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http://dx.doi.org/10.1007/s10059-009-0063-6

Functional Analysis of the Stress-Inducible Soybean Calmodulin Isoform-4 (GmCaM-4) Promoter in Transgenic Tobacco Plants  

Park, Hyeong Cheol (Division of Applied Life Science (Brain Korea 21 program), Plant Molecular Biology and Biotechnology Research Center and Environmental Biotechnology National Core Research Center, Gyeongsang National University)
Kim, Man Lyang (Department of Infection Biology, Biozentrum, University of Basel)
Kang, Yun Hwan (Division of Applied Life Science (Brain Korea 21 program), Plant Molecular Biology and Biotechnology Research Center and Environmental Biotechnology National Core Research Center, Gyeongsang National University)
Jeong, Jae Cheol (Division of Applied Life Science (Brain Korea 21 program), Plant Molecular Biology and Biotechnology Research Center and Environmental Biotechnology National Core Research Center, Gyeongsang National University)
Cheong, Mi Sun (Division of Applied Life Science (Brain Korea 21 program), Plant Molecular Biology and Biotechnology Research Center and Environmental Biotechnology National Core Research Center, Gyeongsang National University)
Choi, Wonkyun (Division of Applied Life Science (Brain Korea 21 program), Plant Molecular Biology and Biotechnology Research Center and Environmental Biotechnology National Core Research Center, Gyeongsang National University)
Lee, Sang Yeol (Division of Applied Life Science (Brain Korea 21 program), Plant Molecular Biology and Biotechnology Research Center and Environmental Biotechnology National Core Research Center, Gyeongsang National University)
Cho, Moo Je (Division of Applied Life Science (Brain Korea 21 program), Plant Molecular Biology and Biotechnology Research Center and Environmental Biotechnology National Core Research Center, Gyeongsang National University)
Kim, Min Chul (Division of Applied Life Science (Brain Korea 21 program), Plant Molecular Biology and Biotechnology Research Center and Environmental Biotechnology National Core Research Center, Gyeongsang National University)
Chung, Woo Sik (Division of Applied Life Science (Brain Korea 21 program), Plant Molecular Biology and Biotechnology Research Center and Environmental Biotechnology National Core Research Center, Gyeongsang National University)
Yun, Dae-Jin (Division of Applied Life Science (Brain Korea 21 program), Plant Molecular Biology and Biotechnology Research Center and Environmental Biotechnology National Core Research Center, Gyeongsang National University)
Publication Information
Molecules and Cells / v.27, no.4, 2009 , pp. 475-480 More about this Journal
Abstract
The transcription of soybean (Glycine max) calmodulin isoform-4 (GmCaM-4) is dramatically induced within 0.5 h of exposure to pathogen or NaCl. Core cis-acting elements that regulate the expression of the GmCaM-4 gene in response to pathogen and salt stress were previously identified, between -1,207 and -1,128 bp, and between -858 and -728 bp, in the GmCaM-4 promoter. Here, we characterized the properties of the DNA-binding complexes that form at the two core cis-acting elements of the GmCaM-4 promoter in pathogen-treated nuclear extracts. We generated GUS reporter constructs harboring various deletions of approximately 1.3-kb GmCaM-4 promoter, and analyzed GUS expression in tobacco plants transformed with these constructs. The GUS expression analysis suggested that the two previously identified core regions are involved in inducing GmCaM-4 expression in the heterologous system. Finally, a transient expression assay of Arabidopsis protoplasts showed that the GmCaM-4 promoter produced greater levels of GUS activity than did the CaMV35S promoter after pathogen or NaCl treatments, suggesting that the GmCaM-4 promoter may be useful in the production of conditional gene expression systems.
Keywords
calmodulin; pathogen; promoter; salt stress; soybean (Glycine max); transcription factor;
Citations & Related Records
Times Cited By KSCI : 2  (Citation Analysis)
Times Cited By Web Of Science : 7  (Related Records In Web of Science)
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1 Aoyama, T., and Chua, N.H. (1997). A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J. 11, 605-612   DOI   ScienceOn
2 Cheung, W.Y. (1980). Calmodulin plays a pivotal role in cellular regulation. Science 207, 19-27   DOI   PUBMED
3 Cho, M.J., Vaghy, P.L., Kondo, R., Lee, S.H., David, J.P., Rehl, R., Heo, W.D., and Johnson, J.D. (1998). Reciprocal regulation of mammalian nitric oxide synthase and calcineurin by plant calmodulin isoforms. Biochemistry 37, 15593-15597   DOI   ScienceOn
4 Kao, Y.L., Deavours, B.E., Phelps, K.K., Walker, R.A., and Reddy, A.S.N. (2000). Bundling of microtubules by motor and tail domains of a kinesin-like calmodulin-binding protein from Arabidopsis: regulation by $Ca^{2+}$/Calmodulin. Biochem. Biophys. Res. Commun. 267, 201-207   DOI   ScienceOn
5 Kozak, M. (1987). An analysis of 5'-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res. 15, 8125-8148   DOI   PUBMED   ScienceOn
6 Lee, S.H., Kim, J.C., Lee, M.S., Heo, W.D., Seo, H.Y., Yoon, H.W., Hong, J.C., Lee, S.Y., Bahk, J.D., Hwang, I., et alK (1995a). Identification of a novel divergent calmodulin isoform from soybean which has differential ability to activate calmodulin-dependent enzymes. J. Biol. Chem. 270, 21806-21812   DOI   ScienceOn
7 Nagao, R.T., Goekjian, V.H., Hong, J.C., and Key, J.L. (1993). Identification of protein-binding DNA sequences in an auxinregulated gene of soybean. Plant Mol. Biol. 21, 1147-1162   DOI   ScienceOn
8 Park, C.Y., Heo, W.D., Yoo, J.H., Lee, J.H., Kim, M.C., Chun, H.J., Moon, B.C., Kim, I.H., Park, H.C., Choi, M.S., et al. (2004a). Pathogenesis-related gene expression by specific calmodulin isoforms is dependent on NIM1, a key regulator of systemic acquired resistance. Mol. Cells 18, 207-213   PUBMED
9 Park, H.C., Kim, M.L., Lee, S.M., Bahk, J.D., Yun, D.-J., Lim, C.O., Hong, J.C., Lee, S.Y., Cho, M.J., and Chung, W.S. (2007). Pathogen-induced binding of the soybean zinc finger homeodomain proteins GmZF-HD1 and GmZF-HD2 to two repeats of ATTA homeodomain binding site in the calmodulin isoform 4 (GmCaM4) promoter. Nucleic Acids Res. 35, 3612-3623   DOI   PUBMED
10 Yang, T., Segal, G., Abbo, S., Feldman, M., and Fromm, H. (1996). Characterization of the calmodulin gene family in wheat: structure, chromosomal location, and evolutionary aspects. Mol. Gen. Genet. 252, 684-694   DOI   ScienceOn
11 Gawienowski, M.C., Szymanski, D., Perera, I.Y. and Zielinski, R.E. (1993) Calmodulin isoforms in Arabidopsis encoded by multiple divergent mRNAs. Plant Mol. Biol. 22, 215-225   DOI   ScienceOn
12 Szymanski, D.B., Liao, B., and Zielinski, R.E. (1996). Calmodulin isoforms differentially enhance the binding of cauliflower nuclear proteins and recombinant TGA3 to a region derived from the Arabidopsis Cam-3 promoter. Plant Cell 8, 1069-1077   DOI   ScienceOn
13 Kozak, M. (1988). Leader length and secondary structure modulate mRNA function under conditions of stress. Mol. Cell. Biol. 8, 2737-2744   DOI   PUBMED
14 Yoo, J.H., Park, C.Y., Kim, J.C., Heo, W.D., Cheong, M.S., Park, H.C., Kim, M.C., Moon, B.C., Choi, M.S., Kang, Y.H., et alK (2005). Direct interaction of a divergent CaM isoform and the transcription factor, MYB2, enhances salt tolerance in Arabidopsis. J. Biol. Chem. 280, 3697-3706   DOI   ScienceOn
15 Harmon, A.C., Gribskov, M., and Harper, J.F. (2000). CDPKs-a kinase for every $Ca^{2+}$ signal? Trends Plant Sci. 5, 154-159   DOI   ScienceOn
16 Snedden, W.A., and Fromm, H. (2001). Calmodulin as a versatile calcium signal transducer in plants. New Phytol. 151, 35-66   DOI   ScienceOn
17 Katagiri, F., Thilmony, R., and He, S.Y. (2002). The Arabidopsis thaliana-Pseudomonas interaction. In the Arabidopsis Book, C.R. Somerville, and E.M. Meyerowitz, eds., (Rockville, USA: American Society of Plant Biologists), doi/10.1199/tab. 0039, http://www.aspb.org/publications/arabidopsis/
18 O'Neil, K.T., and DeGardo, W.F. (1990). How calmodulin binds its targets: sequence independent recognition of amphiphilic $\alpha$- helices. Trends Biochem. Sci. 15, 59-64   DOI   PUBMED   ScienceOn
19 Liao, B., Gawienowski, M.C., and Zielinski, R.E. (1996). Differential stimulation of NAD kinase and binding of peptide substrates by wild-type and mutant plant calmodulin isoform. Arch. Biochem. Biophys. 327, 53-60   DOI   ScienceOn
20 Jeong, J.C., Shin, D., Lee, J., Kang, C.H., Baek, D., Cho, M.J., Kim, M.C., and Yun, D.-J. (2007). Isolation and characterization of a novel calcium/calmodulin-dependent protein kinase, AtCK, from Arabidopsis. Mol. Cells 24, 276-282   PUBMED
21 Lee, S.H., Johnson, J.D., Walsh, M.P., Van Lierop, J.E., Sutherland, C., Xu, A., Snedden, W.A., Kosk-kosicka, D., Fromm, H., Narayanan, N., et alK (2000). Differential regulation of $Ca^{2+}$/calmodulin- dependent enzymes by plant calmodulin isoforms and free $Ca^{2+}$ concentration. Biochem. J. 350, 299-306   DOI   ScienceOn
22 Roberts, D.M., and Harmon, A.C. (1992). Calcium-modulated proteins: Targets of intracellular calcium signals in higher plants. Ann. Rev. Plant Physiol. Plant Mol. Biol. 43, 375-414   DOI   ScienceOn
23 Jefferson, R.A., Kavanagh, T.A., and Bevan, M.W. (1987). GUS fusions: $\beta$-Glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901-3907   PUBMED
24 Ling, V., Perera, I., and Zielinski, R.E. (1991). Primary structures of Arabidopsis calmodulin isoforms deduced from the sequences of cDNA clones. Plant Physiol. 96, 1196-1202   DOI   ScienceOn
25 Bush, D.S. (1995). Calcium regulation in plant cells and its role in signaling. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46, 95-122   DOI   ScienceOn
26 Takezawa, D., Liu, Z.H., An, G., and Poovaiah, B.W. (1995). Calmodulin gene family in potato: developmental and touchinduced expression of the mRNA encoding a novel isoform. Plant Mol. Biol. 27, 693-703   DOI   ScienceOn
27 Kondo, R., Tikunova, S.B., Cho, M.J., and Johnson, J.D. (1999). A point mutation in a plant calmodulin is responsible for its inhibition of nitric-oxide synthase. J. Biol. Chem. 274, 36213-36218   DOI   ScienceOn
28 Lim, E.-K., Roberts, M.R., and Bowles, D.J. (1998). Biochemical characterization of tomato annexin p35. Independence of calcium binding and phosphatase activities. J. Biol. Chem. 273, 34920-34925   DOI   ScienceOn
29 Zielinski, R.E. (2002). Characterization of three new members of the Arabidopsis thaliana calmodulin gene family: conserved and highly diverged members of the gene family functionally complement a yeast calmodulin null. Planta 214, 446-455   DOI   PUBMED   ScienceOn
30 Chin, D., and Means, A.R. (2000). Calmodulin: a prototypical calcium sensor. Trends Cell Biol. 10, 322-328   DOI   ScienceOn
31 Heo, W.D., Lee, S.H., Kim, M.C., Kim, J.C., Chung, W.S., Chun, H.J., Lee, K.J., Park, C.Y., Park, H.C., Choi, J.Y., et al. (1999). Involvement of specific calmodulin isoforms in salicylic acid-independent activation of plant disease resistance responses. Proc. Natl. Acad. Sci. USA 96, 766-771   DOI   ScienceOn
32 Abel, S., and Theologis, A. (1994). Transient transformation of Arabidopsis leaf protoplast: A versatile experimental system to study gene expression. Plant J. 5, 421-427   DOI   ScienceOn
33 Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.D., Smith, J.A., and Struhl, K. (1987). Current protocols in molecular biology, Vol. 2., (New York, USA: John Wiley and Sons)
34 King, E.O., Ward, M.K., and Raney, D.E. (1954). Two simple media for the demonstration of phycocyanin and fluorescin. J. Lab. Clin. Med. 44, 301-307
35 Park, H.C., Kim, M.L., Kang, Y.H., Jeon, J.M., Yoo, J.H., Kim, M.C., Park, C.Y., Jeong, J.C., Moon, B.C., Lee, J.H., et al. (2004b). Pathogen- and NaCl-induced expression of the p`~jJQ promoter is mediated in part by a GT-1 box that interacts with a GT-1-like transcription factor. Plant Physiol. 135, 2150-2161   DOI   ScienceOn
36 Kasuga, M., Liu, Q., Miura, S., Yamaguchi-Shinozaki, K., and Shinozaki, K. (1999). Improving plant drough, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat. Biotechnol. 17, 287-291   DOI   ScienceOn
37 Lee, A., Wong, S.T., Gallagher, D., Li, B., Storm, D.R., Scheuer, T., and Catterall, W.A. (1999). $Ca^{2+}$/calmodulin binds to and modulates P/Q-type calcium channels. Nature 299, 155-158
38 Yamakawa, H., Mitsuhara, I., Ito, N., Seo, S., Kamada, H., and Ohashi, Y. (2001). Transcriptionally and post-transcriptionally regulated response of 13 calmodulin genes to tobacco mosaic virus-induced cell death and wounding in tobacco plant. Eur. J. Biochem. 268, 3916-3929   DOI   ScienceOn
39 Horsch, R.B., Fry, J., Hoffmann, N., Neidermeyer, J., Rogers, S.G., and Fraley, R.T. (1988). Leaf disc transformation. Plant molecular biology manual, S.B. Gelvin, and R.A., Schilperoort, eds. (Dordrecht: Kluwer Academic), A5
40 Lee, S.I., Chun, H.J., Lim, C.O., Bahk, J.D., and Cho, M.J. (1995b). Regeneration of fertile transgenic rice plants from a cultivar, Nakdongbyeo. Korean J. Plant Tissue Culture 22, 175-182
41 Hofmann, A., Proust, J., Dorowski, A., Schantz, R., and Huber, R. (2000). Annexin 24 from capsicum annuum. X-ray structure and biochemical characterization. J. Biol. Chem. 275, 8072-8082   DOI   ScienceOn
42 Potenza, C., Aleman, L., and Sengupta-Gopalan, C. (2004). Targeting transgene expression in research, agricultural, and environmental applications: promoters used in plant transformation. In Vitro Cell. Dev. Biol. Plant 40, 1-22