Hirayama T, Yamaguchi-Shinozaki K, Shinozaki K. 2001. Hyperosmotic stress induced a rapid and transient increase in inositol 1,4,5-trisphosphate independent of abscisic acid in Arabidopsis cell culture. Plant Cell Physiol. 42:214-22
101. Tan BC, Schwartz SH, Zeevaart JAD, McCarty DR. 1997. Genetic control of abscisic acid biosynthesis in maize. Proc. Natl. Acad. Sci. USA 94:12235-40
102. Thompson AJ, Jackson AC, Symonds RC, Mulholland BJ, Dadswell AR, et al. 2000. Ectopic expression of a tomato 9-cis-epoxycarotenoid dioxygenase gene causes overproduction of abscisic acid. Plant J. 23:363-74
103. Tyerman SD, Skerrett IM. 1999. Root ion channels and salinity. Sci. Hortic. 78:175-235
104. Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K. 2000. Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc. Natl. Acad. Sci. USA 97:11632-37
105. + uptake in Saccharomyces cerevisiae. Plant Physiol. 122:1249-60
106. Urao T, Noji M, Yamaguchi-Shinozaki K, Shinozaki K. 1996. A transcriptional activation domain of ATMYB2, a drought-inducible Arabidopsis Myb-related protein. Plant J. 10:1145-48
107. Urao T, Yakubov B, Satoh R, Yamaguchi-Shinozaki K, Seki B, et al. 1999. A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell 11:1743-54
108. Wang H, Qi Q, Schorr P, Cutler AJ, Crosby WL, Fowke LC. 1998. ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis thaliana interacts with both Cdc2a and CycD3, and its expression is induced by abscisic acid. Plant J. 15:501-10
109. Wu SJ, Lei D, Zhu JK. 1996. SOS1, a genetic locus essential for salt tolerance and potassium acquisition. Plant Cell 8: 617-27
110. Wu Y, Kuzma J, Marechal E, Graeff R, Lee HC, et al. 1997. Abscisic acid signaling through cyclic ADP-ribose in plants. Science 278:2126-30
111. Xiong L, Ishitani M, Lee H, Zhu JK. 1999. HOS5 - a negative regulator of osmotic stress-induced gene expression in Arabidopsis thaliana. Plant J. 19:569-78
112. Xiong L, Ishitani M, Lee H, Zhu JK. 2001. The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold and osmotic stress responsive gene expression. Plant Cell. 13:2063-83
113. Xiong L, Ishitani M, Zhu JK. 1999. Interaction of osmotic stress, ABA and low temperature in the regulation of stress gene expression in Arabidopsis thaliana. Plant Physiol. 119:205-11
114. Xiong L, Lee BH, Ishitani M, Lee H, Zhang C, Zhu JK. 2001. FIERY1 encoding an inositol polyphosphate 1-phosphatase is a negative regulator of abscisic acid and stress signaling in Arabidopsis. Genes Dev. 15:1971-84
115. Xiong L, Zhu JK. 2001. Abiotic stress signal transduction in plants: molecular and genetic perspectives. Physiol. Plant 112:152-66
116. Yale J, Bohnert HJ. 2001. Transcript expression in S. cerevisiae at high salinity. J. Biol. Chem. 276:15996-6007
117. Yamaguchi-Shinozaki K, Shinozaki K. 1993. Characterization of the expression of a desiccation-responsive rd29 gene of Arabidopsis thaliana and analysis of its promoter in transgenic plants. Mol. Gen. Genet. 236:331-40
118. Yamaguchi-Shinozaki K, Shinozaki K. 1994. A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6:251-64
119. Zhu JK. 2000. Genetic analysis of plant salt tolerance using Arabidopsis thaliana. Plant Physiol. 124:941-48
120. Zhu JK. 2001. Cell signaling under salt, water and cold stresses. Curr. Opin. Plant Biol. 4:401-6
121. Zhu JK. 2001. Plant salt tolerance. Trends Plant Sci. 6:66-71
122. Zhu JK, Hasegawa PM, Bressan RA. 1996. Molecular aspects of osmotic stress in plants. Crit. Rev. Plant Sci. 16:253-77
123. Zhu JK, Liu J, Xiong L. 1998. Genetic analysis of salt tolerance in Arabidopsis thaliana: evidence of a critical role for potassium nutrition. Plant Cell 10:1181-92