Skip to main content
Log in

Roles of ethylene and cytokinins in development of defense responses in Triticum aestivum plants infected with Septoria nodorum

  • Research Papers
  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

Effects of ethephon (2-chloroethylphosphonic acid, ET), which is a producer of ethylene, and 1-methylcyclopropene (1-MCP), which inhibits ethylene binding with the corresponding receptors, on defense responses caused by the causal agent of leaf blotch (Septoria nodorum Berk.) in leaves of soft spring wheat (Triticum aestivum L.) of cultivars contrast in the resistance to the pathogen were studied. After treatment with 1-MCP, an induction of wheat resistance to the disease, more prominent in the susceptible cv. Kazakhstanskaya 10 than in the resistant cv. Omskaya 35, was found. The rise in the resistance was accompanied by rise in zeatin content in leaves, enhanced generation of hydrogen peroxide (most likely, due to the decreased catalase activity and increased peroxidase activity), and accumulation of transcripts of marker genes of the salicylate signaling pathway (PR-1 and PR-2). On the contrary, in ET-treated plants, all the studied defense responses were inhibited, and the pathogen developed more intensively. The effect of ethylene on zeatin distribution in infected wheat leaves of the susceptible cv. Kazakhstanskaya 10 was also found. In the 1-MCP-treated wheat leaves, cytokinins were localized in mesophyll cells and cell walls. In the ET-treated leaves, cell walls were free of zeatin, and the hormone concentrated in developing hyphae of the pathogen. The results allow for the hypothesis that wheat plant resistance is controlled by antagonistic interaction of signaling pathways of salicylic acid and ethylene with participation of cytokinins.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

CAT:

catalase

CK:

cytokinin

ET:

ethephon

H2O2 :

hydrogen peroxide

JA:

jasmonic acid

Kaz10:

Kazakhstanskaya 10

1-MCP:

1-methylcyclopropene

Om35:

Omskaya 35

PO:

peroxidase

PB:

Na-phosphate buffer

PR proteins:

pathogenesis-related proteins

SA:

salicylic acid

References

  1. Kazan, K. and Lyons, R., Intervention of phytohormone pathways by pathogen effectors, Plant Cell, 2014, vol. 26, pp. 2285–2309.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Almagro, L., Gomez, Ros, L.V., Belchi-Navarro, S., Bru, R., Ros, Barcello, A., and Pedreno, M.A., Class III peroxidases in plant defence reactions, J. Exp. Bot., 2009, vol. 60, pp. 377–390.

    Article  CAS  PubMed  Google Scholar 

  3. Barna, B., Fodor, J., Harrach, B.D., Pogány, M., and Király, Z., The Janus face of reactive oxygen species in resistance and susceptibility of plants to necrotrophic and biotrophic pathogens, Plant Physiol. Biochem., 2012, vol. 59, pp. 37–43.

    Article  CAS  PubMed  Google Scholar 

  4. Van Loon, L.C., Rep, M., and Pieterse, C.M., Significance of inducible defense-related proteins in infected plants, Annu. Rev. Phytopathol., 2006, vol. 44, pp. 135–162.

    Article  PubMed  Google Scholar 

  5. Broekgaarden, C., Caarls, L., Vos, I.A., Pieterse, C.M.J., and van Wees, S.C.M., Ethylene: traffic controller on hormonal crossroads to defense, Plant Physiol., 2015, vol. 169, pp. 2371–2379.

    CAS  PubMed  Google Scholar 

  6. O'Brien, J.A. and Benková, E., Cytokinin cross-talking during biotic and abiotic stress responses, Front. Plant Sci., 2013, vol. 4, p. 451. doi 10.3389/fpls.2013.00451

    PubMed  PubMed Central  Google Scholar 

  7. Chen, H., Xue, L., Chintamanani, S., Germain, H., Lin, H., Cui, H., Cai, R., Zuo, J., Tang, X., Li, X., Guo, H., and Zhou, J.M., Ethylene INSENSITIVE3 and ETHYLENE INSENSITIVE3-LIKE1 repress SALICYLIC ACID INDUCTION DEFICIENT2 expression to negatively regulate plant innate immunity in Arabidopsis, Plant Cell, 2009, vol. 21, pp. 2527–2540.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Choi, J., Huh, S.U., Kojima, M., Sakakibara, H., Paek, K.H., and Hwang, I., The cytokinin-activated transcription factor ARR2 promotes plant immunity via TGA3/NPR1-dependent salicylic acid signaling in Arabidopsis, Dev. Cell, 2010, vol. 19, pp. 284–295.

    Article  CAS  PubMed  Google Scholar 

  9. Choi, J., Choi, D., Lee, S., Ryu, C.M., and Hwang, I., Cytokinins and plant immunity: old foes or new friends? Trends Plant Sci., 2011, vol. 7, pp. 388–394.

    Article  Google Scholar 

  10. Jiang, C.J., Shimono, M., Sugano, S., Kojima, M., Liu, X., Inoue, H., Sakakibara, H., and Takatsuji, H., Cytokinins act synergistically with salicylic acid to activate defense gene expression in rice, Mol. Plant–Microbe Interact., 2013, vol. 3, pp. 287–296.

    Article  Google Scholar 

  11. Sharipova, G.V., Veselov, D.S., Kudoyarova, G.R., Timergalin, M.D., and Wilkinson, S., Effect of ethylene perception inhibitor on growth, water relations, and abscisic acid content in wheat plants under water deficit, Russ. J. Plant Physiol., 2012, vol. 59, pp. 573–580.

    Article  CAS  Google Scholar 

  12. Warner, H.L. and Leopold, A.C., Ethylene evolution from 2-chloroethylphosphonic acid, Plant Physiol., 1969, vol. 44, pp. 156–158.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Maksimov, I.V., Sorokan’, A.V., Cherepanova, E.A., Surina, O.B., Troshina, N.B., and Yarullina, L.G., Effects of salicylic and jasmonic acids on the components of pro/antioxidant system in potato plants infected with late blight, Russ. J. Plant Physiol., 2011, vol. 58, pp. 299–306.

    Article  CAS  Google Scholar 

  14. Xing, L., Qian, C., Cao, A., Li, Y., Jiang, Z., Li, M., Jin, X., Hu, J., Zhang, Y., Wang, X., and Chen, P., The Hv-SGT1 gene from Haynaldia villosa contributes to resistances towards both biotrophic and hemibiotrophic pathogens in common wheat (Triticum aestivum L.), PLoS One, 2013, vol. 3, p. e72571. doi 10.1371/journal.pone.0072571

    Article  Google Scholar 

  15. Maksimov, I.V., Valeev, A.Sh., Cherepanova, E.A., and Burkhanova, G.F., Effect of chitooligosaccharides with different degrees of acetylation on the activity of wheat pathogen-inducible anionic peroxidase, Appl. Biochem. Microbiol., 2014, vol. 50, pp. 82–87.

    Article  CAS  Google Scholar 

  16. Lu, Sh., Friesen, T.L., and Faris, J.D., Molecular characterization and genomic mapping of the pathogenesisrelated protein 1 (PR-1) gene family in hexaploid wheat (Triticum aestivum L.), Mol. Genet. Genom., 2011, vol. 285, pp. 485–503.

    Article  CAS  Google Scholar 

  17. Gimenez, M.J., Piston, F., and Atienza, S.G., Identification of suitable reference genes for normalization of qPCR data in comparative transcriptomics analyses in the Triticeae, Planta, 2011, vol. 233, pp. 163–173.

    Article  CAS  PubMed  Google Scholar 

  18. Akhiyarova, G.R. and Arkhipova, T.N., Exogenous zeatin accumulation in wheat root cells shows its role in regulation of cytokinin transport, Tsitologiya, 2010, vol. 52, pp. 1024–1031.

    CAS  Google Scholar 

  19. Yarullina, L.G., Veselova, S.V., Ibragimov, R.I., Shpirnaya, I.A., Kasimova, R.I., Akhatova, A.R., Tsvetkov, V.O., and Maksimov, I.V., Search for molecular markers of wheat resistance to fungal pathogens, Agr. Sci., 2014, vol. 5, pp. 722–729.

    CAS  Google Scholar 

  20. Zdarska, M., Dobisová, T., Gelová, Z., Pernisová, M., Dabravolski, S., and Hejátko, J., Illuminating light, cytokinin, and ethylene signalling crosstalk in plant development, J. Exp. Bot., 2015, vol. 66, pp. 4913–4931.

    Article  CAS  PubMed  Google Scholar 

  21. Yang, C., Lu, X., Ma, B., Chen, S.Y., and Zhang, J.S., Ethylene signaling in rice and Arabidopsis: conserved and diverged aspects, Mol. Plant, 2015, vol. 8, pp. 495–505.

    Article  CAS  PubMed  Google Scholar 

  22. Ma, Q.H. and Wang, X.M., Characterization of an ethylene receptor homologue from wheat and its expression during leaf senescence, J. Exp. Bot., 2003, vol. 54, pp. 1489–1490.

    Article  CAS  PubMed  Google Scholar 

  23. Vleesschauver, D.D., Yinong, Y., Casiana, V.C., and Monica, H., Abscisic acid-induced resistance against the brown spot pathogen Cochliobolus miyabeanus in rice involves MAP kinase-mediated repression of ethylene signaling, Plant Physiol., 2010, vol. 152, pp. 2036–2052.

    Article  Google Scholar 

  24. Sewelam, N., Kazan, K., Thomas-Hall, S.R., Kidd, B.N., Manners, J.M., and Schenk, P.M., ETHYLENE RESPONSE FACTOR 6 is a regulator of reactive oxygen species signaling in Arabidopsis, PLoS One, 2013, vol. 8, p. e70289. doi 10.1371/journal. pone.0070289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Wendland, M. and Hoffmann, G.M., Proof of quantitative resistance of wheat genotypes to Septoria nodorum by determining the post-infectional ethylene production, Z. Pflanzenk. Pflanzen., 1987, vol. 94, pp. 561–571.

    CAS  Google Scholar 

  26. Maksimov, I.V., Yarullina, L.G., Burkhanova, G.F., and Zaikina, E.A., Relationship between the aggressiveness and catalase activity of Septoria nodorum Berk. in wheat, Biol. Bull., 2013, vol. 5, pp. 441–446.

    Article  Google Scholar 

  27. Harrach, B.D., Fodor, J., Pogány, M., Preuss, J., and Barna, B., Antioxidant, ethylene and membrane leakage responses to powdery mildew infection of nearisogenic barley lines with various types of resistance, Eur. J. Plant Pathol., 2008, vol. 121, pp. 21–33.

    Article  CAS  Google Scholar 

  28. Sasaki, K., Iwai, T., Hiraga, S., Kuroda, K., Seo, S., Mitsuhara, I., Miyasaka, A., Iwano, M., Ito, H., Matsui, H., and Ohashi, Y., Ten rice peroxidases redundantly respond to multiple stresses including infection with rice blast fungus, Plant Cell Physiol., 2004, vol. 45, pp. 1442–1452.

    Article  CAS  PubMed  Google Scholar 

  29. Sorokan', A.V., Burkhanova, G.F., and Maksimov, I.V., Interaction between salicylate- and jasmonate-induced signal transduction pathways in the development of potato resistance to late blight with the involvement of peroxidase gene M21334, Russ. J. Plant Physiol., 2014, vol. 61, pp. 489–495.

    Article  Google Scholar 

  30. Smets, R., Le, J., Prinsen, E., Verbelen, J.-P., and van Onckelen, H.A., Cytokinin-induced hypocotyl elongation in light-grown Arabidopsis plants with inhibited ethylene action or indole-3-acetic acid transport, Planta, 2005, vol. 221, pp. 39–47.

    Article  CAS  PubMed  Google Scholar 

  31. Taverner, E., Letham, D., Wang, J., Cornish, E., and Willcocks, D., Influence of ethylene on cytokinin metabolism in relation to Petunia corolla senescence, Phytochemistry, 1999, vol. 51, pp. 341–347.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. V. Veselova.

Additional information

Original Russian Text © S.V. Veselova, G.F. Burkhanova, T.V. Nuzhnaya, I.V. Maksimov, 2016, published in Fiziologiya Rastenii, 2016, Vol. 63, No. 5, pp. 649–660.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Veselova, S.V., Burkhanova, G.F., Nuzhnaya, T.V. et al. Roles of ethylene and cytokinins in development of defense responses in Triticum aestivum plants infected with Septoria nodorum . Russ J Plant Physiol 63, 609–619 (2016). https://doi.org/10.1134/S1021443716050150

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1021443716050150

Keywords

Navigation