The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
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Theobroxide Treatment Inhibits Wild Fire Disease Occurrence in Nicotiana benthamiana by the Overexpression of Defense-related Genes

  • Received : 2012.08.26
  • Accepted : 2012.11.08
  • Published : 2013.03.01
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Abstract

Theobroxide, a novel compound isolated from a fungus Lasiodiplodia theobromae, stimulates potato tuber formation and induces flowering of morning glory by initiating the jasmonic acid synthesis pathway. To elucidate the effect of theobroxide on pathogen resistance in plants, Nicotiana benthamiana plants treated with theobroxide were immediately infiltrated with Pseudomonas syringae pv. tabaci. Exogenous application of theobroxide inhibited development of lesion symptoms, and growth of the bacterial cells was significantly retarded. Semiquantitative RT-PCRs using the primers of 18 defense-related genes were performed to investigate the molecular mechanisms of resistance. Among the genes, the theobroxide treatment increased the expression of patho-genesis-related protein 1a (PR1a), pathogenesis-related protein 1b (PR1b), glutathione S-transferase (GST), allen oxide cyclase (AOC), and lipoxyganase (LOX). All these data strongly indicate that theobroxide treatment inhibits disease development by faster induction of defense responses, which can be possible by the induction of defense-related genes including PR1a, PR1b, and GST triggered by the elevated jasmonic acid.

Keywords

References

  1. Cornelissen, B. J. C., Horowittz, J., Van Kan, J. A. L., Goldberg, R. B. and Bol, J. F. 1987. Structure of tobacco genes encoding pathogenesis-related proteins from the PR-1 group. Nucleic Acids Res. 15:6799−6811.
  2. Epple, P., Apel, K. and Bohlmann H. 1995. An Arabidopsis thaliana thionin gene is inducible via a signal transduction pathway different from that for pathogenesis-related proteins. Plant Physiol. 109:813−820.
  3. Gao, X., Wang, F., Yang, Q. Matsuura, H. and Yoshihara, T. 2005. Theobroxide triggers jasmonic acid production to induce potato tuberization in vitro. Plant Growth Regul. 47:39−45.
  4. Gao, X., Yang, Q., Minami, C., Matsuura, H., Kimura, A. and Yoshihara, T. 2003. Inhibitory effect of salicylhydroxamic acid on theobroxide-induced potato tuber formation. Plant Sci. 165:993−999.
  5. Hammerschmidt, R. 2009. Systemic acquired resistance. Adv. Bot. Res. 51:173−222.
  6. Hammond-Kosack, K. E., Silverman, P., Raskin, I. and Jones, J. D. G. 1996. Race-specific elicitors of Cladosporium fulvum induce changes in cell morphology and the synthesis of ethylene and salicylic acid in tomato plants carrying the corresponding Cf disease resistance gene. Plant Physiol. 110:1381− 1394.
  7. Kim, Y. J. and Hwang, B. K. 2000. Pepper gene encoding a basic pathogenesis-related 1 protein is pathogen and ethylene inducible. Physiol. Plant Pathol. 108:51−60.
  8. Kong, F., Gao, X., Nam, K. H., Takahashi, K., Matsuura, H. and Yoshihara, T. 2005. Theobroxide inhibits stem elongation in Pharbitis nil by regulating jasmonic acid and gibberellin biosynthesis. Plant Sci. 169:721−725.
  9. Kong, F., Li, Y., Abe, J., Liu, B., Schaller, F., Piotrowski, M., Otagaki, S., Takahashi, K., Matsuura, H., Yoshihara, T. and Nabeta, K. 2009. Expression of allene oxide cyclase from Pharbitis nil upon theobroxide treatment. Biosci. Biotechnol. Biochem. 73:1007−1013.
  10. Lamb, C. and Dixon, R. A. 1997. The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. 48:251−275.
  11. Levine, A., Tenhaken, R., Dixon, R. and Lamb, C. 1994. $H_{2}O_{2}$ from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583−593.
  12. Marrs, K. A. 1996. The functions and regulation of glutathione Stransferases in plants. Annu. Rev. Plant Physiol. Mol. Biol. 47:127−158.
  13. May, M. J., Hammond-Kosack, K. E. and Jones, J. D. G. 1996. Involvement of reactive oxygen species, glutathione metabolism, and lipid peroxidation in the gene-dependent defense response of tomato cotyledons induced by race-specific elicitors of Cladosporium fulvum. Plant Physiol. 110:1367−1379.
  14. Mei, C., Qi, M., Sheng, G. and Yang, Y. 2006. Inducible overexpression of a rice allene oxide synthase gene increases the endogenous jasmonic acid level, PR gene expression, and host resistance to fungal infection. Mol. Plant-Microbe Interact. 19:1127−1137.
  15. Moons, A. 2003. Osgstu3 and osgtu4, encoding tau class glutathione S-transferases, are heavy metal- and hypoxic stress-induced and differentially salt stress-responsive in rice roots. FEBS Lett. 53:427−432.
  16. Nakamori, K., Matsuura, H., Yoshihara, T., Ichihara, A. and Koda, Y. 1994. Potato microtuber inducing substances from Lasiodiplodia theobromae. Phytochemistry 35:835−839. https://doi.org/10.1016/S0031-9422(00)90622-8
  17. Niki, T., Mituhara, I., Seo, S., Ohtsubo, N. and Ohashi, Y. 1998. Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leaves. Plant Cell Physiol. 39:500−507.
  18. Ortiz-Castro, R., Contreras-Cornejo, H. A., Macias-Rodriguez, L. and Lopez-Bucio, J. 2009. The role of microbial signals in plant growth and development. Plant Signal. Behav. 4:701−712.
  19. Pieterse, C. M. J., Van Wees, S. C. M., Van Pelt, J. A., Knoester, M., Laan, R., Gerrits, N., Weisbeek, P. J. and Loon, L. C. 1998. A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571−1580. https://doi.org/10.1105/tpc.10.9.1571
  20. Roxas, V. P., Smith, R. K., Allen E. R. and Allen, R. D. 1997. Overexpression of glutathione-S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nat. Biotechnol. 15:988−991.
  21. Rudrappa, T., Biedrzycki, M. L., Kunjeti, S. G., Donofrio, N. M., Czymmek, K. J., Paré, P. W. and Bais, H. P. 2010. The rhizobacterial elicitor acetoin induces systemic resistance in Arabidopsis thaliana. Commun. Integr. Biol. 3:130−138.
  22. Santamaria, M., Thomson, C. J., Read, N. D. and Loake, G. J. 2001. The promoter of a basic PR1-like gene, AtPRB1, from Arabidopsis establishes an organ-specific expression pattern and responsiveness to ethylene and methyl jasmonate. Plant Mol. Biol. 47:641−652.
  23. Schaller, A. and Stinzi, A. 2009. Enzymes in jasmonates biosynthesis -structure, function, regulation. Phytochemistry 70:1532 −1538.
  24. Schneider, M., Schweizer, P., Meuwly, P. and Métraux, J. P. 1996. Systemic acquired resistance in plants. Intl. Rev. Cytol. 168: 303−340.
  25. Thomma, B., Eggermont, K., Penninckx, I., Mauch-Mani, B., Vogelsang, R., Cammue, B. P. A. and Broekaert, W. F. 1998. Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct pathogens. Proc. Natl. Acad. Sci. USA 95:15107− 15111.
  26. Thomma, B., Eggermont, K., Broekaert, W. F. and Cammue, B. P. A. 2000. Disease development of several fungi on Arabidopsis can be reduced by treatment with methyl jasmonate. Plant Physiol. Biochem. 38:421−427.
  27. Ulmasov, T., Ohmiya, A., Hagen, G. and Guilfoyle, T. 1995. The soybean GH2/4 gene that encodes a glutathione-S-transferase has a promoter that is activated by a wide range of chemical agents. Plant Physiol. 108:919−927.
  28. Van Loon, L. C. and Van Strien, E. A. 1999. The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol. Mol. Plant Pathol. 55:85−97.
  29. Van Loon, L. C., Rep, M. and Pieterse, C. M. J. 2006. Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44:135−162.
  30. Veena, J. H., Doerge, R. W. and Gelvin, S. B. 2003. Transfer of TDNA and Vir proteins to plant cells by Agrobacterium tumefaciens induces expression of host genes involved in mediating transformation and suppresses host defense gene expression. Plant J. 35:219−236.
  31. Wagner, U., Edwards, R., Dixon, D. P. and Mauch, F. 2002. Probing the diversity of the Arabidopsis glutathione-S-transferase gene family. Plant Mol. Biol. 49:515−532.
  32. Yang, Q., Gao, X., Fujino, Y., Matsuura, H. and Yoshihara, T. 2004. Effects of theobroxide, a natural product, on the level of endogenous jasmonoids. Z. Naturforsch. 59:828−834.
  33. Yang, Y., Shah, J. and Klessig, D. F. 1997. Signal perception and transduction in plant defense responses. Genes Dev. 11:1621− 1639.
  34. Yoshihara, T., Ohmori, F., Nakamori, K., Amanuma, M., Tsutsumi, T., Ichihara, A. and Matsuura, H. 2000. Induction of plant tubers and flower buds under non-inducing photoperiod conditions by a natural product, theobroxide. J. Plant Growth Regul. 19:457−461.
  35. Zipfel, C., Kunze, G., Chinchilla, D., Caniard, A., Jones, J. D., Boller, T. and Felix, G. 2006. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacteriummediated transformation. Cell 125:749−760.

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