A novel cold-inducible gene from Arabidopsis, RCI3, encodes a peroxidase that constitutes a component for stress tolerance

Plant Journal

Volumn 32, Issue 1, 2002, Pages 13-24

  Llorente, Francisco ^a   López Cobollo, Rosa María ^a   Catalá, Rafael ^a   Martínez Zapater, José Miguel ^a   Salinas, Julio ^a  

^a INIA   (Spain)

Author keywords

Abiotic stress; Arabidopsis; Dehydration tolerance; Freezing tolerance; Peroxidase; Salt tolerance

Indexed keywords

DEHYDRATION; DNA; ELECTROPHORESIS; ENZYMES; LOW TEMPERATURE EFFECTS; PLANTS (BOTANY); POSITIVE IONS; RNA;

SEEDLINGS;

GENES;

ABSCISIC ACID; ADAPTATION, PHYSIOLOGICAL; AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; COLD; DESICCATION; DNA, COMPLEMENTARY; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; LIGHT; MOLECULAR SEQUENCE DATA; PEROXIDASES; PLANT ROOTS; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; SODIUM CHLORIDE; WATER;

ARABIDOPSIS; EMBRYOPHYTA; EUKARYOTA;

EID: 0036793334     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.2002.01398.x     Document Type: Article

References (58)

1. Abarca, D., Madueño, F., Martinez-Zapater, J.M. and Salinas, J. (1999) Dimerization of Arabidopsis 14-3-3 proteins: structural requirements within the N-terminal domain and effect of calcium. FEBS Lett. 462, 377-382.
2. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generatíon of protein database search programs. Nucl Acids Res. 25, 3389-3402.
3. 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 COR15a gene affects both chloroplast and protoplast freezing tolerance. Proc. Nat. Acad. Sci. USA, 93, 13404-13409.
4. Baker, S.S., Wilhelm, K.S. and Thomashow, M.F. (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, 701-713.
5. Baulcombe, D.C., Saunders, G.R., Bevan, M.W., Mayo, M.A. and Harrison, B.D. (1986) Expression of biologically-active viral satellite RNA from the nuclear genome of transformed plants. Nature, 321, 446-449.
6. Bednarek, S.Y. and Raikhel, N.V. (1992) Intracellular trafficking of secretory proteins. Plant Mol. Biol. 20, 133-150.
7. Botella, M.A., Quesada, M.A., Hasegawa, P.M. and Valpuesta, V. (1993) Nucleotide sequences of two peroxidase genes from tomato (Lycopersicon esculentum). Plant Physiol. 103, 665-666.
8. Botella, M.A., Quesada, M.A., Kononowicz, A.K., Bressan, R.A., Pliego, F., Hasegawa, P.M. and Valpuesta, V. (1994a) Characterization and in situ localization of a salt-induced tomato peroxidase mRNA. Plant Mol. Biol. 25, 105-114.
9. Botella, M.A., Quesada, M.A., Medina, M.I., Pliego, F. and Valpuesta, V. (1994b) Induction of a tomato peroxidase gene in vascular tissue. FEBS Lett. 347, 195-198.
10. Bowles, D.J. (1990) Defense-related proteins in higher plants. Annu, Rev. Biochem. 59, 873-907.
11. Brown, J.W.S. (1996) Arabidopsis intron mutations and pre-mRNA splicing. Plant J. 10, 771-780.
12. Capel, J., Jarillo, J.A., Salinas, J, and Martínez-Zapater, J.M. (1997) Two homologous low-temperature-inducible genes from Arabidopsis encode highly hidrophobic proteins. Plant Physiol. 115, 569-576.
13. Carpin, S., Crèvecoeur, M., Greppin, H. and Penel, C. (1999) Molecular cloning and tissue-specific expression of an anionic peroxidase in zucchini, Plant Physiol. 120, 799-810.
14. Chauvin, L.P., Houde, M. and Sarhan, F. (1993) A leaf-specific gene stimulated by light during wheat acclimation to low temperature. Plant Mol. Biol. 23, 255-265.
15. Chen, T.H.H. and Gusta, L.U. (1983) Abscisic acid induced freezing resistance in cultured plant cells. Plant Physiol. 73, 71-75.
16. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
17. Cloutier, Y. and Siminowitch, D. (1982) Correlation between cold- and drought-induced frost hardiness in winter wheat and rye varieties. Plant Physiol. 69, 256-258.
18. Cruz, R.T., Jordan, W.R. and Drew, M.C. (1992) Structural changes and associated reduction of hydraulic conductance in roots of Sorghum bicolor L. following exposure to water deficit. Plant Physiol. 99, 203-212.
19. Deblaere, R., Bytebier, B., De Greve, H., Deboeck, F., Schell, J., Van Montagu, M. and Leemans, J. (1985) Efficient octopine Ti plasmid-derived vectors for Agrobacterium-mediated gene transfer to plants. Nucl Acids Res. 13, 4777-4788.
20. Dellaporta, S.L., Wood, J. and Hicks, J.B. (1983) A plant DNA minipreparation: version II. Plant Mol. Biol. Report, 1, 19-21.
21. Fujiyama, K., Takemura, H., Shibayama, S., Kobayashi, K., Choi, J.K., Shinmyo, A., Takano, M., Yamada, Y. and Okada, H. (1988) Structure of the horseradish peroxidase isozyme C genes. Eur. J. Biochem. 173, 681-687.
22. Gavel, Y. and von Heijne, G. (1990) Sequence differences between glycosilated and non-glycosilated Asn-X-Thr/Ser acceptor sites: implications for protein engineering. Protein Eng. 3, 433-442.
23. Gilmour, S.J., Zarka, D.G., 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.
24. Hale, M.G. and Orcutt, D.M. (1987) The Physiology of Plants Under Stress. New York, USA: Wiley-Interscience.
25. Haughn, G. and Sommerville, C. (1986) Sulfonylurea-resistant mutants of Arabidopsis thaliana. Mol. General Genet. 204, 430-434.
26. Jaglo-Ottosen, K.R., Gilmour, S.J., Zarka, D.G., Schabenberger, O. and Thomashow, M.F. (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science, 280, 104-106.
27. Jarillo, J.A., Capel, J., Leyva, A., Martínez-Zapater, J.M. and Salinas, 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.
28. Johansson, A., Rassmussen, S.K., Harthill, J.E. and Welinder, K.G. (1992) cDNA, amino acid and carbohydrate sequence of barley seed-specific peroxidase BP1. Plant Mol. Biol. 18, 1151-1161.
29. 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. Nature Biotechn, 17, 287-291.
30. Kiegle, E., Moore, C.A., Haseloff, J., Tester, M.A. and Knight, M.R. (2000) Cell-type-specific calcium responses to drought, salt and cold in the Arabidopsis root. Plant J. 23, 267-278.
31. Kim, J.C., Lee, S.H., Cheong, Y.H., Yoo, C.M., Lee, S.I., Chun, H.J., Yun, D.J., Hong, J.C., Lee, S.Y., Lim, C.O. and Cho, M.J. (2001) A novel cold-inducible zinc finger protein from soybean, SCOF-1, enhances cold tolerance in transgenic plants. Plant J. 25, 247-259.
32. Kjaersgard, I.V., Jespersen, H.M., Rasmussen, S.K. and Welinder, K.G. (1997) Sequence and RT-PCR expression analysis of two peroxidases from Arabidopsis thaliana belonging to a novel evolutionary branch of plant peroxidases. Plant Mol. Biol. 33, 699-708.
33. Levitt, J. (1980) Responses of Plants to Environmental Stresses: Chilling, Freezing and High Temperatures Stresses. New York, USA: Academic Press.
34. Leyva, A., Jarillo, J.A., Salinas, J. and Martínez-Zapater, J.M. (1995) Low temperature induces the accumulation of phenylalanine ammonia-lyase and chalcone synthase mRNAs of Arabidopsis thaliana in a light-dependent manner. Plant Physiol. 108, 39-46.
35. Liu, C.J., Chao, S. and Gale, M.D. (1990) The genetic control of tissue-specific peroxidases, Per-1, Per-2, Per-3, Per-4, and Per-5 in wheat. Theor. Appl. Genet. 79, 305-313.
36. Liu, Q., Kasuga, M., Kasuma, 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.
37. Logeman, J., Schell, J. and Willmitzer, L. (1987) Improved method for the isolation of RNA from plant tissues. Anal. Biochem. 163, 16-20.
38. Mäntylä, E., Lang, V. and Palva, E.T. (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, 141-143.
39. Medina, J., Bargues, M., Terol, J., Pérez-Alonso, M. and Salinas, J. (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, 463-469.
40. Medina, M.I., Botella, M.A., Quesada, M.A. and Valpuesta, V. (1997) Expression of a highly basic peroxidase gene in NaCl-adapted tomato cell suspensions. FEBS Lett. 407, 357-360.
41. 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, 1655-1656.
42. Murashige, Y. and Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Plant Physiol. 15, 473-497.
43. Nordin, K., Vahala, T. and Palva, E.T. (1993) Differential expression of two related, low temperature-induced genes in Arabidopsis thaliana. Plant Mol. Biol. 21, 641-653.
44. O'Shea, E.K., Rutkowski, P.S. and Kim, P.S. (1989) Evidence that the leucine zipper is a co led coil. Science, 243, 538-542.
45. Pearce, R.S., Houlston, C.E., Atherton, K.M., Rixon, J.E., Harrison, P., Hughes, M.A. and Dunn, M.A. (1998) Localization of expression of three cold-induced genes, blt101, blt4.9, and blt14, in different tissues of the crown and developing leaves of cold-acclimated cultivated barley. Plant Physiol. 117, 787-795.
46. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, USA: Cold Spring. Harbor Laboratory Press.
47. Shinozaki, K. and Yamaguchi-Shinozaki, K. (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr. Opin. Plant Biol. 3, 217-223.
48. 2+ binding protein and shows environmentally induced and tissue-specific regulation. Plant Cell, 6, 1553-1565.
49. Steudle, E. and Peterson, C.A. (1998) How does water get through roots?. J. Exp. Bot. 49, 775-788.
50. Stockinger, E.J., Gilmour, S.J. and Thomashow, M.F. (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. Nat. Acad. Sci. USA, 94, 1035-1040.
51. Tähtiharju, S. and Palva. T. (2001) Antisense innibition of protein phosphatase 2C accelerates cold acclimation in Arabidopsis thaliana. Plant J. 26, 461-470.
52. Thomashow, M.F. (1999) Plant cold acclimation: Freezing tolerance genes and regulatory mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 571-599.
53. Tremousaygue, D., Laudie, M., Grellet, F. and Delseny, M. (1992) The Brassica oleracea rDNA spacer revisited. Plant Mol. Biol. 18, 1013-1018.
54. Wang, H. and Cutler, A.J. (1995) Promoters from kin1 and cor6.6, two Arabidopsis thaliana low-temperature- and ABA-inducible genes, direct strong beta-glucuronidase expression in guard cells, pollen and young developing seeds. Plant Mol. Biol. 28, 619-634.
55. Welinder, K.G. (1992) Superfamily of plant, fungal and bacterial peroxidases. Curr. Opin. Struc. Biol. 2, 388-393.
56. Xu, W., Purugganan, M.M., Polisensky, D.H., Antosiewicz, D.M., Fry, S.C. and Braam, J. (1995) Arabidopsis TCH4, regulated by hormones and the environment, encodes a xyloglucan endotransglycosylase. Plant Cell, 7, 1555-1567.
57. Yamaguchi-Shinozaki, K. and Shinozaki, K. (1993) Arabidopsis DNA encoding two desiccation-responsive rd29 genes. Plant Physiol. 101, 1119-1120.
58. 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, 6, 251-264.