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. 1999 May;11(5):875–886. doi: 10.1105/tpc.11.5.875

The sfr6 mutation in Arabidopsis suppresses low-temperature induction of genes dependent on the CRT/DRE sequence motif.

H Knight 1, E L Veale 1, G J Warren 1, M R Knight 1
PMCID: PMC144218  PMID: 10330472

Abstract

The sfr mutations, which result in sensitivity to freezing after cold acclimation, define genes that are required for freezing tolerance. We tested plants homozygous for mutations sfr2 to sfr7 for cold-induced gene expression and found that sfr 6 plants were deficient in cold-inducible expression of the genes KIN1, COR15a, and LTI78, which all contain the C repeat/dehydration-responsive element (CRT/DRE) motif in their promoters. Similarly, sfr 6 plants failed to induce KIN1 normally in response to either osmotic stress or the application of abscisic acid. In contrast, cold-inducible expression of genes CBF1, CBF2, CBF3, and ATP5CS1, which lack the CRT/DRE motif, was not affected. The freezing-sensitive phenotype that defines sfr 6 also was found to be tightly linked to the gene expression phenotype. To determine whether the failure of cold induction of CRT/DRE-containing genes in sfr 6 was due to altered low-temperature calcium signaling, cold-induced cytosolic-free calcium ([Ca2+]cyt) elevations were investigated in the sfr 6 mutant, but these were found to be indistinguishable from those of the wild type. We discuss the possibilities that CRT/DRE binding proteins (such as CBF1) require activation to play a role in transcription and that the SFR6 protein is a vital component of their activation.

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Selected References

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  1. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997 Sep 1;25(17):3389–3402. doi: 10.1093/nar/25.17.3389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Artus N. N., Uemura M., Steponkus P. L., Gilmour S. J., Lin C., Thomashow M. F. Constitutive expression of the cold-regulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance. Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13404–13409. doi: 10.1073/pnas.93.23.13404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baker S. S., Wilhelm K. S., Thomashow M. F. The 5'-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol Biol. 1994 Mar;24(5):701–713. doi: 10.1007/BF00029852. [DOI] [PubMed] [Google Scholar]
  4. Bell C. J., Ecker J. R. Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. Genomics. 1994 Jan 1;19(1):137–144. doi: 10.1006/geno.1994.1023. [DOI] [PubMed] [Google Scholar]
  5. Campbell A. K., Trewavas A. J., Knight M. R. Calcium imaging shows differential sensitivity to cooling and communication in luminous transgenic plants. Cell Calcium. 1996 Mar;19(3):211–218. doi: 10.1016/s0143-4160(96)90022-6. [DOI] [PubMed] [Google Scholar]
  6. Cattivelli L., Bartels D. Molecular cloning and characterization of cold-regulated genes in barley. Plant Physiol. 1990 Aug;93(4):1504–1510. doi: 10.1104/pp.93.4.1504. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Edwards K., Johnstone C., Thompson C. A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res. 1991 Mar 25;19(6):1349–1349. doi: 10.1093/nar/19.6.1349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gilmour S. J., Zarka D. G., Stockinger E. J., Salazar M. P., Houghton J. M., Thomashow M. F. Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J. 1998 Nov;16(4):433–442. doi: 10.1046/j.1365-313x.1998.00310.x. [DOI] [PubMed] [Google Scholar]
  9. Hajela R. K., Horvath D. P., Gilmour S. J., Thomashow M. F. Molecular Cloning and Expression of cor (Cold-Regulated) Genes in Arabidopsis thaliana. Plant Physiol. 1990 Jul;93(3):1246–1252. doi: 10.1104/pp.93.3.1246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Horvath D. P., McLarney B. K., Thomashow M. F. Regulation of Arabidopsis thaliana L. (Heyn) cor78 in response to low temperature. Plant Physiol. 1993 Dec;103(4):1047–1053. doi: 10.1104/pp.103.4.1047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ishitani M., Xiong L., Stevenson B., Zhu J. K. 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. 1997 Nov;9(11):1935–1949. doi: 10.1105/tpc.9.11.1935. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jaglo-Ottosen K. R., Gilmour S. J., Zarka D. G., Schabenberger O., Thomashow M. F. Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science. 1998 Apr 3;280(5360):104–106. doi: 10.1126/science.280.5360.104. [DOI] [PubMed] [Google Scholar]
  13. Jiang C., Iu B., Singh J. Requirement of a CCGAC cis-acting element for cold induction of the BN115 gene from winter Brassica napus. Plant Mol Biol. 1996 Feb;30(3):679–684. doi: 10.1007/BF00049344. [DOI] [PubMed] [Google Scholar]
  14. Knight H., Knight M. R. Recombinant aequorin methods for intracellular calcium measurement in plants. Methods Cell Biol. 1995;49:201–216. doi: 10.1016/s0091-679x(08)61455-7. [DOI] [PubMed] [Google Scholar]
  15. Knight H., Trewavas A. J., Knight M. R. Calcium signalling in Arabidopsis thaliana responding to drought and salinity. Plant J. 1997 Nov;12(5):1067–1078. doi: 10.1046/j.1365-313x.1997.12051067.x. [DOI] [PubMed] [Google Scholar]
  16. Knight H., Trewavas A. J., Knight M. R. Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell. 1996 Mar;8(3):489–503. doi: 10.1105/tpc.8.3.489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Knight M. R., Campbell A. K., Smith S. M., Trewavas A. J. Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature. 1991 Aug 8;352(6335):524–526. doi: 10.1038/352524a0. [DOI] [PubMed] [Google Scholar]
  18. Konieczny A., Ausubel F. M. A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J. 1993 Aug;4(2):403–410. doi: 10.1046/j.1365-313x.1993.04020403.x. [DOI] [PubMed] [Google Scholar]
  19. Kurkela S., Franck M. Cloning and characterization of a cold- and ABA-inducible Arabidopsis gene. Plant Mol Biol. 1990 Jul;15(1):137–144. doi: 10.1007/BF00017731. [DOI] [PubMed] [Google Scholar]
  20. Lang V., Mantyla E., Welin B., Sundberg B., Palva E. T. Alterations in Water Status, Endogenous Abscisic Acid Content, and Expression of rab18 Gene during the Development of Freezing Tolerance in Arabidopsis thaliana. Plant Physiol. 1994 Apr;104(4):1341–1349. doi: 10.1104/pp.104.4.1341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Liu Q., Kasuga M., Sakuma Y., Abe H., Miura S., Yamaguchi-Shinozaki K., Shinozaki K. 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. 1998 Aug;10(8):1391–1406. doi: 10.1105/tpc.10.8.1391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mantyla E., Lang V., Palva E. T. Role of Abscisic Acid in Drought-Induced Freezing Tolerance, Cold Acclimation, and Accumulation of LT178 and RAB18 Proteins in Arabidopsis thaliana. Plant Physiol. 1995 Jan;107(1):141–148. doi: 10.1104/pp.107.1.141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Monroy A. F., Dhindsa R. S. Low-temperature signal transduction: induction of cold acclimation-specific genes of alfalfa by calcium at 25 degrees C. Plant Cell. 1995 Mar;7(3):321–331. doi: 10.1105/tpc.7.3.321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Monroy A. F., Sarhan F., Dhindsa R. S. Cold-Induced Changes in Freezing Tolerance, Protein Phosphorylation, and Gene Expression (Evidence for a Role of Calcium). Plant Physiol. 1993 Aug;102(4):1227–1235. doi: 10.1104/pp.102.4.1227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nordin K., Heino P., Palva E. T. Separate signal pathways regulate the expression of a low-temperature-induced gene in Arabidopsis thaliana (L.) Heynh. Plant Mol Biol. 1991 Jun;16(6):1061–1071. doi: 10.1007/BF00016077. [DOI] [PubMed] [Google Scholar]
  26. Polisensky D. H., Braam J. Cold-shock regulation of the Arabidopsis TCH genes and the effects of modulating intracellular calcium levels. Plant Physiol. 1996 Aug;111(4):1271–1279. doi: 10.1104/pp.111.4.1271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Savouré A., Hua X. J., Bertauche N., Van Montagu M., Verbruggen N. Abscisic acid-independent and abscisic acid-dependent regulation of proline biosynthesis following cold and osmotic stresses in Arabidopsis thaliana. Mol Gen Genet. 1997 Mar 18;254(1):104–109. doi: 10.1007/s004380050397. [DOI] [PubMed] [Google Scholar]
  28. Savouré A., Jaoua S., Hua X. J., Ardiles W., Van Montagu M., Verbruggen N. Isolation, characterization, and chromosomal location of a gene encoding the delta 1-pyrroline-5-carboxylate synthetase in Arabidopsis thaliana. FEBS Lett. 1995 Sep 18;372(1):13–19. doi: 10.1016/0014-5793(95)00935-3. [DOI] [PubMed] [Google Scholar]
  29. Stockinger E. J., Gilmour S. J., Thomashow M. F. 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 U S A. 1997 Feb 4;94(3):1035–1040. doi: 10.1073/pnas.94.3.1035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Strizhov N., Abrahám E., Okrész L., Blickling S., Zilberstein A., Schell J., Koncz C., Szabados L. Differential expression of two P5CS genes controlling proline accumulation during salt-stress requires ABA and is regulated by ABA1, ABI1 and AXR2 in Arabidopsis. Plant J. 1997 Sep;12(3):557–569. doi: 10.1046/j.1365-313x.1997.00557.x. [DOI] [PubMed] [Google Scholar]
  31. Thomashow M. F. Role of cold-responsive genes in plant freezing tolerance. Plant Physiol. 1998 Sep;118(1):1–8. doi: 10.1104/pp.118.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Thorlby G., Veale E., Butcher K., Warren G. Map positions of SFR genes in relation to other freezing-related genes of Arabidopsis thaliana. Plant J. 1999 Feb;17(4):445–452. doi: 10.1046/j.1365-313x.1999.00395.x. [DOI] [PubMed] [Google Scholar]
  33. Tähtiharju S., Sangwan V., Monroy A. F., Dhindsa R. S., Borg M. The induction of kin genes in cold-acclimating Arabidopsis thaliana. Evidence of a role for calcium. Planta. 1997 Dec;203(4):442–447. doi: 10.1007/s004250050212. [DOI] [PubMed] [Google Scholar]
  34. Warren G., McKown R., Marin A. L., Teutonico R. Isolation of mutations affecting the development of freezing tolerance in Arabidopsis thaliana (L.) Heynh. Plant Physiol. 1996 Aug;111(4):1011–1019. doi: 10.1104/pp.111.4.1011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Xin Z., Browse J. Eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant. Proc Natl Acad Sci U S A. 1998 Jun 23;95(13):7799–7804. doi: 10.1073/pnas.95.13.7799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Yamaguchi-Shinozaki K., Shinozaki K. A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell. 1994 Feb;6(2):251–264. doi: 10.1105/tpc.6.2.251. [DOI] [PMC free article] [PubMed] [Google Scholar]

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