Abstract
A gene encoding a tobacco mitogen-activated protein kinase (WIPK) is transcriptionally activated in response to wounding. Transgenic tobacco plants, in which expression of endogenous wipk was suppressed, did not accumulate jasmonic acid or its methyl ester when wounded, suggesting that WIPK is involved in jasmonate-mediated wound signal transduction. Here, we demonstrate that activation of WIPK is required for triggering the jasmonate-mediated signal transduction cascade that occurs when wild-type tobacco plants are wounded. We also show that when plants are wounded, WIPK is rapidly and transiently activated, whereas the quantity of WIPK protein is maintained at a constant level. A transgenic tobacco plant in which the wipk gene was constitutively expressed at a high level showed constitutive enzymatic activation of WIPK and exhibited three- to fourfold higher levels of jasmonate than did its wild-type counterpart. This plant also showed constitutive accumulation of jasmonate-inducible proteinase inhibitor II transcripts. These results show that WIPK is activated in response to wounding, which subsequently causes an increase in jasmonate synthesis.
Full Text
The Full Text of this article is available as a PDF (480.4 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- A simple and general method for transferring genes into plants. Science. 1985 Mar 8;227(4691):1229–1231. doi: 10.1126/science.227.4691.1229. [DOI] [PubMed] [Google Scholar]
- Anderson N. G., Maller J. L., Tonks N. K., Sturgill T. W. Requirement for integration of signals from two distinct phosphorylation pathways for activation of MAP kinase. Nature. 1990 Feb 15;343(6259):651–653. doi: 10.1038/343651a0. [DOI] [PubMed] [Google Scholar]
- Balandin T., Castresana C. Silencing of a beta-1,3-glucanase transgene is overcome during seed formation. Plant Mol Biol. 1997 May;34(1):125–137. doi: 10.1023/a:1005882106266. [DOI] [PubMed] [Google Scholar]
- Balandin T., van der Does C., Albert J. M., Bol J. F., Linthorst H. J. Structure and induction pattern of a novel proteinase inhibitor class II gene of tobacco. Plant Mol Biol. 1995 Mar;27(6):1197–1204. doi: 10.1007/BF00020893. [DOI] [PubMed] [Google Scholar]
- Bergey D. R., Howe G. A., Ryan C. A. Polypeptide signaling for plant defensive genes exhibits analogies to defense signaling in animals. Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12053–12058. doi: 10.1073/pnas.93.22.12053. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Blumer K. J., Johnson G. L. Diversity in function and regulation of MAP kinase pathways. Trends Biochem Sci. 1994 Jun;19(6):236–240. doi: 10.1016/0968-0004(94)90147-3. [DOI] [PubMed] [Google Scholar]
- Bogre L., Ligterink W., Meskiene I., Barker P. J., Heberle-Bors E., Huskisson N. S., Hirt H. Wounding Induces the Rapid and Transient Activation of a Specific MAP Kinase Pathway. Plant Cell. 1997 Jan;9(1):75–83. doi: 10.1105/tpc.9.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cano E., Mahadevan L. C. Parallel signal processing among mammalian MAPKs. Trends Biochem Sci. 1995 Mar;20(3):117–122. doi: 10.1016/s0968-0004(00)88978-1. [DOI] [PubMed] [Google Scholar]
- Creelman R. A., Tierney M. L., Mullet J. E. Jasmonic acid/methyl jasmonate accumulate in wounded soybean hypocotyls and modulate wound gene expression. Proc Natl Acad Sci U S A. 1992 Jun 1;89(11):4938–4941. doi: 10.1073/pnas.89.11.4938. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Davis R. J. MAPKs: new JNK expands the group. Trends Biochem Sci. 1994 Nov;19(11):470–473. doi: 10.1016/0968-0004(94)90132-5. [DOI] [PubMed] [Google Scholar]
- Doi K., Gartner A., Ammerer G., Errede B., Shinkawa H., Sugimoto K., Matsumoto K. MSG5, a novel protein phosphatase promotes adaptation to pheromone response in S. cerevisiae. EMBO J. 1994 Jan 1;13(1):61–70. doi: 10.1002/j.1460-2075.1994.tb06235.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eyal Y., Sagee O., Fluhr R. Dark-induced accumulation of a basic pathogenesis-related (PR-1) transcript and a light requirement for its induction by ethylene. Plant Mol Biol. 1992 Jul;19(4):589–599. doi: 10.1007/BF00026785. [DOI] [PubMed] [Google Scholar]
- Farmer E. E., Johnson R. R., Ryan C. A. Regulation of expression of proteinase inhibitor genes by methyl jasmonate and jasmonic Acid. Plant Physiol. 1992 Mar;98(3):995–1002. doi: 10.1104/pp.98.3.995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Farmer E. E., Ryan C. A. Octadecanoid Precursors of Jasmonic Acid Activate the Synthesis of Wound-Inducible Proteinase Inhibitors. Plant Cell. 1992 Feb;4(2):129–134. doi: 10.1105/tpc.4.2.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gotoh Y., Moriyama K., Matsuda S., Okumura E., Kishimoto T., Kawasaki H., Suzuki K., Yahara I., Sakai H., Nishida E. Xenopus M phase MAP kinase: isolation of its cDNA and activation by MPF. EMBO J. 1991 Sep;10(9):2661–2668. doi: 10.1002/j.1460-2075.1991.tb07809.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Herskowitz I. MAP kinase pathways in yeast: for mating and more. Cell. 1995 Jan 27;80(2):187–197. doi: 10.1016/0092-8674(95)90402-6. [DOI] [PubMed] [Google Scholar]
- Jonak C., Heberle-Bors E., Hirt H. MAP kinases: universal multi-purpose signaling tools. Plant Mol Biol. 1994 Feb;24(3):407–416. doi: 10.1007/BF00024109. [DOI] [PubMed] [Google Scholar]
- Jonak C., Kiegerl S., Ligterink W., Barker P. J., Huskisson N. S., Hirt H. Stress signaling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought. Proc Natl Acad Sci U S A. 1996 Oct 1;93(20):11274–11279. doi: 10.1073/pnas.93.20.11274. [DOI] [PMC free article] [PubMed] [Google Scholar]
- León J., Rojo E., Titarenko E., Sánchez-Serrano J. J. Jasmonic acid-dependent and -independent wound signal transduction pathways are differentially regulated by Ca2+/calmodulin in Arabidopsis thaliana. Mol Gen Genet. 1998 May;258(4):412–419. doi: 10.1007/s004380050749. [DOI] [PubMed] [Google Scholar]
- Meskiene I., Bögre L., Glaser W., Balog J., Brandstötter M., Zwerger K., Ammerer G., Hirt H. 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 U S A. 1998 Feb 17;95(4):1938–1943. doi: 10.1073/pnas.95.4.1938. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mizoguchi T., Ichimura K., Shinozaki K. Environmental stress response in plants: the role of mitogen-activated protein kinases. Trends Biotechnol. 1997 Jan;15(1):15–19. doi: 10.1016/S0167-7799(96)10074-3. [DOI] [PubMed] [Google Scholar]
- Mizoguchi T., Irie K., Hirayama T., Hayashida N., Yamaguchi-Shinozaki K., Matsumoto K., Shinozaki K. A gene encoding a mitogen-activated protein kinase kinase kinase is induced simultaneously with genes for a mitogen-activated protein kinase and an S6 ribosomal protein kinase by touch, cold, and water stress in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1996 Jan 23;93(2):765–769. doi: 10.1073/pnas.93.2.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nielsen B. P., Willumsen H., Rasmussen O. V. Fibrinklaebers sekretionshaemmende effekt i mastektomicikatricer. En prospektiv, randomiseret, klinisk kontrolleret undersøgelse. Ugeskr Laeger. 1985 Jun 17;147(25):1995–1996. [PubMed] [Google Scholar]
- Nishida E., Gotoh Y. The MAP kinase cascade is essential for diverse signal transduction pathways. Trends Biochem Sci. 1993 Apr;18(4):128–131. doi: 10.1016/0968-0004(93)90019-j. [DOI] [PubMed] [Google Scholar]
- Nishihama R., Banno H., Shibata W., Hirano K., Nakashima M., Usami S., Machida Y. Plant homologues of components of MAPK (mitogen-activated protein kinase) signal pathways in yeast and animal cells. Plant Cell Physiol. 1995 Jul;36(5):749–757. doi: 10.1093/oxfordjournals.pcp.a078818. [DOI] [PubMed] [Google Scholar]
- Seo S., Okamoto M., Seto H., Ishizuka K., Sano H., Ohashi Y. Tobacco MAP kinase: a possible mediator in wound signal transduction pathways. Science. 1995 Dec 22;270(5244):1988–1992. doi: 10.1126/science.270.5244.1988. [DOI] [PubMed] [Google Scholar]
- Sessa G., Yang X. Q., Raz V., Eyal Y., Fluhr R. Dark induction and subcellular localization of the pathogenesis-related PRB-1b protein. Plant Mol Biol. 1995 Jun;28(3):537–547. doi: 10.1007/BF00020400. [DOI] [PubMed] [Google Scholar]
- Shen W. J., Forde B. G. Efficient transformation of Agrobacterium spp. by high voltage electroporation. Nucleic Acids Res. 1989 Oct 25;17(20):8385–8385. doi: 10.1093/nar/17.20.8385. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shiozaki K., Russell P. Counteractive roles of protein phosphatase 2C (PP2C) and a MAP kinase kinase homolog in the osmoregulation of fission yeast. EMBO J. 1995 Feb 1;14(3):492–502. doi: 10.1002/j.1460-2075.1995.tb07025.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smith D. B., Johnson K. S. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene. 1988 Jul 15;67(1):31–40. doi: 10.1016/0378-1119(88)90005-4. [DOI] [PubMed] [Google Scholar]
- Stratmann J. W., Ryan C. A. Myelin basic protein kinase activity in tomato leaves is induced systemically by wounding and increases in response to systemin and oligosaccharide elicitors. Proc Natl Acad Sci U S A. 1997 Sep 30;94(20):11085–11089. doi: 10.1073/pnas.94.20.11085. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sun H., Charles C. H., Lau L. F., Tonks N. K. MKP-1 (3CH134), an immediate early gene product, is a dual specificity phosphatase that dephosphorylates MAP kinase in vivo. Cell. 1993 Nov 5;75(3):487–493. doi: 10.1016/0092-8674(93)90383-2. [DOI] [PubMed] [Google Scholar]
- Usami S., Banno H., Ito Y., Nishihama R., Machida Y. Cutting activates a 46-kilodalton protein kinase in plants. Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8660–8664. doi: 10.1073/pnas.92.19.8660. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wilson C., Anglmayer R., Vicente O., Heberle-Bors E. Molecular cloning, functional expression in Escherichia coli, and characterization of multiple mitogen-activated-protein kinases from tobacco. Eur J Biochem. 1995 Oct 1;233(1):249–257. doi: 10.1111/j.1432-1033.1995.249_1.x. [DOI] [PubMed] [Google Scholar]
- Wilson C., Eller N., Gartner A., Vicente O., Heberle-Bors E. Isolation and characterization of a tobacco cDNA clone encoding a putative MAP kinase. Plant Mol Biol. 1993 Nov;23(3):543–551. doi: 10.1007/BF00019302. [DOI] [PubMed] [Google Scholar]
- Wurgler-Murphy S. M., Maeda T., Witten E. A., Saito H. Regulation of the Saccharomyces cerevisiae HOG1 mitogen-activated protein kinase by the PTP2 and PTP3 protein tyrosine phosphatases. Mol Cell Biol. 1997 Mar;17(3):1289–1297. doi: 10.1128/mcb.17.3.1289. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Xu Y., Chang PFL., Liu D., Narasimhan M. L., Raghothama K. G., Hasegawa P. M., Bressan R. A. Plant Defense Genes Are Synergistically Induced by Ethylene and Methyl Jasmonate. Plant Cell. 1994 Aug;6(8):1077–1085. doi: 10.1105/tpc.6.8.1077. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhang S., Du H., Klessig D. F. Activation of the tobacco SIP kinase by both a cell wall-derived carbohydrate elicitor and purified proteinaceous elicitins from Phytophthora spp. Plant Cell. 1998 Mar;10(3):435–450. doi: 10.1105/tpc.10.3.435. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhang S., Klessig D. F. Resistance gene N-mediated de novo synthesis and activation of a tobacco mitogen-activated protein kinase by tobacco mosaic virus infection. Proc Natl Acad Sci U S A. 1998 Jun 23;95(13):7433–7438. doi: 10.1073/pnas.95.13.7433. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhang S., Klessig D. F. Salicylic acid activates a 48-kD MAP kinase in tobacco. Plant Cell. 1997 May;9(5):809–824. doi: 10.1105/tpc.9.5.809. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhang S., Klessig D. F. The tobacco wounding-activated mitogen-activated protein kinase is encoded by SIPK. Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):7225–7230. doi: 10.1073/pnas.95.12.7225. [DOI] [PMC free article] [PubMed] [Google Scholar]
