Plant cold acclimation: Freezing tolerance genes and regulatory mechanisms

Annual Review of Plant Biology

Volumn 50, Issue , 1999, Pages 571-599

  Thomashow, Michael F ^a  

^a Michigan State University ^*  (United States)

Author keywords

Cold acclimation; Environmental stress; Freezing tolerance; Gene regulation; Signal transduction

Indexed keywords

ARABIDOPSIS;

EID: 0033498862     PISSN: 15435008     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.arplant.50.1.571     Document Type: Article

References (131)

1. Anchordoguy TJ, Rudolph AS, Carpenter JF, Crowe JH. 1987. Modes of interaction of cryoprotectants with membrane phospholipids during freezing. Cryobiology 24:324-31
2. Anderson JV, Li QB, Haskell DW, Guy CL. 1994. Structural organization of the spinach endoplasmic reticulum-luminal 70-kilodalton heat-shock cognate gene and expression of 70-kilodalton heat-shock genes during cold acclimation. Plant Physiol. 104:1359-70
3. Antikainen M, Griffith M. 1997. Antifreeze protein accumulation in freezing-tolerant cereals. Physiol. Plant. 99:423-32
4. Artus NN, Uemura M, Steponkus PL, Gilmour SJ, Lin CT, Thomashow MF. 1996. Constitutive expression of the cold-regulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance. Proc. Natl. Acad. Sci. USA 93:13404-9
5. Baker SS, Wilhelm KS, Thomashow MF. 1994. The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol. Biol. 24:701-13
6. Brule-Babel AL, Fowler DB. 1988. Genetic control of cold hardiness and vernalization requirement in winter wheat. Crop Sci. 28:879-84
7. Carpenter JF, Hand SC, Crowe LM, Crowe JH. 1986. Cryoprotection of phosphofructokinase with organic solutes: characterization of enhanced protection in the presence of divalent cations. Arch. Biochem. Biophys. 250:505-12
8. Chen H-H, Li PH, Brenner ML. 1983. Involvement of abscisic acid in potato cold acclimation. Plant Physiol. 71:362-65
9. Close TJ. 1997.Dehydrins: a commonality in the response of plants to dehydration and low temperature. Physiol. Plant. 100:291-96
10. Ding JP, Pickard BG. 1993. Modulation of mechanosensitive calcium-selective cation channels by temperature. Plant J. 3:713-20
11. Duman JG. 1994. Purification and characterization of a thermal hysteresis protein from a plant, the bittersweet nightshade Solanum dulcamara. Biochim. Biophys. Acta 1206:129-35
12. Dunn MA, Goddard NJ, Zhang L, Pearce RS, Hughes MA. 1994. Low-temperature-responsive barley genes have different control mechanisms. Plant Mol. Biol. 24:879-88
13. Dure L III. 1993. A repeating 11-mer amino acid motif and plant desiccation. Plant J. 3:363-69
14. Epand RM, Shai Y, Segrest JP, Anantharamaiah GM. 1995. Mechanisms for the modulation of membrane bilayer properties by amphipathic helical peptides. Biopolymers 37:319-38
15. Foster R, Izawa T, Chua NH. 1994. Plant bZIP proteins gather at ACGT elements. FASEB J. 8:192-200
16. Fowler DB, Gusta LV. 1979. Selection for winterhardiness in wheat. I. Identification of genotypic variability. Crop Sci. 19:769-72
17. Galiba G, Quarrie SA, Sutka J, Morounov A, Snape JW. 1995. RFLP mapping of the vernalization (Vrn1) and frost resistance (Fr1) genes on chromosome 5A of wheat. Theor. Appl. Genet. 90:1174-79
18. Gibson S, Arondel V, Iba K, Somerville C. 1994. Cloning of a temperature-regulated gene encoding a chloroplast omega-3 desaturase from Arabidopsis thaliana. Plant Physiol. 106:1615-21
19. Gilmour SJ, Artus NN, Thomashow MF. 1992. cDNA sequence analysis and expression of two cold-regulated genes of Arabidopsis thaliana. Plant Mol. Biol. 18:13-21
20. Gilmour SJ, Hajela RK, Thomashow MF. 1988. Cold acclimation in Arabidopsis thaliana. Plant Physiol. 87:745-50
21. Gilmour SJ, Thomashow MF. 1991. Cold acclimation and cold-regulated gene expression in ABA mutants of Arabidopsis thaliana. Plant Mol. Biol. 17:1233-40
22. 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
23. Griffith M, Antikainen M, Hon W-C, Pihakaski-Maunsbach K, Yu X-M, et al. 1997. Antifreeze proteins in winter rye. Physiol. Plant. 100:327-32
24. Guiltinan MJ, Marcotte WR Jr, Quatrano RS. 1990. A plant leucine zipper protein that recognizes an abscisic acid response element. Science 250:267-71
25. Guy C, Haskell D, Li QB. 1998. Association of proteins with the stress 70 molecular chaperones at low temperature: evidence for the existence of cold labile proteins in spinach. Cryobiology 36:301-14
26. Guy C, Haskell D, Neven L, Klein P, Smelser C. 1992. Hydration-state-responsive proteins link cold and drought stress in spinach. Planta 188:265-70
27. Guy CL. 1990. Cold acclimation and freezing stress tolerance: role of protein metabolism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41:187-223
28. Guy CL, Haskell D. 1988. Detection of polypeptides associated with the cold acclimation process in spinach. Electrophoresis 9:787-96
29. Guy CL, Haskell D. 1987. Induction of freezing tolerance in spinach is associated with the synthesis of cold acclimation induced proteins. Plant Physiol. 84:872-78
30. Guy CL, Haskell D. 1989. Preliminary characterization of high molecular mass proteins associated with cold acclimation in spinach. Plant Physiol. Biochem. 27:777-84
31. Guy CL, Haskell D, Yelenosky G. 1988. Changes in freezing tolerance and polypeptide content of spinach and citrus at 5°C. Cryobiology 25:264-71
32. Guy CL, Li QB. 1998. The organization and evolution of the spinach stress 70 molecular chaperone gene family. Plant Cell 10:539-56
33. Guy CL, Niemi KJ, Brambl R. 1985. Altered gene expression during cold acclimation of spinach. Proc. Natl. Acad. Sci. USA 82:3673-77
34. Hajela RK, Horvath DP, Gilmour SJ, Thomashow MF. 1990. Molecular cloning and expression of cor (cold-regulated) genes in Arabidopsis thaliana. Plant Physiol. 93:1246-52
35. Hayes PM, Blake T, Chen THH, Tragoonrung S, Chen F, et al. 1993. Quantitative trait loci on barley (Hordeum vulgare L.) chromosome 7 associated with components of winterhardiness. Genome 36:66-71
36. Heino P, Sandman G, Lång V, Nordin K, Palva ET. 1990. Abscisic acid deficiency prevents development of freezing tolerance in Arabidopsis thaliana (L.) Heynh. Theor. Appl. Genet. 79:801-6
37. Hong B, Barg R, Ho T-HD. 1992. Developmental and organ-specific expression of an ABA- and stress-induced protein in barley. Plant Mol. Biol. 18:663-74
38. Hong B, Uknes S, Ho T-HD. 1988. Cloning and characterization of a cDNA encoding a mRNA rapidly induced by ABA in barley aleurone layers. Plant Mol. Biol. 11:495-506
39. 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
40. Horvath DP, McLarney BK, Thomashow MF. 1993. Regulation of Arabidopsis thaliana L. (Heyn) cor78 in response to low temperature. Plant Physiol. 103: 1047-53
41. Houde M, Dhindsa RS, Sarhan F. 1992. A molecular marker to select for freezing tolerance in Gramineae. Mol. Gen. Genet. 234:43-48
42. Hughes MA, Dunn MA. 1996. The molecular biology of plant acclimation to low temperature. J. Exp. Bot. 47:291-305
43. Huner NPA, Oquist G, Sarhan F. 1998. Energy balance and acclimation to light and cold. Trends Plant Sci. 3:224-30
44. Ingram J, Bartels D. 1996. The molecular basis of dehydration tolerance in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:377-403
45. Ishikawa M, Robertson AJ, Gusta LV. 1990. Effect of temperature, light, nutrients and dehardening on abscisic acid-induced cold hardiness in Bromus inermis Leyss suspension cultured cells. Plant Cell Physiol. 31:51-59
46. Ishitani M, Xiong L, Lee H, Stevenson B, Zhu JK. 1998. HOS1, a genetic locus involved in cold-responsive gene expression in Arabidopsis. Plant Cell 10:1151-61
47. Ishitani M, Xiong L, Stevenson B, Zhu JK. 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: 1935-49
48. Islam AKMR, Shepherd KW, Sparrow DHB. 1981. Isolation and characterization of wheat-barley chromosome addition lines. Heredity 46:161-74
49. 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
50. Jarillo JA, Capel J, Leyva A, Martínez-Zapater JM, Saunas J. 1994. Two related low-temperature-inducible genes of Arabidopsis encode proteins showing high homology to 14-3-3 proteins, a family of putative kinase regulators. Plant Mol. Biol. 25:693-704
51. Jiang C, Iu B, Singh J. 1996. Requirement of a CCGAC cis-acting element for cold induction of the BN115 gene from winter Brassica napus. Plant Mol. Biol. 30:679-84
52. Jofuku KD, den Boer BG, Van Montagu M, Okamuro JK. 1994. Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6:1211-25
53. 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
54. Kaye C, Neven L, Hofig A, Li QB, Haskell D, Guy C. 1998. Characterization of a gene for spinach CAP160 and expression of two spinach cold-acclimation proteins in tobacco. Plant Physiol. 116:1367-77
55. Klucher KM, Chow H, Reiser L, Fischer RL. 1996. The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell 8:137-53
56. Knight H, Trewavas AJ, Knight MR. 1996. Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 8:489-503
57. Koornneef M, Leon-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
58. Krishna P, Sacco M, Cherutti JF, Hill S. 1995. Cold-induced accumulation of hsp90 transcripts in Brassica napus. Plant Physiol. 107:915-23
59. Kurkela S, Borg-Franck M. 1992. Structure and expression of kin2, one of two cold- and ABA-induced genes of Arabidopsis thaliana. Plant Mol. Biol. 19: 689-92
60. Kurkela S, Franck M. 1990. Cloning and characterization of a cold- and ABA-inducible Arabidopsis gene. Plant Mol. Biol. 15:137-44
61. Kurkela S, Franck M, Heino P, Lång V, Palva ET. 1988. Cold induced gene expression in Arabidopsis thaliana L. Plant Cell Rep. 7:495-98
62. Lalk I, Dörffling K. 1985. Hardening, abscisic acid, proline, and freezing resistance in two winter wheat varieties. Physiol. Plant. 63:287-92
63. Lång V, Mäntylä 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
64. Lång V, Palva ET. 1992. The expression of a rab-related gene, rab18, is induced by abscisic acid during the cold acclimation process of Arabidopsis thaliana (L.) Heynh. Plant Mol. Biol. 20:951-62
65. Laurie DA, Pratchett N, Bezant J, Snape JW. 1995. RFLP mapping of five major genes and eight quantitative trait loci controlling flowering time in a winter x spring barley (Hordeum vulgare L.) cross. Genome 38:575-85
66. Leung J, Bouvier Durand M, Morris PC, Guerrier D, Chefdor F, Giraudat J. 1994. Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science 264:1448-52
67. Levitt J. 1980. Responses of Plants to Environmental Stresses. New York: Academic. 2nd ed.
68. Li PH, Chen THH. 1997. Plant Cold Hardiness. Molecular Biology, Biochemistry and Physiology. New York: Plenum
69. Limin AE, Danyluk J, Chauvin LP, Fowler DB, Sarhan F. 1997. Chromosome mapping in low-temperature induced Wcs120 family genes and regulation of cold-tolerance expression in wheat. Mol. Gen. Genet. 253:720-27
70. Lin C, Thomashow MF. 1992. DNA sequence analysis of a complementary DNA for cold-regulated Arabidopsis gene cor15 and characterization of the COR15 polypeptide. Plant Physiol. 99:519-25
71. Lisse T, Bartels D, Kalbitzer HR, Jaenicke R. 1996. The recombinant dehydrin-like desiccation stress protein from the resurrection plant Craterostigma plantagineum displays no defined three-dimensional structure in its native state. Biol. Chem. 377:555-61
72. 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
73. Livingston DP III, Henson CA. 1998. Apoplastic sugars, fructans, fructan exohydrolase, and invertase in winter oat: responses to second-phase cold hardening. Plant Physiol. 116:403-8
74. Luo M, Liu J, Mohapatra S, Hill RD, Mohapatra SS. 1992. Characterization of a gene family encoding abscisic acid and environmental stress-inducible proteins of alfalfa. J. Biol. Chem. 267:15367-74
75. Mäntylä E, Lång V, Palva ET. 1995. Role of abscisic acid in drought-induced freezing tolerance, cold acclimation, and accumulation of LTI78 and RAB18 proteins in Arabidopsis thaliana. Plant Physiol. 107:141-48
76. 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
77. McKersie BD, Bowley SR. 1997. Active oxygen and freezing tolerance in transgenic plants. See Ref. 68, pp. 203-14
78. McKown R, Kuroki G, Warren G. 1996. Cold responses of Arabidopsis mutants impaired in freezing tolerance. J. Exp. Bot. 47:1919-25
79. Meyer K, Leube MP, Grill E. 1994. A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science 264:1452-55
80. Mizoguchi T, Hayashida N, Yamaguchi-Shinozaki K, Kamada H, Shinozaki K. 1993. ATMPKs: a gene family of plant MAP kinases in Arabidopsis thaliana. FEBS Lett. 336:440-44
81. Mizoguchi T, Irie K, Hirayama T, Hayashida N, Yamaguchi-Shinozaki K, et al. 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: 765-69
82. Monroy AF, Castonguay Y, Laberge S, Sarhan F, Vezina LP, Dhindsa RS. 1993. A new cold-induced alfalfa gene is associated with enhanced hardening at subzero temperature. Plant Physiol. 102:873-79
83. Monroy AF, Dhindsa RS. 1995. Low-temperature signal transduction: induction of cold acclimation-specific genes of alfalfa by calcium at 25°C. Plant Cell 7: 321-31
84. Monroy AF, Sangwan V, Dhindsa RS. 1998. Low temperature signal transduction during cold acclimation: protein phosphatase 2A as an early target for cold-inactivation. Plant J. 13:653-60
85. Monroy AF, SarhanF, Dhindsa RS. 1993. Cold-induced changes in freezing tolerance, protein phosphorylation, and gene expression. Plant Physiol. 102:1127-35
86. Neven LG, Haskell DW, Hofig A, Li QB, Guy CL. 1993. Characterization of a spinach gene responsive to low temperature and water stress. Plant Mol. Biol. 21:291-305
87. 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 16:1061-71
88. Nordin K, VahalaT, Palva ET. 1993. Differential expression of two related, low-temperature-induced genes in Arabidopsis thaliana (L.) Heynh. Plant Mol. Biol. 21:641-53
89. Ohme-Takagi M, Shinshi H. 1995. Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7:173-82
90. Olien CR, Smith MN. 1977. Ice adhesions in relation to freeze stress. Plant Physiol. 60:499-503
91. Orr W, Keller WA, Singh J. 1986. Induction of freezing tolerance in an embryogenic cell suspension culture of Brassica napus by abscisic acid at room temperature. J. Plant Physiol. 126:23-32
92. Quellet F, Vazquez-Tello A, Sarhan F. 1998. The wheat wcs120 promoter is cold-inducible in both monocotyledonous and dicotyledonous species. FEBS Lett. 423:324-28
93. Pan A, Hayes PM, Chen F, Chen THH, Blake T, et al. 1994. Genetic analysis of the components of winterhardiness in barley (Hordeum vulgare L.). Theor. Appl. Genet. 89:900-10
94. Phillips JR, Dunn MA, Hughes MA. 1997. mRNA stability and localisation of the low-temperature-responsive barley gene family blt14. Plant Mol. Biol. 33: 1013-23
95. Polisensky DH, Braam J. 1996. Cold-shock regulation of the Arabidopsis TCH genes and the effects of modulating intracellular calcium levels. Plant Physiol. 111:1271-79
96. Pugsley AT. 1971. A genetic analysis of the spring-winter habit in wheat. Aust. J. Agric. Res. 22:21-31
97. Riechmann JL, Meyerowitz EM. 1998. The AP2/EREBP family of plant transcription factors. Biol. Chem. 379:633-46
98. Rudolph AS, Crowe JH. 1985. Membrane stabilization during freezing: the role of two natural cryoprotectants, trehalose and proline. Cryobiology 22:367-77
99. Sakai A, Larcher W. 1987. Frost Survival of Plants: Responses and Adaptation to Freezing Stress. Berlin: Springer-Verlag
100. Sarhan F, Danyluk J. 1998. Engineering cold-tolerant crops - throwing the master switch. Trends Plant Sci. 3:289-90
101. Sarhan F, Quellet F, Vazquez-Tello A. 1997. The wheat wcs120 gene family. A useful model to understand the molecular genetics of freezing tolerance in cereals. Physiol. Plant. 101:439-45
102. Shinwari ZK, Nakashima K, Miura S, Kasuga M, Seki M, et al. 1998. An Arabidopsis gene family encoding DRE/CRT binding proteins involved in low-temperature-responsive gene expression. Biochem. Biophys. Res. Commun. 250: 161-70
103. Sieg F, Schroder W, Schmitt JM, Hincha DK. 1996. Purification and characterization of a cryoprotective protein (cryoprotectin) from the leaves of cold-acclimated cabbage. Plant Physiol. 111:215-21
104. Snape JW, Law CN, Worland AJ. 1976. Chromosome variation for loci controlling ear-emergence time on chromosome 5A of wheat. Heredity 37:335-40
105. Steponkus PL. 1984. Role of the plasma membrane in freezing injury and cold acclimation. Annu. Rev. Plant. Physiol. 35: 543-84
106. Steponkus PL, Uemura M, Joseph RA, Gilmour SJ, Thomashow MF. 1998. Mode of action of the COR15a gene on the freezing tolerance of Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 95:14570-75
107. Steponkus PL, Uemura M, Webb MS. 1993. A contrast of the cryostability of the plasma membrane of winter rye and spring oat - two species that widely differ in their freezing tolerance and plasma membrane lipid composition. In Advances in Low-Temperature Biology, ed. PL Steponkus, 2:211-312. London: JAI Press
108. Steponkus PL, Uemura M, Webb MS. 1993. Membrane destabilization during freeze-induced dehydration. Curr. Topics Plant Physiol. 10:37-17
109. 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
110. Storlie EW, Allan RE, Walker-Simmons MK. 1998. Effect of the Vrn1-Fr1 interval on cold hardiness levels in near-isogenic wheat lines. Crop Sci. 38:483-88
111. Strauss G, Hauser H. 1986. Stabilization of lipid bilayer vesicles by sucrose during freezing. Proc. Natl. Acad. Sci. USA 83:2422-26
112. Sukumaran NP, Weiser CJ. 1972. An excised leaflet test for evaluating potato frost tolerance. HortScience 7:467-68
113. Tahtiharju S, Sangwan V, Monroy AF, Dhindsa RS, Borg M. 1997. The induction of kin genes in cold-acclimating Ambidopsis thaliana. Evidence of a role for calcium. Planta 203:442-47
114. Thomashow MF. 1990. Molecular genetics of cold acclimation in higher plants. Adv. Genet. 28:99-131
115. Thomashow MF. 1998. Role of cold-responsive genes in plant freezing tolerance. Plant Physiol. 118:1-7
116. Uemura M, Joseph RA, Steponkus PL. 1995. Cold acclimation of Arabidopsis thaliana. Effect on plasma membrane lipid composition and freeze-induced lesions. Plant Physiol. 109:15-30
117. Uemura M, Steponkus PL. 1997. Effect of cold acclimation on membrane lipid composition and freeze-induced membrane destabilization. See Ref. 68, pp. 171-79
118. Urao T, Yakubov B, Yamaguchi-Shinozaki K, Shinozaki K. 1998. Stress-responsive expression of genes for two-component response regulator-like proteins in Arabidopsis thaliana. FEBS Lett. 427:175-78
119. Van Zee K, Chen FQ, Hayes PM, Close TJ, Chen THH. 1995. Cold-specific induction of a dehydrin gene family member in barley. Plant Physiol. 108:1233-39
120. Vazquez-Tello A, Quellet F, Sarhan F. 1998. Low temperature-stimulated phosphorylation regulates the binding of nuclear factors to the promoter of Wcs120, a cold-specific gene in wheat. Mol. Gen. Genet. 257:157-66
121. Wang H, Datla R, Georges F, Loewen M, Cutler AJ. 1995. Promoters from kin1 and cor6.6, two homologous Arabidopsis thaliana genes: transcriptional regulation and gene expression induced by low temperature, ABA, osmoticum and dehydration. Plant Mol. Biol. 28:605-17
122. Wang H, Georges F, Pelcher LE, Saleem M, Cutler AJ. 1994. A 5.3-kilobase genomic fragment from Arabidopsis thaliana containing kin1 and cor6.6. Plant Physiol. 104:291-92
123. Warren G, McKown R, Marin A, Teutonico R. 1996. Isolation of mutations affecting the development of freezing tolerance in Arabidopsis thaliana (L.) Heynh. Plant Physiol. 111:1011-19
124. Welin BV, Olson A, Nylander M, Palva ET. 1994. Characterization and differential expression of dhn/lea/rab-like genes during cold acclimation and drought stress in Arabidopsis thaliana. Plant Mol. Biol. 26:131-44
125. Welin BV, Olson A, Palva ET. 1995. Structure and organization of two closely related low-temperature-induced dhn/lea/rab-like genes in Arabidopsis thaliana L. Heynh. Plant Mol. Biol. 29: 391-95
126. Wilhelm KS, Thomashow MF. 1993. Arabidopsis thaliana cor15b, an apparent homologue of cor15a, is strongly responsive to cold and ABA, but not drought. Plant Mol. Biol. 23:1073-77
127. Wilson K, Long D, Swinburne J, Coupland G. 1996. A Dissociation insertion causes a semidominant mutation that increases expression of TINY, an Arabidopsis gene related to APETALA2. Plant Cell 8:659-71
128. Worrall D, Elias L, Ashford D, Smallwood MCS, Lillford P, et al. 1998. A carrot leucine-rich-repeat protein that inhibits ice recrystallization. Science 282: 115-17
129. Xin Z, Browse J. 1998. eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant. Proc. Natl. Acad. Sci. USA 95:7799-804
130. 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
131. 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