Biologia plantarum 63:690-698, 2019 | DOI: 10.32615/bp.2019.139
Application of sodium salicylate up-regulates defense responseagainst Fusarium graminearum in wheat spikes
- 1 Department of Plant Biology, School of Biology, College of Science, University of Tehran, 1417466191, Tehran, Iran
- 2 Department of Plant Pathology, Tarbiat Modares University, 1411713116, Tehran, Iran
- 3 Department of Genetic, School of Biological Sciences, Tarbiat Modares University, 1411713116, Tehran, Iran
- 4 Department of Plant Breeding and Biotechnology, Gorgan University of Agricultural Sciences and Natural Resources, 4918943464, Gorgan, Iran
- 5 Center of Excellence in Medicinal Plant Metabolites, Tarbiat Modares University, 1411713116, Tehran, Iran
Fusarium head blight caused by the hemibiotrophic fungus Fusarium graminearum is one of the most devastating diseases of wheat which reduces both grain yield and quality. To better understand mechanism underlying wheat resistance to this pathogen, the expressions of five candidate genes encoding phenylalanine ammonia-lyase (PAL), glucanase-2 (Gl 2), class IV chitinase (Cht-4), cytochrome P450 (CYP), and pleiotropic drug resistance (PDR) following spike inoculation with F. graminearum was compared in susceptible cv. Falat and resistant cv. Sumai3 at three time points (48, 96, 144 h after inoculation). Real-time quantitative PCR analysis indicated earlier and greater inductions of PAL, Glu-2, and Cht-4 in spikes of 'Sumai3' as compared to 'Falat' in response to F. graminearum inoculation. The expression of CYP in the resistant 'Sumai3' was about three times higher than in 'Falat' at 144 h after pathogen inoculation. Moreover, soil drench application of sodium salicylate (SA) one day before pathogen inoculation drastically curtailed pathogen infection in both the cultivars. Furthermore, SA treatment caused an induction of these genes in spikes of the susceptible cultivar to show a similar pattern as in the resistant one when inoculated with F. graminearum. Proteomics analysis of F. graminearum treated spikes 96 h after inoculation confirmed an increase of Glu and Cht spot volume in 'Sumai3' whereas a decrease in 'Falat'. The SA treatment also caused significant increases in Glu and Cht spot volumes in both the cultivars. Our findings show an association between SA improvement of wheat defense against F. graminearum infection and induction of genes encoding proteins involved in pathogen response (Glu-2, Cht-4), secondary metabolite biosyntheses (PAL), and xenobiotic detoxification (CYP and PDR).
Keywords: Cht-4, CYP, fusarium head blight, Glu-2, resistance, PAL, PDR, Triticum aestivum.
Received: September 19, 2015; Revised: April 1, 2019; Accepted: April 16, 2019; Published online: November 11, 2019 Show citation
| ACS | AIP | APA | ASA | Harvard | Chicago | Chicago Notes | IEEE | ISO690 | MLA | NLM | Turabian | Vancouver |
Supplementary files
| Download file | Sorahinobar4244 Suppl.pdf File size: 109.01 kB |
References
- Ancillo, G., Witte, B., Schmelzer, E., Kombrink, E.: A distinct member of the basic (class I) chitinase gene family in potato is specifically expressed in epidermal cells. - Plant mol. Biol. 39: 1137-1151, 1999.
Go to original source... - Bai, G., Shaner, G.: Management and resistance in wheat and barley to Fusarium head blight 1. - Annu. Rev. Phytopathol. 42: 135-161, 2004.
Go to original source... - Bienert, M.D., Siegmund, S.E., Drozak, A., Trombik, T., Bultreys, A., Baldwin, I.T., Boutry, M.: A pleiotropic drug resistance transporter in Nicotiana tabacum is involved in defense against the herbivore Manduca sexta. - Plant. J. 72: 745-757, 2012.
Go to original source... - Bokshi, A., Morris, S., Deverall, B.: Effects of benzothiadiazole and acetylsalicylic acid on β-1,3-glucanase activity and disease resistance in potato. - Plant Pathol. 52: 22-27, 2003.
Go to original source... - Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. - Anal. Biochem. 72: 248-254, 1976.
Go to original source... - Brederode, F.T., Linthorst, H.J.M., Bol, J.F.: Differential induction of acquired resistance and PR gene expression in tobacco by virus infection, ethephon treatment, UV light and wounding. - Plant mol. Biol. 17: 1117-1125, 1991.
Go to original source... - Buchter, R., Stromberg, A., Schmelzer, E., Kombrink, E.: Primary structure and expression of acidic (class II) chitinase in potato. - Plant mol. Biol. 35: 749-761, 1997.
Go to original source... - Chapple, C.: Molecular-genetic analysis of plant cytochrome P450-dependent monooxygenases. - Annu. Rev. Plant Biol. 49: 311-343, 1998.
Go to original source... - Dempsey, D.A., Vlot, A.C., Wildermuth, M.C., Klessig, D.F.: Salicylic acid biosynthesis and metabolism. - In: Torii, K. (ed.): The Arabidopsis Book. Pp. 1-24. Amer. Soc. Plant Biologists, Rockville 2011.
Go to original source... - Ding, C.K., Wang, C., Gross, K.C., Smith, D.L.: Jasmonate and salicylate induce the expression of pathogenesis-related-protein genes and increase resistance to chilling injury in tomato fruit. - Planta 214: 895-901, 2002.
Go to original source... - Ding, L., Xu, H., Yi, H., Yang, L., Kong, Z., Zhang, L., Ma, Z.: Resistance to hemi-biotrophic F. graminearum infection is associated with coordinated and ordered expression of diverse defense signaling pathways. - PloS ONE 6: e19008, 2011.
Go to original source... - Dong, X.: SA, JA, ethylene, and disease resistance in plants. - Curr. Opin. Plant Biol. 1: 316-323, 1998.
Go to original source... - Fraissinet-Tachet, L., Baltz, R., Chong, J., Kauffmann, S., Fritig, B., Saindrenan, P.: Two tobacco genes induced by infection, elicitor and salicylic acid encode glucosyl-transferases acting on phenylpropanoids and benzoic acid derivatives, including salicylic acid. - FEBS Lett. 437: 319-323, 1998.
Go to original source... - Gottwald, S., Samans, B., Lück, S., Friedt, W.: Jasmonate and ethylene dependent defence gene expression and suppression of fungal virulence factors: two essential mechanisms of Fusarium head blight resistance in wheat? - BMC Genomics 13: 369, 2012.
Go to original source... - Hwang, B.K., Sunwoo, J.Y., Kim, Y.J., Kim, B.S.: Accumulation of β-1,3-glucanase and chitinase isoforms, and salicylic acid in the DL-β-amino-n-butyric acid-induced resistance response of pepper stems to Phytophthora capsici. - Physiol. mol. Plant Pathol. 51: 305-322, 1997.
Go to original source... - Hurkman, W.J., Tanaka, C.K.: Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. - Plant Physiol. 81: 802-806, 1986.
Go to original source... - Jia, Y., Martin, G.B.: Rapid transcript accumulation of pathogenesis-related genes during an incompatible interaction in bacterial speck disease-resistant tomato plants. -Plant mol. Biol. 40: 455-465, 1999.
Go to original source... - Jones, J.D., Dangl, J.L.: The plant immune system. - Nature 444: 323-329, 2006.
Go to original source... - Kang, J., Hwang, J.-U., Lee, M., Kim, Y.-Y., Assmann, S. M., Martinoia, E., Lee, Y.: PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. - Proc. nat. Acad. Sci. USA 107: 2355-2360, 2010.
Go to original source... - Kim, D.S., Hwang, B.K.: An important role of the pepper phenylalanine ammonia-lyase gene (PAL1) in salicylic acid-dependent signaling of the defense response to microbial pathogens. - J. exp. Bot. 65: 2295-2306, 2014.
Go to original source... - Kong, L., Anderson, J.M., Ohm, H.W.: Induction of wheat defense and stress-related genes in response to Fusarium graminearum. - Genome 48: 29-40, 2005.
Go to original source... - Kosaka, A., Manickavelu, A., Kajihara, D., Nakagawa, H., Ban, T.: Altered gene expression profiles of wheat genotypes against Fusarium head blight. - Toxins 7: 604-620, 2015.
Go to original source... - Lawton, K.A., Beck, J., Potter, S., Ward, E., Ryals, J.: Regulation of cucumber class III chitinase gene expression. - Mol. Plant-Microbe Interact. 7: 48-57, 1994.
Go to original source... - Li, G., Yen, Y.; Jasmonate and ethylene signaling pathway may mediate Fusarium head blight resistance in wheat. - Crop Sci. 48:1888-1896, 2008.
Go to original source... - Li, X., Zhang, J., Song, B., Li, H., Xu, H., Qu, B., Liao, Y.: Resistance to Fusarium head blight and seedling blight in wheat is associated with activation of a cytochrome P450 gene. - Phytopathoogy 100: 183-191, 2010.
Go to original source... - Livak, K., Schmittgen, T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2- ΔΔCT method. - Methods 25: 402-408, 2001.
Go to original source... - Loake, G., Grant, M.: Salicylic acid in plant defence - the players and protagonists. - Curr. Opin. Plant Biol. 10: 466-472, 2007.
Go to original source... - Makandar, R., Essig, J.S., Schapaugh, M.A., Trick, H.N., Shah, J.: Genetically engineered resistance to Fusarium head blight in wheat by expression of Arabidopsis NPR1. - Mol. Plant-Microbe Interact. 19: 123-129, 2006.
Go to original source... - Makandar, R., Nalam, V., Chaturvedi, R., Jeannotte, R., Sparks, A.A., Shah, J.: Involvement of salicylate and jasmonate signaling pathways in Arabidopsis interaction with Fusarium graminearum. - Mol. Plant-Microbe Interact. 23: 861-870, 2010.
Go to original source... - Makandar, R., Nalam, V.J., Lee, H., Trick, H.N., Dong, Y., Shah, J.: Salicylic acid regulates basal resistance to Fusarium head blight in wheat. - Mol. Plant-Microbe Interact. 25: 431-439, 2012.
Go to original source... - Mitterbauer, R., Adam, G.: Saccharomyces cerevisiae and Arabidopsis thaliana: useful model systems for the identification of molecular mechanisms involved in resistance of plants to toxins. - In: Logrieco A., Bailey, J.A., Corazza L., Cooke B.M. (eds): Mycotoxins in Plant Disease. Pp. 699-703. Springer, Dordrecht 2002.
Go to original source... - Moosawi-Jorf, S.A., Farrokhi-Nejad, R., Azimi, S., Afarin, S.: Study of Fusarium Head Blight of wheat in Khuzestan Province in Iran and reporting of Fusarium xylaroides as new causal agents for disease. - J. Agron. 6: 212, 2007.
Go to original source... - Neuhoff, V., Arnold, N., Taube, D., Ehrhardt, W.: Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. - Electrophoresis 9: 255-262, 1988.
Go to original source... - Nürnberger, T., Brunner, F., Kemmerling, B., Piater, L.: Innate immunity in plants and animals: striking similarities and obvious differences. - Immunol. Rev. 198: 249-266, 2004.
Go to original source... - Paranidharan, V., Abu-Nada, Y., Hamzehzarghani, H., Kushalappa, A., Mamer, O., Dion, Y., Choiniere, L.: Resistance-related metabolites in wheat against Fusarium graminearum and the virulence factor deoxynivalenol (DON). - Botany 86: 1168-1179, 2008.
Go to original source... - Rivera, M.E., Codina, J.C., Olea, F., De Vicente, A., Pérez-García, A.: Differential expression of β-1, 3-glucanase in susceptible and resistant melon cultivars in response to infection by Sphaerotheca fusca. - Physiol. mol. Plant Pathol. 61: 257-265, 2002.
Go to original source... - Sadat Ejtehad, R., Radjabian, T., Tafreshi, S.A.H.: Expression analysis of phenylalanine ammonia lyase gene and rosmarinic acid production in Salvia officinalis and Salvia virgata shoots under salicylic acid elicitation. - Appl. Biochem. Biotechnol. 176: 1846-1858, 2015.
Go to original source... - Savitch, L.V., Subramaniam, R., Allard, G.C., Singh, J.: The GLK1 'regulon' encodes disease defense related proteins and confers resistance to Fusarium graminearum in Arabidopsis. - Biochem. Biophys. Res. Commun. 359: 234-238, 2007.
Go to original source... - Silverman, P., Seskar, M., Kanter, D., Schweizer, P., Metraux, J.-P., Raskin, I.: Salicylic acid in rice (biosynthesis, conjugation, and possible role). - Plant Physiol. 108: 633-639, 1995.
Go to original source... - Sorahinobar, M., Niknam, V., Ebrahimzadeh, H., Soltanloo, H., Behmanesh, M., Tahmasebi Enferadi, S.: Central role of salicylic acid in resistance of wheat against Fusarium graminearum. - J. Plant Growth Regul. 35: 477-491, 2016.
Go to original source... - Thulke, O., Conrath, U.: Salicylic acid has a dual role in the activation of defence-related genes in parsley. - Plant J. 14: 35-42, 1998.
Go to original source... - Van Kan, J.A., Joosten, M.H., Wagemakers, C.A., Van den Berg-Velthuis, G.C., De Wit, P.J.: Differential accumulation of mRNAs encoding extracellular and intracellular PR proteins in tomato induced by virulent and avirulent races of Cladosporium fulvum. - Plant. mol. Biol. 20: 513-527, 1992.
Go to original source... - Vidhyasekaran, P.: Salicylic acid signaling in plant innate immunity plant hormone signaling systems. - In: Vidhyasekaran P. (ed.): Plant Innate Immunity. Pp. 27-122. Springer, Dordrecht 2015.
Go to original source... - Walter, S., Brennan, J.M., Arunachalam, C., Ansari, K.I., Hu, X., Khan, M.R., Egan, D.: Components of the gene network associated with genotype-dependent response of wheat to the Fusarium mycotoxin deoxynivalenol. - Funct. integr. Genomics 8: 421-427, 2008.
Go to original source... - Wen, P.F., Chen, J.Y., Kong, W.F., Pan, Q.H., Wan, S.B., Huang, W.D.: Salicylic acid induced the expression of phenylalanine ammonia-lyase gene in grape berry. - Plant Sci. 169: 928-934, 2005.
Go to original source... - Woloshuk, C.P., Meulenhoff, J.S., Sela-Buurlage, M., Van den Elzen, P., Cornelissen, B.: Pathogen-induced proteins with inhibitory activity toward Phytophthora infestans. - Plant Cell 3: 619-628, 1991.
Go to original source... - Yu, G.Y., Muehlbauer, G.J.: Benzothiadiazole-induced gene expression in wheat spikes does not provide resistance to Fusarium head blight. - Physiol. mol. Plant Pathol. 59: 129-136, 2001.
Go to original source... - Zhang, H.-F., Li, Z.-H., Liu, J.-Y., Liu, T.-T., Wang, P., Fang, Y., Zhou, J., Cui, M.-Z., Gao, N., Tian, X.: Correlation of cytochrome P450 oxidoreductase expression with the expression of 10 isoforms of cytochrome P450 in human liver. - Drug Metab. Dispos. 44: 1193-1200, 2016.
Go to original source...



