The Leaf-Order-Dependent Enhancement of Freezing Tolerance in Cold-Acclimated Arabidopsis Rosettes is not Correlated with the Transcript Levels of the Cold-Inducible Transcription Factors of CBF/DREB1

Plant and Cell Physiology

Volumn 44, Issue 9, 2003, Pages 922-931

  Takagi, Taro ^a,c   Nakamura, Masanobu ^a   Hayashi, Hiroaki ^b   Inatsugi, Rie ^a   Yano, Ryoichi ^a   Nishida, Ikuo ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c Kyowa Seed   (Japan)

Author keywords

Arabidopsis thaliana; Cold acclimation; COR protein; Freezing tolerance; Leaf order

Indexed keywords

ADAPTATION, PHYSIOLOGICAL; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; DNA PRIMERS; FREEZING; OSMOTIC PRESSURE; PLANT LEAVES; RNA, MESSENGER; TRANSCRIPTION FACTORS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EMBRYOPHYTA;

EID: 0141941729     PISSN: 00320781     EISSN: None     Source Type: Journal    
DOI: 10.1093/pcp/pcg117     Document Type: Article

References (51)

1. Artus, N.N., Uemura, M., Steponkus, P.L., Gilmour, S.J., Lin, C. and Thomashow, M.F. (1996) Constitutive expression of the cold-regulated Arabidopsis thaliana CORI5a gene affects both chloroplast and protoplast freezing tolerance. Proc. Natl Acad. Sci. USA 93: 13404-13409.
2. Baker, S.S., Wilhelm, K.S. and Thomashow, M.F. (1994) The 5′-region of Arabidopsis thaliana corI5a has cis-acting elements that confer cold-, drought-, and ABA-regulated gene expression. Plant Mol. Biol. 24: 701-713.
3. Capel, J., Jarillo, J.A., Salinas, J. and Martinez-Zapater, J.M. (1997) Two homologous low-temperature-inducible genes from Arabidopsis encode highly hydrophobic proteins. Plant Physiol. 115: 569-576.
4. Dörffling, K., Abromeit, M., Bradersen, U., Dörffling, H. and Melz, G. (1998) Involvement of abscisic acid and proline in cold acclimation of winter wheat. In Plant Cold Hardiness. Edited by Li, P.H. and Chen, T.H.H. pp. 283-292. Plenum Press, New York.
5. Fowler, S. and Thomashow, M.F. (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.
6. Gilmour, S.J., Hajera, R.K. and Thomashow, M.F. (1988) Cold acclimation of Arabidopsis thaliana. Plant Physiol. 78: 745-750.
7. Gilmour, S.J., Sebolt, A.M., Salazar, M.P., Everard, J.D. and Thomashow, M.F. (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol. 124: 1854-1865.
8. Gilmour, S.J., Zarka, D.O., Stockinger, E.J., Salazar, M.P., Houghton, J.M. and Thomashow, M.F. (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: 433-442.
9. Guy, C.L. (1990) Molecular mechanisms of cold acclimation. In Environmental Injury to Plants. Edited by Katterman, F. pp. 35-61. Academic Press, London.
10. Guy, C.L., Niemi, K.J. and Brambl, R. (1985) Altered gene expression during cold acclimation of spinach (Spinacia oleracea cultivar Bloomsdale). Proc. Natl Acad. Sci. USA 28: 3673-3677.
11. Hajela, R.K., Horvath, D.P., Gilmour, S.J. and Thomashow, M.F. (1991) Molecular cloning and expression of cor (cold-regulated) genes in Arabidopsis thaliana. Plant Physiol. 93: 1246-1252.
12. Hare, P.D. and Cress, W.A. (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul. 21: 79-102.
13. Hare, P.D., Cress, W.A. and van Staden, J. (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ. 21: 535-553.
14. Horvath, D.P., McLarney, B.K. and Thomashow, M.F. (1993) Regulation of Arabidopsis thaliana L. (Heynh) cor78 in response to low temperature. Plant Physiol. 103: 1047-1053.
15. Inatsugi, R., Nakamura, M. and Nishida, I. (2002) Phosphatidylcholine biosynthesis at low temperature: Differential expression of CTP: phosphorylcholine cytidylyltransferase isogenes in Arabidopsis thaliana. Plant Cell Physiol. 43: 1342-1350.
16. Jaglo-Ottosen, K.R., Gilmour, S.J., Zarka, D.O., Schabenberger, O. and Thomashow, M.F. (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280: 104-106.
17. Jaglo, K.R., Kleff, S., Amundsen, K.L., Zhang, X., Haake, V., Zhang, J.Z., Deits, T. and Thomashow, M.F. (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.
18. Kasuga, M., Liu, Q., Miura, S., Yamaguchi-Shinozaki, K. and Shinozaki, K. (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat. Biotechnol. 17: 287-291.
19. Knight, H., Veale, E.L., Warren, G.J. and Knight, M.R. (1999) The sfr6 mutation in Arabidopsis suppresses low-temperature induction of genes dependent on the CRT/DRE sequence motif. Plant Cell 11: 875-886.
20. Lång, V., Mäntylä, E., Welin, B., Sundberg, B. and Palva, E.T. (1994) Alteration in water status, endogenous abscisic acid content, and expression of rabI8 gene during the development of freezing tolerance in Arabidopsis thaliana. Plant Physiol. 104: 1341-1349.
21. Le Saint, A.-M. (1969) Variations comparées des teneurs en proline libre et en glucides solubles, en relation avec l'inégale sensibilité au gel des organes de plants de choux de Milan, cuit. Pontoise. C. R. Acad. Sci. Paris D268: 310-313.
22. Lee, B., Lee, H., Xiong, L. and Zhu, J.-K. (2002) A mitochondrial complex I defect impairs cold-regulated nuclear gene expression. Plant Cell 14: 1235-1251.
23. Levitt, J. (1980) Responses of Plants to Environmental Stresses, Vol. I. Academic Press, Orlando, FL.
24. Liu, Q., Kasuga, Q., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K. and Shinozaki, K. (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.
25. McKown, R., Kuroki, G. and Warren, G. (1996) Cold response of Arabidopsis mutants impaired in freezing tolerance. J. Exp. Bot. 47: 1919-1925.
26. Medina, J., Catalá, R. and Salinas, J. (2001) Developmental and stress regulation of RCI2A and RCI2B, two cold-inducible genes of Arabidopsis encoding highly conserved hydrophobic proteins. Plant Physiol. 125: 1655-1666.
27. Nanjo, T., Kobayashi, M., Yoshiba, Y., Kakubari, Y., Yamaguchi-Shinozaki, K. and Shinozaki, K. (1999) Antisense suppression of proline degradation improves tolerance to freezing and salinity in Arabidopsis tha/iana. FEBS Lett. 461: 205-210.
28. Nordin, K., Vahala, T. and Palva, E.T. (1993) Differential expression of two related, low-temperature-induced genes in Arabidopsis thaliana (L.) Heynh. Plant Mol. Biol. 21: 641-653.
29. Nylander, M., Scensson, J., Palva, E.T. and Welin, E.V. (2001) Stress-induced accumulation and tissue-specific localization of dehydrins in Arabidopsis thaliana. Plant Mol. Biol. 45: 263-279.
30. Palta, J. and Weiss, L.S. (1993) Ice formation and freezing injury: an over view on the survival mechanisms and molecular aspects of injury and cold acclimation in herbaceous plants. In Advances in Plant Cold Hardiness. Edited by Li, P.H. and Christersson, L. pp. 143-176. CRC Press, Boca Raton, FL.
31. Ristic, Z. and Ashworth, E.N. (1993) Changes in leaf ultrastructure and carbohydrates in Arabidopsis thaliana L. (Heynh) cv. Columbia during rapid cold acclimation. Protoplasma 172: 111-123.
32. Rudolph, A.S. and Crowe, J.H. (1985) Membrane stabilization during freezing: The role of two natural cryoprotectants, trehalose and proline. Cryobiology 22: 367-377.
33. Shinwari, Z.K., Nakashima, K., Miura, S., Kasuga, M., Seki, M., Yamaguchi-Shinozaki, K. and Shinozaki, K. (1998) An Arabidopsis gene family encoding DRE/CRT binding proteins involved in low-temperature-responsive gene expression. Biochem. Biophys. Res. Commun. 250: 161-170.
34. Soga, T. and Ross, G.A. (1999) Simultaneous determination of inorganic anions, organic acids, amino acids and carbohydrates by capillary electrophoresis. J. Chromatogr. 837: 231-239.
35. Steponkus, P.L. (1990) Cold acclimation and freezing injury from a perspective of the plasma membrane. In Environmental Injury to Plants. Edited by Katterman, F. pp. 1-16. Academic Press, London.
36. Steponkus, P.L., Uemura, M., Joseph, R.A., Gilmour, S. and Thomashow, M.F. (1998) Mode of action of the CORI5a gene on the freezing tolerance of Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 95: 14570-14575.
37. Stockinger, E.J., Gilmour, S.J. and Thomashow, M.F. (1997) Arabidopsis thaliana CBFI encodes an AP2 domain-containing a 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.
38. Stone, J.M., Palta, J.P., Bamberg, J.B., Weiss, L.S. and Harbage, J.F. (1993) Inheritance of freezing resistance in tuber-bearing Solanum species: Evidence for independent genetic control of nonacclimated freezing tolerance and cold acclimation capacity. Proc. Natl Acad. Sci. USA 90: 7869-7873.
39. Strand, Å., Foyer, C.H., Gustafsson, P., Gardeström, P. and Hurry, V. (2003) Altering flux through the sucrose biosynthesis pathway in transgenic Arabidopsis thaliana modifies photosynthetic acclimation at low temperatures and the development of freezing tolerance. Plant Cell Environ. 26: 523-536.
40. Strand, Å., Hurry, V., Henkes, S., Huner, N., Gustafsson, P., Gardeström, P. and Stitt, M. (1999) Acclimation of Arabidopsis leaves developing at low temperatures. Increasing cytoplasmic volume accompanies increased activities of enzymes in the Calvin cycle and in the sucrose-biosynthesis pathway. Plant Physiol. 119: 1387-1397.
41. Strauss, G. and Hauser, H. (1986) Stabilization of lipid bilayer vesicles by sucrose during freezing. Proc. Natl Acad. Sci. USA 83: 2422-2426.
42. Thomashow, M.F. (1998) Role of cold-responsive genes in plant freezing tolerance. Plant Physiol. 118: 1-7.
43. Thomashow, M.F. (1999) Plant cold acclimation: freezing tolerance gene and regulatory mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 571-599.
44. Uemura, M., Joseph, R. A. and Steponkus, P.L. (1995) Cold acclimation of Arabidopsis thaliana. Effect on plasma membrane lipid composition and freeze-induced lesions. Plant Physiol. 109: 15-30.
45. Uemura, M. and Steponkus, P.L. (1994) A contrast of the plasma membrane lipid composition of oat and rye leaves in relation to freezing tolerance. Plant Physiol. 104: 479-496.
46. Wanner, L.A. and Junttila, O. (1999) Cold-induced freezing tolerance in Arabidopsis. Plant Physiol. 120: 391-399.
47. Warren, G., McKown, R., Marin, A. and Teutonico, R. (1996) Isolation of mutations affecting the development of freezing tolerance in Arabidopsis thaliana (L.) Heynh. Plant Physiol. 111: 1011-1019.
48. Xin, Z. and Browse, J. (1998) eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant. Proc. Natl Acad. Sci. USA 95: 7799-7804.
49. Yamaguchi-Shinozaki, K. and 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: 331-340.
50. Yamaguchi-Shinozaki, K. and 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 104: 251-264.
51. Yoshida, S. (1984) Chemical and biophysical changes in the plasma membrane during cold acclimation of mulberry bark cells (Morus bombycis Koids. cv Goroji). Plant Physiol. 76: 257-265.