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Russian Journal of Plant Physiology

, Volume 63, Issue 5, pp 609–619 | Cite as

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

  • S. V. Veselova
  • G. F. Burkhanova
  • T. V. Nuzhnaya
  • I. V. Maksimov
Research Papers

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.

Keywords

Triticum aestivum Septoria nodorum cytokinins ethylene hydrogen peroxide immunolocalization PR proteins resistance 

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

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References

  1. 1.
    Kazan, K. and Lyons, R., Intervention of phytohormone pathways by pathogen effectors, Plant Cell, 2014, vol. 26, pp. 2285–2309.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 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.CrossRefPubMedGoogle Scholar
  3. 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.CrossRefPubMedGoogle Scholar
  4. 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.CrossRefPubMedGoogle Scholar
  5. 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.PubMedGoogle Scholar
  6. 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.2013.00451PubMedPubMedCentralGoogle Scholar
  7. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 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.CrossRefPubMedGoogle Scholar
  9. 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.CrossRefGoogle Scholar
  10. 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.CrossRefGoogle Scholar
  11. 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.CrossRefGoogle Scholar
  12. 12.
    Warner, H.L. and Leopold, A.C., Ethylene evolution from 2-chloroethylphosphonic acid, Plant Physiol., 1969, vol. 44, pp. 156–158.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 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.CrossRefGoogle Scholar
  14. 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.0072571CrossRefGoogle Scholar
  15. 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.CrossRefGoogle Scholar
  16. 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.CrossRefGoogle Scholar
  17. 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.CrossRefPubMedGoogle Scholar
  18. 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.Google Scholar
  19. 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.Google Scholar
  20. 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.CrossRefPubMedGoogle Scholar
  21. 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.CrossRefPubMedGoogle Scholar
  22. 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.CrossRefPubMedGoogle Scholar
  23. 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.CrossRefGoogle Scholar
  24. 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.0070289CrossRefPubMedPubMedCentralGoogle Scholar
  25. 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.Google Scholar
  26. 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.CrossRefGoogle Scholar
  27. 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.CrossRefGoogle Scholar
  28. 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.CrossRefPubMedGoogle Scholar
  29. 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.CrossRefGoogle Scholar
  30. 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.CrossRefPubMedGoogle Scholar
  31. 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.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2016

Authors and Affiliations

  • S. V. Veselova
    • 1
  • G. F. Burkhanova
    • 1
  • T. V. Nuzhnaya
    • 1
  • I. V. Maksimov
    • 1
  1. 1.Institute of Biochemistry and Genetics, Ufa Scientific CenterRussian Academy of SciencesUfaBashkortostan, Russia

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