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Plant Molecular Biology

, Volume 40, Issue 5, pp 815–823 | Cite as

Wound- and systemin-inducible calmodulin gene expression in tomato leaves

  • Daniel R. Bergey
  • Clarence A. Ryan
Article

Abstract

Using a calmodulin (CaM) cDNA as a probe in northern analyses, transgenic tomato plants that overexpress the prosystemin gene were found to express increased levels of CaM mRNA and protein in leaves compared to wild-type plants. These transgenic plants have been reported previously to express several wound-inducible defense-related genes in the absence of wounding. Calmodulin mRNA and protein levels were found to increase in leaves of young wild-type tomato plants after wounding, or treatment with systemin, methyl jasmonate, or linolenic acid. CaM mRNA appeared within 0.5 h after wounding or supplying young tomato plants with systemin, and peaked at 1 h. The timing of CaM gene expression is similar to the expression of the wound- or systemin-induced lipoxygenase and prosystemin genes, signal pathway genes whose expression have been reported to begin at 0.5–1 h after wounding and 1–2 h earlier than the genes coding for defensive proteinase inhibitor genes. The similarities in timing between the synthesis of CaM mRNA and the mRNAs for signal pathway components suggests that CaM gene expression may be associated with the signaling cascade that activates defensive genes in response to wounding.

calmodulin cDNA systemin-induced wound-induced plant defense 

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References

  1. Bergey, D.R., Howe, G.A. and Ryan, C.A. 1996. Polypeptide signaling for plant defensive genes exhibits analogies to defense signaling in animals. Proc. Natl. Acad. Sci. USA 93: 12053-12058.Google Scholar
  2. Bergey, D.R., Orozco-Cardenas, M. and Ryan, C.A. 1999. A wound-and systemin-inducible polygalacturonase in tomato leaves. Proc. Natl. Acad. Sci. USA 96: 1756-1760.Google Scholar
  3. Bogre, 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.Google Scholar
  4. Botella, J.R. and Arteca, R.N. 1994. Differential expression of two calmodulin genes in response to physical and chemical stimuli. Plant Mol. Biol. 24: 757-766.Google Scholar
  5. Braam, J. and Davis, R.W. 1990. Rain-, wind-, and touch-induced expression of calmodulin and calmodulin-related genes in Arabidopsis. Cell 60: 357-364.Google Scholar
  6. Bush, D.S. 1995. Calcium regulation in plant cells and its role in signaling. Annu. Rev. Plant Physiol. PlantMol. Biol. 46: 95-122.Google Scholar
  7. Cheung, W.Y. 1980. Calmodulin plays a pivotal role in cellular regulation. Science 207: 19-27.Google Scholar
  8. Conconi, A., Miguel, M. Browse, J. and Ryan, C.A. 1996. Intracellular levels of free linolenic acid increases in tomato leaves in response to wounding. Plant Physiol. 111: 797-803.Google Scholar
  9. Constabel, C.P., Bergey, D.R. and Ryan, C.A. 1995. Systemin activates the synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway. Proc. Natl. Acad. Sci. USA 92: 407-411.Google Scholar
  10. Crabtree, G.R. and Clipstone, N.A. 1994. Signal transmission between the plasma membrane and nucleus of T lymphocytes. Annu. Rev. Biochem. 63: 1045-1083.Google Scholar
  11. Depege, N., Thonat, C., Coutand, C., Julien, J.-L. and Boyer, N. 1997. Morphological responses and molecular modifications in tomato plants after mechanical stimulation. Plant Cell Physiol. 38: 1127-1134.Google Scholar
  12. Enslen, H., Tokumitsu, H., Stork, P.J.S., Davis, R.J. and Soderling, T.R. 1996. Regulation of mitogen-activated protein kinases by a calcium/calmodulin-dependent proteins kinase cascade. Proc. Natl. Acad. Sci. USA 93: 10803-10808.Google Scholar
  13. Farmer, E.E. and Ryan, C.A. 1990. Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc. Natl. Acad. Sci. USA 87: 7713-7716.Google Scholar
  14. 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.Google Scholar
  15. Gardner, P. 1989. Calcium and T lymphocyte activation. Cell 59: 15-20.Google Scholar
  16. Graham, J.S., Hall, G., Pearce, G. and Ryan, C.A. 1986. Regulation of synthesis of proteinase inhibitors I and II mRNAs in leaves of wounded tomato plants. Planta 169: 399-405.Google Scholar
  17. Green, T.R. and Ryan, C.A. 1972. Wound-induced proteinase inhibitors in plant leaves: a possible defense mechanism against insects. Science 175: 776-777.Google Scholar
  18. Harding, S.A., Oh, S.-H. and Roberts, D.M. 1997. Transgenic tobacco expressing a foreign calmodulin gene shows an enhanced production of active oxygen species. EMBO J. 16: 1137-1144.Google Scholar
  19. Heitz, T., Bergey D.R., Ryan, C.A. 1997. A gene encoding a chloroplast-targeted lipoxygenase in tomato leaves is transiently induced by wounding, systemin, and methyl jasmonate. Plant Physiol. 114: 1085-1093.Google Scholar
  20. Hildmann, T., Ebneth, M., Pena-Cortes, H., Sanchez-Serrano, J.J., Willmitzer, L. and Prat, S. 1992. General roles for abscisic and jasmonic acids in gene activation as a result of mechanical wounding. Plant Cell 4: 1157-1170.Google Scholar
  21. Hirt, H. 1997. Multiple roles of MAP kinases in plant signal transduction. Trends Plant Sci. 2: 11-15.Google Scholar
  22. Jacinto, J., McGurl, B., Franceschi, V., Delano-Freier, J. and Ryan, C.A. 1997. Tomato prosystemin promoter confers wound-inducible, vascular bundle-specific expression of the _-glucuronidase gene in transgenic tomato plants. Planta 203: 406-412.Google Scholar
  23. Lamb, C.J. 1994. Plant defense resistance genes in signal perception and transduction. Cell 76: 419-422.Google Scholar
  24. Lee, S., Suh, S., Kin, S., Crain, R.C., Kwak, J.M., Nam, G.-G. and Lee, Y. 1997. Systemic elevation of phosphatidic and lysophospholipid levels in wounded plants. Plant Cell 12: 547-556.Google Scholar
  25. Leonard, R.T. and Hepler, P.K. 1990. Calcium in Plant Growth and Development. American Society of Plant Physiologist, Rockville, M.D.Google Scholar
  26. Lin, L.-L., Wartman, M., Lin, A., Knopf, J.L., Seth, A. and Davis, R.J. 1994. cPLa2 phosphorylated and activated by MAP kinase. Cell 72: 269-278.Google Scholar
  27. Low, P.S. and Merida, J.R. 1996. The oxidative burst in plant defense: function and signal transduction. Physiol. Plant 96: 533-542.Google Scholar
  28. McGurl, B., Pearce, G., Orozco-Cardenas, M. and Ryan, C.A. 1992. Structure, expression, and antisense inhibition of the systemin precursor gene. Science 225: 1570-1573.Google Scholar
  29. McGurl, B., Orozco-Cardenas, M., Pearce, G. and Ryan, C.A. 1994. Overexpression of a the prosystemin gene in transgenic tomato plants generates a systemic signal that constitutively induces proteinase inhibitor synthesis. Proc. Natl. Acad. Sci. USA 91: 9799-9802.Google Scholar
  30. Mehdy, M.C. 1994. Active oxygen species in plant defense against pathogens. Plant Physiol. 105: 467-472.Google Scholar
  31. Moyen, C., Hammond-Kosack, K.E., Jones, J., Knight, M.R. and Johannes, E. 1998. Systemin triggers an increase of cytoplas823 mic calcium in tomato mesophyllo cells: Ca2C mobilization from intra-and extracellular compartments. Plant Cell Envir. 21: 1101-1111.Google Scholar
  32. Narvaez-Vasquez, J., Pearce, G., Orozco-Cardenas, M.L., Franceschi, V.R. and Ryan, C.A. 1995. Autoradiographic and biochemical evidence for the systemic translocation of systemin in tomato plants. Planta 195: 593-600.Google Scholar
  33. Niki, I., Yokokura, H., Sudo, T., Kato, M. and Hidaka, H. 1996. Ca2C signaling and intracellular Ca2C binding proteins. J. Biochem. 120: 685-698.Google Scholar
  34. Orozco-Cardenas, M. and Ryan, C.A. 1999. Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc. Natl. Acad. Sci. USA 96: 6553-6557.Google Scholar
  35. Orozco-Cardenas, M., McGurl, B. and Ryan, C.A. 1993. Expression of an antisense prosystemin gene in tomato plants reduces resistance toward Manduca Sexta larvae. Proc. Natl. Acad. Sci. USA 90: 8273-8276.Google Scholar
  36. Pautot, V., Holzer, F.M., Reisch, B. and Walling, L.L. 1993. Leucine aminopeptidase: an inducible component of the defense response in Lycopersicon esculentum (tomato). Proc. Natl. Acad. Sci. USA 90: 9906-9910.Google Scholar
  37. Pearce, G., Strydom, D., Johnson, S., Ryan, C.A. 1991. A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253: 895-898.Google Scholar
  38. Poovaiah, B.W. and Reddy, A.S.N. 1987. Calcium messenger system in plants. Crit. Rev. Plant Sci. 6: 47-75.Google Scholar
  39. Poovaiah, B.W. and Reddy, A.S.N. 1993. Calcium and signal transduction in plants. Crit. Rev. Plant Sci. 12: 185-211.Google Scholar
  40. Qui, Z.-H., Gijon, M.A., de Carvalho, M.S., Spencer, D.M. and Leslie, C.C. 1998. The role of calcium and phosphorylation of cytosolic phospholipase A2 in regulating arachidonic acid release in macrophages. J. Biol. Chem. 273: 8203-8211.Google Scholar
  41. Roberts, D.M. and Harmon, A.C. 1992. Calcium-modulated proteins: targets of intracellular calcium signals in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43: 375-415.Google Scholar
  42. Royo, J., Vancanney, G., Perez, A.G., Sanz, C., Stormann, K., Rosahl, S. and Sanchez-Serrano, J.J. 1996. Characterization of three potato lipoxygenases with distinct enzymatic activities and different organ-specific and wound-regulated expression patterns. J. Biol. Chem. 271: 21012-21019.Google Scholar
  43. Ryan, C.A. 1967. Quantitative determination of soluble cellular proteins by radial diffusion in agar gels containing antibodies. Anal. Biochem. 19: 434-440.Google Scholar
  44. Sambrook, J., Fritsch, E.F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.Google Scholar
  45. Schroeder, J.I. and Thuleau, P. 1991. Ca2C channels in higher plants. Plant Cell 3: 555-559.Google Scholar
  46. 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.Google Scholar
  47. Sheen, J. 1996. Ca2C-dependent protein kinases and stress signal transduction in plants. Science 274: 1900-1902.Google Scholar
  48. Shumway, K. and Ryan, C.A. 1976. Evidence for the presence of proteinase inhibitor I in plant cell vacuolar protein bodies. Planta 129: 161-164.Google Scholar
  49. Somssich, I.E. 1997. MAP kinases and plant defense. Trends Sci. 2: 406-408.Google Scholar
  50. Stratmann, J.W. and Ryan, C.A. 1997. 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. USA 94: 11085-11089.Google Scholar
  51. Suzuki, K. and Shinshi, H. 1995. Transient activation and tyrosine phosphorylation of a protein kinase in tobacco cells treated with a fungal elicitor. Plant Cell 7: 639-647.Google Scholar
  52. Takezwa, D., Liu, Z.H., An, G. and Poovaiah, B.W. 1995. Calmodulin gene family in potato: developmental and touch-induced expression of the mRNA encoding a novel isoform. Plant Mol. Biol. 27: 693-703.Google Scholar
  53. Trautman, R., Cowan, K.M. and Wahner, G.G. 1971. Data for processing from radial immunodiffusion. Immunochemistry 8: 901-916.Google Scholar
  54. Usami, C., 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.Google Scholar

Copyright information

© Kluwer Academic Publishers 1999

Authors and Affiliations

  • Daniel R. Bergey
    • 1
  • Clarence A. Ryan
    • 1
  1. 1.Institute of Biological ChemistryWashington State UniversityPullmanUSA

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