Signal transduction during cold stress in plants

Physiology and Molecular Biology of Plants

Volumn 14, Issue 1-2, 2008, Pages 69-79

  Solanke, Amolkumar U ^a   Sharma, Arun K ^a  

^a UNIVERSITY OF DELHI   (India)

Author keywords

Calcium; CBF; Cold; Reactive oxygen species; Signal transduction

Indexed keywords

ARABIDOPSIS;

EID: 49349103103     PISSN: 09715894     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12298-008-0006-2     Document Type: Review

References (115)

1. M. Agarwal Y. Hao A. Kapoor C.H. Dong H. Fujii X. Zheng J.K. Zhu 2006 A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance J. Biol. Chem. 281 37636 37645
2. P.S. Aguilar A.M. Hernandez-Arriaga L.E. Cybulski A.C. Erazo D. de Mendoza 2001 Molecular basis of thermosensing: a two-component signal transduction thermometer in Bacillus subtilis EMBO J. 20 1681 1691
3. E.H. Beck S. Fettig C. Knake K. Hartig T. Bhattarai 2007 Specific and unspecific responses of plants to cold and drought stress J. Biosci. 32 501 510
4. Y.H. Cheong K.N. Kim G.K. Pandey R. Gupta J.J. Grant S. Luan 2003 CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis Plant Cell 15 1833 1845
5. V. Chinnusamy M. Ohta S. Kanrar B.H. Lee X. Hong M. Agarwal J.K. Zhu 2003 ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis Genes Dev. 17 1043 1054
6. V. Chinnusamy K. Schumaker J.K. Zhu 2004 Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants J. Exp. Bot. 55 225 236
7. V. Chinnusamy J. Zhu J.K. Zhu 2006 Gene regulation during cold acclimation in plants Physiol. Plant. 126 52 61
8. D. Cook S. Fowler O. Fiehn M.F. Thomashow 2004 A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis Proc. Natl. Acad. Sci. USA 101 15243 15248
9. S. Davletova K. Schlauch J. Coutu R. Mittler 2005 The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis Plant Physiol. 139 847 856
10. O. del Pozo K.F. Pedley G.B. Martin 2004 MAPKKKalpha is a positive regulator of cell death associated with both plant immunity and disease EMBO J. 23 3072 3082
11. R. Deswal G.K. Chowdhary S.K. Sopory 2004 Purification and characterization of a PMA-stimulated kinase and identification of PMA-induced phosphorylation of a polypeptide that is dephosphorylated by low temperature in Brassica juncea Biochem. Biophys. Res. Commun. 322 420 427
12. P. Dhonukshe A.M. Laxalt J. Goedhart T.W. Gadella T. Munnik 2003 Phospholipase D activation correlates with microtubule reorganization in living plant cells Plant Cell 15 2666 2679
13. C.H. Dong M. Agarwal Y. Zhang Q. Xie J.K. Zhu 2006 The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE1 Proc. Natl. Acad. Sci. USA 103 8281 8286
14. I. Ensminger F. Busch N.P.A. Huner 2006 Photostasis and cold acclimation: sensing low temperature through photosynthesis Physiol. Plant. 126 28 44
15. N.H. Evans M.R. McAinsh A.M. Hetherington 2001 Calcium oscillations in higher plants Curr. Plant Biol. 4 415 420
16. V. Fey R. Wagner K. Brautigam T. Pfannschmidt 2005 Photosynthetic redox control of nuclear gene expression J. Exp. Bot. 56 1491 1498
17. S. Fowler M.F. Thomashow 2002 Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway Plant Cell 14 1675 1690
18. J.C. Gardiner J.D. Harper N.D. Weerakoon D.A. Collings S. Ritchie S. Gilroy R.J. Cyr J. Marc 2001 A 90-kD phospholipase D from tobacco binds to microtubules and the plasma membrane Plant Cell 13 2143 2158
19. S.J. Gilmour S.G. Fowler M.F. Thomashow 2004 Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities Plant Mol. Biol. 54 767 781
20. S.J. Gilmour A.M. Sebolt M.P. Salazar J.D. Everard M.F. Thomashow 2000 Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation Plant Physiol. 124 1854 1865
21. G.R. Gray L.P. Chauvin F. Sarhan N. Huner 1997 Cold acclimation and freezing tolerance (A complex interaction of light and temperature) Plant Physiol. 114 467 474
22. L.V. Gusta R. Trischuk C.J. Weiser 2005 Plant cold acclimation: The role of abscisic acid J. Plant Growth Regul. 24 308 318
23. C.L. Guy 1990 Cold acclimation and freezing stress tolerance: Role of protein metabolism Annu. Rev. Plant Physiol. Plant Mol. Biol. 41 187 223
24. 2+ levels Plant, Cell Environ. 26 485 496
25. S.W. Hong J.H. Jon J.M. Kwak H.G. Nam 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 1212
26. N.P.A. Huner G. Oquist F. Sarhan 1998 Energy balance and acclimation to light and cold Trends Plant Sci. 3 224 230
27. M. Inaba I. Suzuki B. Szalontai Y. Kanesaki D.A. Los H. Hayashi N. Murata 2003 Gene-engineered rigidification of membrane lipids enhances the cold inducibility of gene expression in synechocystis J. Biol. Chem. 278 12191 12198
28. M. Ishitani L. Xiong B. Stevenson J.K. Zhu 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
29. K.R. Jaglo-Ottosen S.J. Gilmour D.G. Zarka O. Schabenberger M.F. Thomashow 1998 Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance Science 280 104 106
30. K.R. Jaglo S. Kleff K.L. Amundsen X. Zhang V. Haake J.Z. Zhang T. Deits M.F. Thomashow 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
31. H. Jin M.J. Axtell D. Dahlbeck O. Ekwenna S. Zhang B. Staskawicz B. Baker 2002 NPK1, an MEKK1-like mitogen-activated protein kinase kinase kinase, regulates innate immunity and development in plants Dev. Cell 3 291 297
32. C. Jonak S. Kiegerl W. Ligterink P.J. Barker N.S. Huskisson H. Hirt 1996 Stress signaling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought Proc. Natl. Acad. Sci. USA 93 11274 11279
33. K.N. Kim Y.H. Cheong J.J. Grant G.K. Pandey S. Luan 2003 CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis Plant Cell 15 411 423
34. M. Klimecka G. Muszynska 2007 Structure and functions of plant calcium-dependent protein kinases Acta Biochim. Pol. 54 219 233
35. H. Knight M.R. Knight 2000 Imaging spatial and cellular characteristics of low temperature calcium signature after cold acclimation in Arabidopsis J. Exp. Bot. 51 1679 1686
36. H. Knight M.R. Knight 2001 Abiotic stress signalling pathways: specificity and cross-talk Trends Plant Sci. 6 262 267
37. H. Knight A.J. Trewavas M.R. Knight 1996 Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation Plant Cell 8 489 503
38. H. Knight E.L. Veale G.J. Warren M.R. Knight 1999 The sfr6 mutation in Arabidopsis suppresses low-temperature induction of genes dependent on the CRT/DRE sequence motif Plant Cell 11 875 886
39. M.R. Knight A.K. Campbell S.M. Smith A.J. Trewavas 1991 Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium Nature 352 524 526
40. S. Komatsu G. Yang M. Khan H. Onodera S. Toki M. Yamaguchi 2007 Over-expression of calcium-dependent protein kinase 13 and calreticulin interacting protein 1 confers cold tolerance on rice plants Mol. Genet. Genomics 277 713 723
41. Y. Kovtun W.L. Chiu G. Tena J. Sheen 2000 Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants Proc. Natl. Acad. Sci. USA 97 2940 2945
42. Y. Kovtun W.L. Chiu W. Zeng J. Sheen 1998 Suppression of auxin signal transduction by a MAPK cascade in higher plants Nature 395 716 720
43. J. Kudla Q. Xu K. Harter W. Gruissem S. Luan 1999 Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals Proc. Natl. Acad. Sci. USA 96 4718 4723
44. D. Lecourieux R. Ranjeva A. Pugin 2006 Calcium in plant defence-signalling pathways New Phytol. 171 249 269
45. H. Lee L. Xiong Z. Gong M. Ishitani B. Stevenson J.K. Zhu 2001 The Arabidopsis HOS1 gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold-regulated nucleo-cytoplasmic partitioning Genes Dev. 15 912 924
46. Q. Liu M. Kasuga Y. Sakuma H. Abe S. Miura K. Yamaguchi-Shinozaki K. Shinozaki 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
47. D.A. Los N. Murata 2004 Membrane fluidity and its roles in the perception of environmental signals Biochim. Biophys. Acta. 1666 142 157
48. K. Maruyama Y. Sakuma M. Kasuga Y. Ito M. Seki H. Goda Y. Shimada S. Yoshida K. Shinozaki K. Yamaguchi-Shinozaki 2004 Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems Plant J. 38 982 993
49. J. Medina M. Bargues J. Terol M. Perez-Alonso J. Salinas 1999 The Arabidopsis CBF gene family is composed of three genes encoding AP2 domain-containing proteins whose expression is regulated by low temperature but not by abscisic acid or dehydration Plant Physiol. 119 463 470
50. K. Mikami N. Murata 2003 Membrane fluidity and the perception of environmental signals in cyanobacteria and plants Prog. Lipid. Res. 42 527 543
51. P.V. Minorsky 1989 Temperature sensing by plants: A review and hypothesis Plant Cell Environ. 12 119 135
52. P.V. Minorsky R.M. Spanswick 1989 Electrophysiological evidence for calcium in temperature sensing by roots of cucumber seedlings Plant Cell Environ. 12 137 143
53. R. Mittler 2002 Oxidative stress, antioxidants and stress tolerance Trends Plant Sci. 7 405 410
54. R. Mittler S. Vanderauwera M. Gollery F. Van Breusegem 2004 Reactive oxygen gene network of plants Trends Plant Sci. 9 490 498
55. K. Miura J.B. Jin J. Lee C.Y. Yoo V. Stirm T. Miura E.N. Ashworth R.A. Bressan D.J. Yun P.M. Hasegawa 2007 SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis Plant Cell 19 1403 1414
56. T. Mizoguchi N. Hayashida K. Yamaguchi-Shinozaki H. Kamada K. Shinozaki 1995 Two genes that encode ribosomal-protein S6 kinase homologs are induced by cold or salinity stress in Arabidopsis thaliana FEBS Lett. 358 199 204
57. T. Mizoguchi K. Irie T. Hirayama N. Hayashida K. Yamaguchi-Shinozaki K. Matsumoto K. Shinozaki 1996 A gene encoding a mitogen-activated protein kinase kinase kinase is induced simultaneously with genes for a mitogen-activated protein kinase and an S6 ribosomal protein kinase by touch, cold, and water stress in Arabidopsis thaliana Proc. Natl. Acad. Sci. USA 93 765 769
58. A.F. Monroy Y. Castonguay S. Laberge F. Sarhan L.P. Vezina R.S. Dhindsa 1993 A new cold-induced alfalfa gene is associated with enhanced hardening at subzero temperature Plant Physiol. 102 873 879
59. A.F. Monroy R.S. Dhindsa 1995 Low-temperature signal transduction: induction of cold acclimation-specific genes of alfalfa by calcium at 25 degrees C Plant Cell 7 321 331
60. A.F. Monroy V. Sangwan R.S. Dhindsa 1998 Low temperature signal transduction during cold acclimation: protein phosphatase 2A as an early target for cold-inactivation Plant J. 13 653 660
61. H. Moon B. Lee G. Choi D. Shin D.T. Prasad O. Lee S.S. Kwak D.H. Kim J. Nam J. Bahk J.C. Hong S.Y. Lee M.J. Cho C.O. Lim D.J. Yun 2003 NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants Proc. Natl. Acad. Sci. USA 100 358 363
62. N. Murata D.A. Los 1997 Membrane Fluidity and Temperature Perception Plant Physiol. 115 875 879
63. H. Nakagami A. Pitzschke H. Hirt 2005 Emerging MAP kinase pathways in plant stress signalling Trends Plant Sci. 10 339 346
64. F. Novillo J.M. Alonso J.R. Ecker J. Salinas 2004 CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis Proc. Natl. Acad. Sci. USA 101 3985 3990
65. B.L. Orvar V. Sangwan F. Omann R.S. Dhindsa 2000 Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity Plant J. 23 785 794
66. C. Plieth 2005 Calcium: Just another regulator in the machinery of life? Ann. Bot. (Lond.) 96 1 8
67. C. Plieth U.P. Hansen H. Knight M.R. Knight 1999 Temperature sensing by plants: the primary characteristics of signal perception and calcium response Plant J. 18 491 497
68. T.K. Prasad M.D. Anderson B.A. Martin C.R. Stewart 1994 Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide Plant Cell 6 65 74
69. Ray, S., Agarwal, P., Arora, R., Kapoor, S. and Tyagi, A.K. (2007). Expression analysis of calcium-dependent protein kinase gene family during reproductive development and abiotic stress conditions in rice (Oryza sativa L. ssp. indica). Mol. Genet. Genomics, (DOI 10.1007/s00438-007-0267-4)
70. V.S. Reddy A.S. Reddy 2004 Proteomics of calcium-signaling components in plants Phytochemistry 65 1745 1776
71. E. Ruelland C. Cantrel M. Gawer J.C. Kader A. Zachowski 2002 Activation of phospholipases C and D is an early response to a cold exposure in Arabidopsis suspension cells Plant Physiol. 130 999 1007
72. 2+-dependent protein kinase that endows rice plants with cold-and salt-stress tolerance functions in vascular bundles Plant Cell Physiol. 42 1228 1233
73. Salinas, J. (2002) Molecular mechanisms of signal transduction in cold acclimation. In: Plant Signal Transduction (Eds. Scheel D. and Wasternack C.) Oxford University Press, pp. 116-139.
74. 2+ influx Plant J. 27 1 12
75. V. Sangwan B.L. Orvar J. Beyerly H. Hirt R.S. Dhindsa 2002 Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways Plant J. 31 629 638
76. F. Sarhan J. Danyluk 1998 Engineering cold-tolerant crops-throwing the master switch Trends Plant Sci. 3 289 290
77. S. Sarhan J.M. Hitchcock C.A. Grauffel J.G. Wettstein 1997 Comparative antipsychotic profiles of neurotensin and a related systemically active peptide agonist Peptides 18 1223 1227
78. 2+ signals in plants CRC Crit. Rev. Plant Sci. 23 1 11
79. P. Sharma N. Sharma R. Deswal 2005 The molecular biology of the low-temperature response in plants BioEssays 27 1048 1059
80. K. Shinozaki K. Yamaguchi-Shinozaki M. Seki 2003 Regulatory network of gene expression in the drought and cold stress responses Curr. Opin. Plant Biol. 6 410 417
81. H. Shou P. Bordallo J.B. Fan J.M. Yeakley M. Bibikova J. Sheen K. Wang 2004 Expression of an active tobacco mitogen-activated protein kinase kinase kinase enhances freezing tolerance in transgenic maize Proc. Natl. Acad. Sci. USA 101 3298 3303
82. H. Shou P. Bordallo K. Wang 2004 Expression of the Nicotiana protein kinase (NPK1) enhanced drought tolerance in transgenic maize J. Exp. Bot. 55 1013 1019
83. E.J. Stockinger S.J. Gilmour M.F. Thomashow 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 1040
84. E.J. Stockinger Y. Mao M.K. Regier S.J. Triezenberg M.F. Thomashow 2001 Transcriptional adaptor and histone acetyltransferase proteins in Arabidopsis and their interactions with CBF1, a transcriptional activator involved in cold-regulated gene expression Nucleic Acids Res. 29 1524 1533
85. 2+ signal in maize suspension-cultured cells Plant Physiol. 118 759 771
86. I. Suzuki D.A. Los N. Murata 2000 Perception and transduction of low-temperature signals to induce desaturation of fatty acids Biochem. Soc. Trans. 28 628 630
87. N. Suzuki R. Mittler 2006 Reactive oxygen species and temperature stresses: A delicate balance between signaling and destruction Phisiol. Plant. 126 45 51
88. S. Tahtiharju V. Sangwan A.F. Monroy R.S. Dhindsa M. Borg 1997 The induction of kin genes in cold-acclimating Arabidopsis thaliana. Evidence of a role for calcium Planta 203 442 447
89. M.F. Thomashow 1998 Role of cold-responsive genes in plant freezing tolerance Plant Physiol. 118 1 7
90. M.F. Thomashow 1999 Plant cold acclimation: Freezing tolerance genes and regulatory mechanisms Annu. Rev. Plant Physiol. Plant Mol. Biol. 50 571 599
91. M. Uemura R.A. Joseph P.L. Steponkus 1995 Cold acclimation of Arabidopsis thaliana (Effect on plasma membrane lipid composition and freeze-induced lesions) Plant Physiol. 109 15 30
92. T. Urao S. Miyata K. Yamaguchi-Shinozaki K. Shinozaki 2000 Possible His to Asp phosphorelay signaling in an Arabidopsis two-component system FEBS Lett. 478 227 232
93. T. Urao B. Yakubov R. Satoh K. Yamaguchi-Shinozaki M. Seki T. Hirayama K. Shinozaki 1999 A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor Plant Cell 11 1743 1754
94. T. Urao K. Yamaguchi-Shinozaki K. Shinozaki 2000 Two-component systems in plant signal transduction Trends Plant Sci. 5 67 74
95. H.A. Van Buskirk M.F. Thomashow 2006 Arabidopsis transcription factors regulating cold acclimation Phisiol. Plant. 126 72 80
96. A.H. van der Luit C. Olivari A. Haley M.R. Knight A.J. Trewavas 1999 Distinct calcium signaling pathways regulate calmodulin gene expression in tobacco Plant Physiol. 121 705 714
97. M.N. Vaultier C. Cantrel C. Vergnolle A.M. Justin C. Demandre G. Benhassaine-Kesri D. Cicek A. Zachowski E. Ruelland 2006 Desaturase mutants reveal that membrane rigidification acts as a cold perception mechanism upstream of the diacylglycerol kinase pathway in Arabidopsis cells FEBS Lett. 580 4218 4223
98. S. Vij A.K. Tyagi 2007 Emerging trends in the functional genomics of the abiotic stress response in crop plants Plant Biotechnol. J. 5 361 380
99. J.T. Vogel D.G. Zarka H.A. Van Buskirk S.G. Fowler M.F. Thomashow 2005 Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis Plant J. 41 195 211
100. X. Wang W. Li M. Li R. Welti 2006 Profiling lipid changes in plant response to low temperatures Phisiol. Plant. 126 90 96
101. C. Widmann S. Gibson M.B. Jarpe G.L. Johnson 1999 Mitogen-Activated Protein Kinase: Conservation of a three-kinase module from yeast to human Phisiol. Review 79 143 180
102. Y. Xiang Y. Huang L. Xiong 2007 Characterization of stress-responsive CIPK genes in rice for stress tolerance improvement Plant Physiol. 144 1416 1428
103. Z. Xin J. Browse 1998 Eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant Proc. Natl. Acad. Sci. USA 95 7799 7804
104. Z. Xin A. Mandaokar J. Chen R.L. Last J. Browse 2007 Arabidopsis ESK1 encodes a novel regulator of freezing tolerance Plant J. 49 786 799
105. L. Xiong K.S. Schumaker J.K. Zhu 2002 Cell signaling during cold, drought, and salt stress Plant Cell 14 Suppl S165 S183
106. K. Yamaguchi-Shinozaki K. Shinozaki 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. 236 331 340
107. K. Yamaguchi-Shinozaki K. Shinozaki 1994 A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress Plant Cell 6 251 264
108. K. Yamaguchi-Shinozaki K. Shinozaki 2005 Organization of cis-acting regulatory elements in osmotic-and cold-stress-responsive promoters Trends Plant Sci. 10 88 94
109. K. Yamaguchi-Shinozaki K. Shinozaki 2006 Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses Annu. Rev. Plant Biol. 57 781 803
110. T. Yang B.W. Poovaiah 2003 Calcium/calmodulin-mediated signal network in plants Trends Plant Sci. 8 505 512
111. X. Zhang S.G. Fowler H. Cheng Y. Lou S.Y. Rhee E.J. Stockinger M.F. Thomashow 2004 Freezing-sensitive tomato has a functional CBF cold response pathway, but a CBF regulon that differs from that of freezing-tolerant Arabidopsis Plant J. 39 905 919
112. J. Zhu C.H. Dong J.K. Zhu 2007 Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation Curr. Opin. Plant Biol. 10 290 295
113. J. Zhu H. Shi B.H. Lee B. Damsz S. Cheng V. Stirm J.K. Zhu P.M. Hasegawa R.A. Bressan 2004 An Arabidopsis homeodomain transcription factor gene, HOS9, mediates cold tolerance through a CBF-independent pathway Proc. Natl. Acad. Sci. USA 101 9873 9878
114. J. Zhu P.E. Verslues X. Zheng B.H. Lee X. Zhan Y. Manabe I. Sokolchik Y. Zhu C.H. Dong J.K. Zhu P.M. Hasegawa R.A. Bressan 2005 HOS10 encodes an R2R3-type MYB transcription factor essential for cold acclimation in plants Proc. Natl. Acad. Sci. USA 102 9966 9971
115. J.K. Zhu 2001 Cell signaling under salt, water and cold stresses Curr. Opin. Plant Biol. 4 401 406