Regulation of Low Temperature-Induced Genes during Cold Acclimation of Arabidopsis Thaliana

  • E. Tapio Palva
  • Björn Welin
  • Tiina Vahala
  • Åke Olson
  • Kerstin Nordin-Henriksson
  • Einar Mäntylä
  • Viola Lång
Part of the NATO ASI Series book series (volume 86)


Arabidopsis thaliana provides an ideal model system for molecular analysis of plant cold acclimation. This small Cruciferae can readily cold acclimate and the acclimation process is accompanied by expression of a specific set of low temperature-responsive genes. Structural analysis of such Iti (low temperature induced) genes has demonstrated that many of them code for polypeptides related to members of the RAB/LEA/DHN family of water stress responsive proteins. This structural similarity is indicative of common function for these proteins and suggests overlapping responses to freezing and desiccation stress. The other Iti genes characterized seem to code for novel, often very hydrophilic proteins. Enhanced freezing tolerance of A. thaliana can be induced by exposure to low temperature, mild desiccation or exogenous abscisic acid (ABA). Mutant studies have suggested that ABA-controlled processes appear to be required for a normal acclimation response. In accordance with the observed pattern of freezing tolerance induction, expression of the lti genes is responsive to the same three stimuli. However, there are marked differences in the expression patterns of the lti genes during the different modes of induction. Furthermore, the genes seem to fall into three different categories with respect to the signal pathways employed for their expression. Existence of separate response pathways to the different stimuli appears to be the most common mechanism for induction of these genes. Accordingly, stimulus specific DNA elements appear to be present in the lti promoters.


Cold Acclimation Freezing Tolerance Desiccation Stress Acclimation Process Ideal Model System 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Baker J, Steele C, Dure L (1988) Sequence and characterization of 6 Lea proteins and their genes from cotton. Plant Mol Biol 11: 277–291CrossRefGoogle Scholar
  2. Bray E (1988) Drought-and ABA-induced changes in polypeptide and mRNA accumulation i tomato leaves. Plant Physiol 88: 1210–1214PubMedCrossRefGoogle Scholar
  3. Cattivelli L, Bartels D (1990) Molecular cloning and characterization of cold-regulated genes in barley. Plant Physiol 93: 1504–1510PubMedCrossRefGoogle Scholar
  4. Chen HH, Gavinlertvatana P, Li PH (1979) Cold acclimation of stem-cultured plants and leaf callus of solanum species. Bot Gaz 140: 142–147CrossRefGoogle Scholar
  5. Chen HH, Li PH, Brenner ML (1983) Involvement of abscisic acid in potato cold acclimation. Plant Physiol 71: 362–365PubMedCrossRefGoogle Scholar
  6. Chen HH, Gusta LV (1983) Abscisic acid-induced freezing resistance in cultured plant cells. Plant Physiol 73: 71–75PubMedCrossRefGoogle Scholar
  7. Close TJ, Kortt AA, Chandler PM (1989) A cDNA-based comparison of dehydration-induced proteins (dehydrins) in barley and corn. Plant Mol Biol 13: 95–108PubMedCrossRefGoogle Scholar
  8. Cloutier Y, Siminovitch D (1982) Correlation between cold- and drought-induced frost hardiness in winter wheat and rye varieties. Plant Physiol 69: 256–258PubMedCrossRefGoogle Scholar
  9. Cohen A, Bray EA (1990) Characterization of three mRNAs that accumulate in wilted tomato leaves in response to elevated levels of endogenous abscisic acid. Planta 182: 27–33CrossRefGoogle Scholar
  10. Dure IL, Crouch M, Harada J, Ho THD, Mundy J, Quatrano R, Thomas T, Sung ZR (1989) Common amino acid sequence domains among the LEA proteins of higher plants. Plant Mol Biol 12: 475–486CrossRefGoogle Scholar
  11. Dunn MA, Hughes MA, Pearce RS, Jack PL (1990) Molecular characterization of a barley gene induced by cold treatment. J Exp Bot 41: 1405–1413CrossRefGoogle Scholar
  12. Gilmour SJ, Hajela RK, Thomashow MF (1988) Cold acclimation in Arabidopsis thaliana. Plant Physiol 87: 745–750PubMedCrossRefGoogle Scholar
  13. Gilmour SJ, Thomashow MF (1991) Cold acclimation and cold-regulated gene expression in ABA mutants of Arabidopsis thaliana. Plant Mol Biol 17: 1233–1240PubMedCrossRefGoogle Scholar
  14. Gilmour SJ, Artus NN, Thomashow MF (1992) cDNA sequence analysis and expression of two coldregulated genes of Arabidopsis thaliana. Plant Mol Biol 18: 13–21PubMedCrossRefGoogle Scholar
  15. Giraudat J, Hauge BM, Valon C, Smalle J, Parcy F, Goodman H (1992) Isolation of the Arabidopsis abi3 gene by positional cloning. Plant Cell 4: 1251–1261PubMedCrossRefGoogle Scholar
  16. Guiltinan MJ, Marcotte WR Jr, Quatrano RS (1990) A plant leucine zipper protein that recognizes an abscisic acid response element. Science 250: 267–271PubMedCrossRefGoogle Scholar
  17. Guo W, Ward RW, Thomashow MF (1992) Characterization of a cold-regulated wheat gene related to Arabidopsis cor47. Plant Physiol 100: 915–922PubMedCrossRefGoogle Scholar
  18. Guy CL, Niemi KJ. Brambl R (1985) Altered gene expression during cold acclimation of spinach. Proc Nad Acad Sci USA 82: 3673–3677CrossRefGoogle Scholar
  19. Guy C, Haskell D, Neven L, Klein P, Smelser C (1992) Hydration-state-responsive proteins link cold and drought stress in spinach. Planta 188: 265–270CrossRefGoogle Scholar
  20. Hajela RK, Horvath DP, Gilmour SJ, Thomashow MF (1990) Molecular cloning and expression of cor (cold-regulated) genes in Arabidopsis thaliana. Plant Physiol 93: 1246–1252PubMedCrossRefGoogle Scholar
  21. Heino P, Sandman G, Lång V, Nordin K, Palva ET (1990) Abscisid acid deficiency prevents development of freezing tolerance in Arabidopsis thaliana ( L.) Heynh. Theor Appl Genet 79: 801–806CrossRefGoogle Scholar
  22. Houde M, Danyluk J, Laliberfé J, Rassart E, Dhindsa RS, Sarhan F (1992) Cloning, characterization and expression of a cDNA encoding a 50-kilodalton protein specifically induced by cold acclimation in wheat. Plant Physiol 99: 1381–1387PubMedCrossRefGoogle Scholar
  23. Koornneef M, Hanhart CJ, Hilhorst HWM, Karssen CM (1989) In vivo inhibition of seed development and reserve protein accumulation in recombinants of abscisic acid biosynthesis and responsiveness mutants in Arabidopsis thaliana. Plant Physiol 90: 463–469PubMedCrossRefGoogle Scholar
  24. Koornneef M, Jorna ML, Brinkhorst-van der Swan DLC, Karssen CM (1982) The isolation of abscisic acid (ABA) deficient mutants by selection of induced revertants in non-germinating gibberellin sensitive lines of Arabidopsis thaliana ( L.) Heynh. Theor Appl Genet 61: 385–393Google Scholar
  25. Koornneef M, Reuling G, Karssen CM (1984) The isolation and characterization of abscisic acidinsensitive mutants of Arabidopsis thaliana. Physiol Plan/ 61: 377–383CrossRefGoogle Scholar
  26. Kurkela S, Franck M, Heino P, Lamp;ng V, Palva ET (1988) Cold induced gene expression in Arabidopsis thaliana L. Plant Cell Reports 7: 495 - 498Google Scholar
  27. Kurkela S, Franck M (1990) Cloning and characterization of a cold- and ABA-inducible Arabidopsis gene. Plant Mol Biol 15: 137–144PubMedCrossRefGoogle Scholar
  28. Kurkela S (1991) Structure and expression analysis of an Arabidopsis thaliana gene family of two cold induced genes. PhD Thesis, University of Helsinki, Helsinki, FinlandGoogle Scholar
  29. 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: 689–692PubMedCrossRefGoogle Scholar
  30. Levitt J (1980) Responses of plants to environmental stresses: Vol 1. Chilling, freezing and high temperature stresses. Academic Press, New YorkGoogle Scholar
  31. Lin C, Guo WW, Everson E, Thomashow MF (1990) Cold acclimation in Arabidopsis and wheat: a response associated with expression of related genes encoding ‘boiling-stable’ polypeptides. Plant Physiol 94: 1078–1083PubMedCrossRefGoogle Scholar
  32. Lin C, Thomashow MF (1992a) A cold-regulated Arabidopsis gene encodes a polypeptide having potent cryoprotective activity. Biochem Biophys Res Commun 183: 1103–1108PubMedCrossRefGoogle Scholar
  33. Lin C, Thomashow MF (1992b) DNA sequence analysis of a complementary DNA for cold-regulated Arabidopsis gene corl5 and characterization of the COR 15 polypeptide. Plant Physiol 99: 519–525PubMedCrossRefGoogle Scholar
  34. Ling V, Heino P, Palva ET (1989) Low temperature acclimation and treatment with exogenous abscisic acid induce common polypeptides in Arabidopsis thaliana ( L.) Heynh. Theor Appl Genet 77: 729–734Google Scholar
  35. Ling V, Palva ET (1992) The expression of a rab-related gene, rabl8, is induced by abscisid acid during the cold acclimation process of Arabidopsis thaliana ( L.) Heynh. Plant Mol Biol 20: 951–962CrossRefGoogle Scholar
  36. Meyerowitz EM (1989) Arabidopsis, a useful weed. Cell 56: 263–269Google Scholar
  37. Mohapatra SS, Poole RJ, Dhindsa RS (1987) Changes in protein patterns and translatable mRNA populations during cold acclimation of alfalfa. Plant Physiol 84: 1172–1176PubMedCrossRefGoogle Scholar
  38. Mohapatra SS, Wolfraim L, Poole RJ, Dhindsa RS (1989) Molecular cloning and relationship to freezing tolerance of cold-acclimation-specific genes in alfalfa. Plant Physiol 89: 375–380PubMedCrossRefGoogle Scholar
  39. Mundy J, Chua N-H (1988) Abscisic acid and water-stress induce the expression of a novel rice gene. EMBO J 7: 2279–2286PubMedGoogle Scholar
  40. Mundy J, Yamaguchi-Shinozaki K, Chua N-H (1990) Nuclear proteins bind conserved elements in the abscisic acid-responsive promoter of a rice rab gene. Proc Natl Acad Sci USA 87: 1406–1410PubMedCrossRefGoogle Scholar
  41. Neven LG, Haskell DW, Hofig A, Li Q-B, Guy CL (1993) Characterization of a spinach gene responsive to low temperature and water stress. Plant Mol Biol 21: 291–305PubMedCrossRefGoogle Scholar
  42. Nordin K, Heino P, Palva ET (1991) Separate signal pathways regulate the expression of a lowtemperature-induced gene in Arabidopsis thaliana ( L.) Heynh. Plant Mol Biol 16: 1061–1071PubMedCrossRefGoogle Scholar
  43. Nordin K, Lang V, Mantyla E, Heino P, Welin B, Baudo M, Holmstrom K-O, Palva ET (1993a) Role of ABA in regulation of low temperature-induced genes in Arabidopsis thaliana. In Advances in Plant Cold Hardiness, edited by P.H. Li and L. Christersson, pp. 45–56. CRC Press, Boca Raton, FloridaGoogle Scholar
  44. Nordin K, Vahala T, Palva ET (1993b) Differential expression of two related, low-temperature-induced genes in Arabidopsis thaliana ( L.) Heynh. Plant Mol Biol 21: 641–653Google Scholar
  45. 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: 23–32Google Scholar
  46. Orr W, Iu B, White TC, Robert LS, Singh J (1992) Complementary DNA sequence of a low temperature-induced Brassica napus gene with homology to the Arabidopsis thaliana kinl gene. Plant Physiol 98: 1532–1534PubMedCrossRefGoogle Scholar
  47. Picket M, Scott G, Davies P, Wang N, Joshi S, Few C (1984) Sequence of antifreeze protein precursor. Eur J Biochem 143: 35–38CrossRefGoogle Scholar
  48. Rouse D, Gehring CA, Parish RW (1992) Structure and sequence of a dehydrin-Iike gene in Arabidopsis thaliana. Plant Mol Biol 19: 531–532PubMedCrossRefGoogle Scholar
  49. Sakai A, Larcher W (1987) Frost survival of plants. Responses and adaptations to freezing stress. Springer-Verlag, BerlinGoogle Scholar
  50. Skriver K, Mundy J (1990) Gene expression in response to abscisic acid in osmotic stress. Plant Cell 2: 503–512PubMedCrossRefGoogle Scholar
  51. Stebbins GL (1972) Flowering plants: Evolution above the species level. Belknap, Harvard BostonGoogle Scholar
  52. Weiser CJ (1970) Cold resistance and injury in wooded plants. Science 169, 1269–1278PubMedCrossRefGoogle Scholar
  53. Weretilnyk E, Orr W, White TC, Iu B, Singh J (1993) Characterization of three related lowtemperature-regulated cDNAs from winter Brassica napus. Plant Physiol 101: 171–177PubMedCrossRefGoogle Scholar
  54. Wolfram LA, Langis R, Tyson H, Dhindsa RS (1993) cDNA sequence, expression and transcript stability of a cold acclimation-specific gene, cas18, of alfalfa (Medicago falcata). Plant Physiol 101:1275–1282CrossRefGoogle Scholar
  55. Yamaguchi-Shinozaki K, Shinozaki K (1993) Characterization of the expression of a desiccationresponsive rd29 gene of Arabidopsis thaliana and analysis of its promoter in transgenic plants. Mol Gen Genet 236: 331–340PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1994

Authors and Affiliations

  • E. Tapio Palva
    • 1
  • Björn Welin
    • 1
  • Tiina Vahala
    • 1
  • Åke Olson
    • 1
  • Kerstin Nordin-Henriksson
    • 1
  • Einar Mäntylä
    • 1
  • Viola Lång
    • 1
  1. 1.Department of Molecular Genetics, Uppsala Genetic CenterSwedish University of Agricultural SciencesUppsalaSweden

Personalised recommendations