Abstract
We have previously demonstrated that cutting induces the rapid response of genes for ethylene-responsive transcription factors (ERFs) in leaf strips of tobacco, and that the induction was not interfered but enhanced in the presence of the protein synthesis inhibitor cycloheximide (CHX). In this study, we analyzed the expression of genes for ERFs in tobacco plants by injuring leaf tissues with a hemostat. The results verified that mechanical damage is a trigger for rapid and concurrent induction of both the local and the systemic expression of genes for ERFs in tobacco plants. Further studies on systemic response of ERF genes in response to different severity and position of the wound on a leaf suggested that a threshold value might exist for the magnitude of wound signal to induce systemic activation of these genes. Then, we examined expression of genes for ERFs by analysis in transgenic tobacco plants that harbored reporter genes in which the promoter of the gene for NsERF2, NsERF3 or NsERF4 was fused to a gene for β-glucuronidase. The results suggested that the local and systemic accumulation of ERF mRNAs after wounding was primarily mediated by the rapid activation of transcription of the respective genes. In addition, we found that cycloheximide triggered rapid activation of genes for ERFs which might be mediated via activation of transcription of the genes for ERFs.
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References
Abel, S. and Theologis, A. 1996. Early genes and auxin action. Plant Physiol. 111: 9–17.
Boari, F. and Malone, M. 1993. Wound-induced hydraulic signals: survey of occurrence in a range of species. J. Exp. Bot. 44: 741–746.
Bögre, L., Ligterink, W., Meskiene, I., Barker, P.J., Heberle-Bors, E., Huskisson, N.S. and Hirt, H. 1997. Wounding induces the rapid and transient activation of a specific MAP kinase pathway. Plant Cell 9: 75–83.
Bowles, D.J. 1990. Defense-related proteins in higher plants. Annu. Rev. Biochem. 59: 873–907.
Bowles, D.J. 1993. Local and systemic signals in the wound response. Semin. Cell Biol. 4: 103–111.
Chen, H.-C., Klein, A., Xiang, M., Backhaus, R.A. and Kuntz, M. 1998. Drought-and wound-induced expression in leaves of a gene encoding a chroloplast carotenoid-associated protein. Plant J. 14: 317–326.
Devoto, A., Leckie, F., Lupotto, E., Cervone, F. and De Lorenzo, G. 1998. The promoter of a gene encoding a polygalacturonase-inhibiting protein of Phaseolus vulgaris L. is activated by wounding but not by elicitors or pathogen infection. Planta 205: 65–174.
Durrant, W.E., Rowland, O., Piedras, P., Hammond-Kosack, K.E. and Jones, J.D. 2000. cDNA-AFLP reveals a striking overlap in race-specific resistance and wound response gene expression profiles. Plant Cell 12: 963–977.
Elliott, K.A. and Shirsat, A.H. 1998. Promoter regions of the extA extensin gene from Brassica napus control activation in response to wounding and tensile stress. Plant Mol. Biol. 37: 675–687.
Farmer, E.E. and Ryan, C.A. 1992. Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell 4: 129–134.
Farmer, E.E., Weber, H. and Vollenweider, S. 1998. Fatty acid signaling in Arabidopsis. Planta 206: 167–174.
Hara, K., Yagi, M., Kusano, T. and Sano, H. 2000. Rapid systemic accumulation of transcripts encoding a tobacco WRKY transcription factor upon wounding. Mol. Gen. Genet. 263: 30–37.
Herde, O., Peña-Cortés, H., Wasternack, C., Willmitzer, L. and Fisahn, J. 1999. Electric signaling and pin2 gene expression on different abiotic stimuli depend on a distinct threshold level of endogenous abscisic acid in several abscisic acid-deficient tomato mutants. Plant Physiol. 119: 213–218.
Herschman, H.R. 1991. Primary response genes induced by growth factors and tumor promoters. Annu. Rev. Biochem. 60: 281–319.
Horvath, D.M. and Chua, N.H. 1996. Identification of an immediate-early salicylic acid-inducible tobacco gene and characterization of induction by other compounds. Plant Mol. Biol. 31: 1061–1072.
Horvath, D.M., Huang, D.J. and Chua, N.H. 1998. Four classes of salicylate-induced tobacco genes. Mol. Plant-Microbe Interact. 11: 895–905.
Jacinto, T., McGurl, B. and Ryan, A. 1999. Wound-regulation and tissue specificity of the tomato prosystemin promoter in transgenic tobacco plants. Plant Sci. 140: 155–159.
Jacinto, T., McGurl, B. and Ryan, A. 1997. Tomato prosystemin promoter confers wound-inducible, vascular bundle-specific expression of the β-glucuronidase gene in transgenic tomato plants. Planta 203: 406–412.
Jonak, C., Ligterink, W. and Hirt, H. 1999. MAP kinases in plant signal transduction. Cell Mol. Life Sci. 55: 204–213.
Kawaoka, A., Kawamoto, T., Sekine, M., Yoshida, K., Takano, M. and Shinmyo, A. 1994. A cis-acting element and a trans-acting factor involved in the wound-induced expression of a horseradish peroxidase gene. Plant J. 6: 87–97.
Kitajima, S., Koyama, T., Ohme-Takagi, M., Shinshi, H. and Sato, F. 2000. Characterization of gene expression of NsERFs, transcription factors of basic PR genes from Nicotiana sylvestris. Plant Cell Physiol. 41: 817–824.
Koshiba, T., Ballas, N., Wong, L.M. and Theologis, A. 1995. Transcriptional regulation of PS-IAA4/5 and PS-IAA6 early gene expression by indoleacetic acid and protein synthesis inhibitors in pea (Pisum sativum). J. Mol. Biol. 253: 396–413.
Kudla, J., Xu, Q., Harter, K., Gruissem, W. and Luan, S. 1999. Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals. Proc. Natl. Acad. Sci. USA 96: 4718–4723.
León, J., Rojo, E. and Sánchez-Serrano, J.J. 2001.Wound signalling in plants. J. Exp. Bot. 52: 1–9.
Malone, M. and Alarcon, J.J. 1995. Only xylem-borne factors can account for systemic wound signalling in the tomato plants. Planta 196: 740–746.
Malone, M., Alarcon, J.J. and Palumbo, L. 1994. A hydraulic interpretation of rapid, long-distance wound signaling in tomato. Planta 193: 181–185.
Meskiene, I., Bögre, L., Glaser, W., Balog, J., Brandstotter, M., Zwerger, K., Ammerer, G. and Hirt, H. 1998. MP2C, a plant protein phosphatase 2C, functions as a negative regulator of mitogen-activated protein kinase pathways in yeast and plants. Proc. Natl. Acad. Sci. USA 95: 1938–1943.
Nishiuchi, T., Hamada, T., Kodama, H. and Iba, K. 1997. Wounding changes the spatial expression pattern of the Arabidopsis plastid ω-3 fatty acid desaturase gene (FAD7) through different signal transduction pathways. Plant Cell 9: 1701–1712.
Nishiuchi, T., Kodama, H., Yanagisawa, S. and Iba, K. 1999. Wound-induced expression of the FAD7 gene is mediated by different regulatory domains of its promoter in leaves/stems and roots. Plant Physiol. 121: 1239–1246.
O'Donnell, P.J., Truesdale, M.R., Calvert, C.M., Dorans, A., Roberts, M.R. and Bowles, D.J. 1998. A novel tomato gene that rapidly responds to wound-and pathogen-related signals. Plant J. 14: 137–142.
Ohme-Takagi, M. and Shinshi, H. 1995. Ethylene-inducible DNA-binding proteins that interact with an ethylene-responsive element. Plant Cell 7: 173–82.
Ohme-Takagi, M., Suzuki, K. and Shinshi, H. 2000. Regulation of ethylene-induced transcription of defense genes. Plant Cell Physiol. 41: 1187–1192.
Ohta, M., Ohme-Takagi, M. and Shinshi, H. 2000. Three ethylene-responsive transcription factors in tobacco with distinct transactivation functions. Plant J. 22: 29–38.
Pastuglia, M., Roby, D., Dumas, C. and Cock, J.M. 1997. Rapid induction by wounding and bacterial infection of an S gene family receptor-like kinase gene in Brassica oleracea. Plant Cell 9: 49–60.
Ryan, C.A. and Pearce, G. 1998. Systemin: a polypeptide signal for plant defensive genes. Annu. Rev. Cell Dev. Biol. 14: 1–17.
Salvador, M.L., Klein, U. and Bogorad, L. 1993. 5′ Sequences are important positive and negative determinants of the longevity of Chlamydomonas chloroplast gene transcripts. Proc. Natl. Acad. Sci. USA 90: 1556–1560.
Seo, S., Okamoto, M., Seto, H., Ishizuka, K., Sano, H. and Ohashi, Y. 1995. Tobacco MAP kinase: a possible mediator in wound signal transduction pathways. Science 270: 1988–1992.
Seo, S., Sano, H. and Ohashi, Y. 1999. Jasmonate-based wound signal transduction requires activation of WIPK, a tobacco mitogen-activated protein kinase. Plant Cell 11: 289–298.
Shinshi, H., Usami, S. and Ohme-Takagi, M. 1995. Identification of an ethylene-responsive region in the promoter of a tobacco class I chitinase gene. Plant Mol. Biol. 27: 923–932.
Stanford, A.C., Northcote, D.H. and Bevan, M.W. 1990. Spatial and temporal patterns of transcription of a wound-induced gene in potato. EMBO J. 9: 593–603.
Stankovic, B. and Davies, E. 1996. Both action potentials and variation potentials induce proteinase inhibitor gene expression in tomato. FEBS Lett. 390: 275–279.
Stankovic, B. and Davies, E. 1997. Intracellular communication in plants: electrical stimulation of proteinase inhibitor gene expression in tomato. Planta 202: 402–406.
Stankovic, B. and Vian, A., Henry-Vian, C., and Davis, E. 2000. Molecular cloning and characterization of a tomato cDNA encoding a systemically wound-inducible bZIP DNA-binding protein. Planta 212: 60–66.
Suzuki, K., Fukuda, Y. and Shinshi, H. 1995. Studies on elicitorsignal transduction leading to differential expression of defense genes in cultured tobacco cells. Plant Cell. Physiol. 36: 281–289.
Suzuki, K., Suzuki, N., Ohme-Takagi, M. and Shinshi, H. 1998. Immediate early induction of mRNAs for ethylene-responsive transcriptional factors in tobacco leaf strips after cutting. Plant J. 15: 657–665.
Theologis, A., Huynh, T.V. and Davis, R.W. 1985. Rapid induction of specific mRNAs by auxin in pea epicotyl tissue. J. Mol. Biol. 183: 53–68.
Usami, S., Banno, H., Ito, Y., Nishihama, R. and Machida, Y. 1995. Cutting activates a 46–kilodalton protein kinase in plants. Proc. Natl. Acad. Sci. USA 92: 8660–8664.
Warner, S.A.J., Scott, R. and Draper, J. 1993. Isolation of an asparagus intracellular PR gene (AoPR1) wound-responsive promoter by the inverse polymerase chain reaction and its characterization in transgenic tobacco. Plant J. 3: 191–201.
Wildon, D.C., Thain, J.F., Minchin, P.E.H., Gubb, I.R., Reilly, A.J., Skipper, Y.D., Doherty, H.M., O'Donnell, P.J. and Bowles, D.J. 1992. Electrical signaling and systemic proteinase inhibitor induction in the wounded plant. Nature 360: 62–65.
Yamamoto, S., Suzuki, K. and Shinshi, H. 1999. Elicitor-responsive, ethylene-independent activation of GCC box-mediated transcription that is regulated by both protein phosphorylation and dephosphorylation in cultured tobacco cells. Plant J. 20: 571–580.
Zhang, S. and Klessig, D.F. 1998. The tobacco wounding-activated mitogen-activated protein kinase is encoded by SIPK. Proc. Natl. Acad. Sci. USA 95: 7225–7230.
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Nishiuchi, T., Suzuki, K., Kitajima, S. et al. Wounding activates immediate early transcription of genes for ERFs in tobacco plants. Plant Mol Biol 49, 473–482 (2002). https://doi.org/10.1023/A:1015553232309
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DOI: https://doi.org/10.1023/A:1015553232309