Induction of Basal Resistance by Methyl Jasmonate against Fusarium culmorumin Bread Wheat

Abstract

Fusarium culmorum is a soilborne fungal pathogen, agent of crown and root rot disease (FCRR), responsible of major economic losses in wheat plants. This host-pathogen interaction, following methyl jasmonate (MeJA) application at the beginning of the necrotrophic stage of infection, has not been previously studied at molecular level. In this study, using real-time quantitative PCR, the emerging role of MeJA in the basal resistance of two bread wheat cultivars against F. culmorum has been investigated. MeJA treatment was dispensed 6 hours after pathogen inoculation (6 hai) to detect the defense response at the beginning of the necrotrophic stage. The expression of phenylalanine ammonia-lyase (PAL), lipoxygenase (LOX), cytochrome P450 (CYP709C1) genes and of some pathogenesis related (PR) genes, including PR3, PR4 and PR9, was examined in both root and crown tissues of the susceptible wheat cultivar Falat and the tolerant cultivar Sumai3. The pathogen responsive defense genes were induced in both cultivars, with a higher level of induction in Sumai3 than in Falat. MeJA treatment reduced the symptoms in cv Falat, whereas no significant effects have been detected in cv Sumai3. In fact, MeJA treatment caused a striking difference in defense gene induction. The genetic change was present in root and crown tissues of both wheat cultivars, demonstrating a systemic signaling pathway. The chemically induced protection correlated with induction of the F. culmorum-responsive genes supports a possible role of jasmonate signaling in regulating basal resistance in wheat-F. culmorum interaction.

References

  1. Backhouse, D., Burgess, L.W. 2002. Climatic analysis of the distribution of Fusarium graminearum, F. pseudograminearumand F. culmorumon cereals in Australia. Austr. Plant Pathol. 31:321–332.

    Article  Google Scholar 

  2. Bari, R., Jones, J.D.G. 2009. Role of plant hormones in plant defense responses. Plant Mol. Biol. 69:473–488.

    CAS  Article  Google Scholar 

  3. Beccari, G., Covarelli, L., Nicholson, P. 2011. Infection processes and soft wheat response to root rot and crown rot caused by Fusarium culmorum.Plant Pathol. 60:671–684.

    CAS  Article  Google Scholar 

  4. Bell, E., Mullet, J.E. 1993. Characterization of an Arabidopsislipoxygenase gene responsive to methyl jasmonate and wounding. Plant Physiol. 103:1133–1137.

    CAS  Article  Google Scholar 

  5. Caruso, C., Chilosi, G., Caporale, C., Leonardi, L., Bertini, L., Magro, P., Buonocore, V. 1999. Induction of pathogenesis-related proteins in germinating wheat seeds infected with Fusarium culmorum. Plant Sci. 140:87–97.

    CAS  Article  Google Scholar 

  6. Chaturvedi, R., Shah, J. 2007. Salicylic acid in plant disease resistance. In: Hayat, S., Ahmad, A. (eds), Salicylic Acid-A Plant Hormone. Springer. Dordrecht, The Netherlands. pp. 335–370.

  7. Chen, C., Belanger, R.R., Benhamou, N., Paulitz, T.C. 2000. Defense enzymes induced in cucumber roots by treatment with plant growth-promoting rhizobacteria (PGPR) and Pythium aphanidermatum. Physiol. and Mol. Plant Pathol. 56:13–23.

    CAS  Article  Google Scholar 

  8. Coram, T.E., Wang, M.N., Chen, X.M. 2008. Transcriptome analysis of the wheat–Puccinia striiformisf.sp. triticiinteraction.Mol. Plant Pathol. 9:157–169.

    CAS  Article  Google Scholar 

  9. Creelman, R.A., Mullet, J.E. 1997. Oligosaccharins, brassinolides and jasmonates: nontraditional regulators of plant growth, development, and gene expression. Plant Cell 9:1211–1223.

    CAS  Article  Google Scholar 

  10. Desmond, O.J., Edgar, C.I., Manners, J.M., Maclean, D.J., Schenk, P.M., Kazan, K. 2006. Methyl jasmonate induced gene expression in wheat delays symptom development by the crown rot pathogen Fusarium pseudograminearum. Physiol. and Mol. Plant Pathol. 67:171–179.

    Article  Google Scholar 

  11. Desmond, O.J., Manners, J.M., Schenk, P.M., Maclean, D.J., Kazan, K. 2008. Gene expression analysis of the wheat response to infection by Fusarium pseudograminearum. Physiol. and Mol. Plant Pathol. 3:40–47.

    Article  Google Scholar 

  12. Devi, P.U.M., Reddy, P.S., Rani, N.U., Reddy, K., Reddy, M.N., Reddanna, P. 2000. Lipoxygenase metabolites of α-linolenic acid in the development of resistance in Pigeon pea, Cajanus cajan(L.) Millsp, seedlings against Fusarium uduminfection. Eur. J. Plant Pathol. 106:857–865.

    CAS  Article  Google Scholar 

  13. Ding, L., Xu, H., Yi, H., Yang, L., Kong, Z., Zhang, L., Xue, S., Jia, H., Ma, Z. 2011. Resistance to hemibiotrophic F. graminearuminfection is associated with coordinated and ordered expression of diverse defense signaling pathways. PLOS One, 6:e19008.

    CAS  Article  Google Scholar 

  14. Durrant, W.E., Dong, X. 2004. Systemic acquired resistance. Annu. Rev. Phytopathol. 42:185–209.

    CAS  Article  Google Scholar 

  15. Glazebrook, J. 2005. Contrasting mechanism of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43:205–227.

    CAS  Article  Google Scholar 

  16. Hope, R., Magan, N. 2003. Two-dimensional environmental profiles of growth, deoxynivalenol and nivalenol production by Fusarium culmorumon a wheat-based substrate. Letters in Appl. Microbiol. 37:70–74.

    CAS  Article  Google Scholar 

  17. Li, G., Yen, Y. 2008. Jasmonate and ethylene signaling pathway may mediate Fusariumhead blight resistance in wheat. Crop Sci. 48:1888–1896.

    Article  Google Scholar 

  18. Li, X., Zhang, J.B., Song, B., Li, H.P., Xu, H.Q., Qu, B., Dang, F.J., Liao, Y.C. 2010. Resistance to Fusariumhead blight and seedling blight in wheat is associated with activation of a cytochrome P450 gene. Phytopathol. 100:183–191.

    CAS  Article  Google Scholar 

  19. Livak, K.J., Schmittgen, T.D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods 25:402–408.

    CAS  Article  Google Scholar 

  20. Makandar, R., Nalam, V., Chaturvedi, R., Jeannotte, R., Sparks, A.A., Shah, J. 2010. Involvement of salicylate and jasmonate signaling pathways in Arabidopsisinteraction with Fusarium graminearum. Mol. Plant-Microbe Interactions 23:861–870.

    CAS  Article  Google Scholar 

  21. Makandar, R., Nalam, V.J., Lee, H., Trick, H.N., Dong, Y., Shah, J. 2012. Salicylic acid regulates basal resistance to Fusariumhead blight in wheat. Mol. Plant-Microbe Interactions 25:431–439.

    CAS  Article  Google Scholar 

  22. Mandal, S., Mallick, N., Mitra, A. 2009. Salicylic acid-induced resistance to Fusarium oxysporumf.sp. lycopersiciin tomato. Plant Physiol. and Biochem. 47:642–649.

    CAS  Article  Google Scholar 

  23. McKinney, H.H. 1923. Influence of soil temperature and moisture on infection of wheat seedlings by Helminthosporium sativum. J. of Agric. Res. 26:195–217.

    Google Scholar 

  24. Mhaske, S.D., Mahatma, M.K., Jha, S., Singh, P., Ahmad, T. 2013. Polyamine metabolism and lipoxygenase activity during Fusarium oxysporumf. sp. ricini-castor interaction. Physiol. and Mol. Biol. of Plants 19:323–331.

    CAS  Article  Google Scholar 

  25. Motallebi, P., Alkadri, D., Pisi, A., Nipoti, P., Tonti, S., Niknam, V., Hashemi, M., Prodi, A. 2015a. Biomolecular study on Iranian Fusarium culmorumstrains on durum wheat and comparison with Italian and Syrian populations. Phytopathologia Mediterranea, 54:437−445.

    Google Scholar 

  26. Motallebi, P., Niknam, V., Ebrahimzadeh, H., Hashemi, M., Pisi, A., Prodi, A., Tonti, S., Nipoti, P. 2015b. Methyl jasmonate strengthens wheat plants against root and crown rot pathogen Fusarium culmoruminfection. J. of Plant Growth Regulation 34:624–636.

    CAS  Article  Google Scholar 

  27. Petti, C., Reiber, K., Ali, S.S., Berney, M., Doohan, F.M. 2012. Auxin as a player in the biocontrol of Fusariumhead blight disease of barley and its potential as a disease control agent. BMC Plant Biol. 12:224.

    CAS  Article  Google Scholar 

  28. Pieterse, C.M.J., Leon-Reyes, A., Van der Ent, S., Van Wees, S.C.M. 2009. Networking by small-molecule hormones in plant immunity. Nature Chem. Biol. 5:308–316.

    CAS  Article  Google Scholar 

  29. Scherm, B., Balmas, V., Spanu, F., Pani, G., Delogu, G., Pasquali, M., Migheli, Q. 2013. Fusarium culmorum: causal agent of foot and root rot and head blight on wheat. Mol. Plant Pathol. 14:323–341.

    CAS  Article  Google Scholar 

  30. Verhagen, B.W.M., Glazebrook, J., Zhu, T., Chang, H.S., Van Loon, L.C., Pieterse, C.M.J. 2004. The transcriptome of rhizobacteria induced systemic resistance in Arabidopsis. Mol. Plant-Microbe Interactions 17:895–908.

    CAS  Article  Google Scholar 

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Correspondence to S. Tonti.

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Communicated by J. Kolmer

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Motallebi, P., Tonti, S., Niknam, V. et al. Induction of Basal Resistance by Methyl Jasmonate against Fusarium culmorumin Bread Wheat. CEREAL RESEARCH COMMUNICATIONS 45, 248–259 (2017). https://doi.org/10.1556/0806.45.2017.008

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Keywords

  • Fusarium culmorum
  • systemic acquired resistance
  • methyl jasmonate
  • realtime quantitative PCR
  • Triticum aestivum