Abstract
Rice sheath blight is caused by the necrotrophic soil-borne fungus Rhizoctonia solani Kühn. It is one of the most destructive rice disease. Jasmonic acid (JA) plays a vital role in plant defense mechanisms. This study aims to increase the understanding of JA in plant defense mechanisms against R. solani. In this study, we applied four different JA concentrations: 0.01, 0.1, 0.5, and 1 mM. JA application significantly increased the plant resistance against R. solani. The highest relative control of 82.38% was achieved by plants treated with a concentration of 0.1 mM. JA concentration of 0.1 mM is the most suitable treatment and above this concentration, the lesion length started to increase which indicates the reduction of plant resistance. Treatment 0.1 mM JA is further used to investigate defense-related enzymes and the expression of genes. 0.1 mM JA treatment effectively increases the activity of enzymes involved in plant defense mechanisms such as phenylalanine ammonia-lyase (PAL), peroxidase (POD), and β-1,3-glucanase, JA also lowers the malondialdehyde (MDA) content which proves its effectiveness against R. solani. The POX, PAL, and OsPR1b genes are the key marker genes for the plant defense, and the application of JA positively increases the relative expressions of these genes. These results confirm the significance of JA in plant defense mechanisms.
REFERENCES
VanWallendael, A., Soltani, A., Emery, N.C., Peixoto, M.M., Olsen, J., and Lowry, D.B., A molecular view of plant local adaptation: incorporating stress-response networks, Annu. Rev. Plant Biol., 2019, vol. 70, p. 559. https://doi.org/10.1146/annurev-arplant-050718-100114
Hane, J.K., Anderson, J.P., Williams, A.H., Sperschneider, J., and Singh, K.B., Genome sequencing and comparative genomics of the broad host-range pathogen Rhizoctonia solani AG8, PLoS Genet., 2014, vol. 10:e1004281. https://doi.org/10.1371/journal.pgen.1004281
Sridevi, G., Parameswari, C., Sabapathi, N., Raghupathy, V., and Veluthambi, K., Combined expression of chitinase and β-1, 3-glucanase genes in indica rice (Oryza sativa L.) enhances resistance against Rhizoctonia solani, Plant Sci., 2008, vol. 175, p. 283. https://doi.org/10.1016/j.plantsci.2008.04.011
Kagale, S., Marimuthu, T., Kagale, J., Thayumanavan, B., and Samiyappan, R., Induction of systemic resistance in rice by leaf extracts of Zizyphus jujuba and Ipomoea carnea against Rhizoctonia solani, Plant Signaling Behav., 2011, vol. 6, p. 919. https://doi.org/10.4161/psb.6.715304
Taheri, P., Gnanamanickam, S., and Höfte, M., Characterization, genetic structure, and pathogenicity of Rhizoctonia spp. associated with rice sheath diseases in India, Phytopathology, 2007, vol. 97, p. 373. https://doi.org/10.1094/PHYTO-97-3-0373
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, p. 135. https://doi.org/10.1146/annurev.phyto.44.070505.143425
Bari, R. and Jones, J.D., Role of plant hormones in plant defence responses, Plant Mol. Biol., 2009, vol. 69, p. 473. https://doi.org/10.1007/s11103-008-9435-0
Li, N., Han, X., Feng, D., Yuan, D., and Huang, L.J., Signaling crosstalk between salicylic acid and ethylene/jasmonate in plant defense: Do we understand what they are whispering? Int. J. Mol. Sci., 2019, vol. 20, p. 671. https://doi.org/10.3390/ijms20030671
Yang, J., Duan, G., Li, C., Liu, L., Han, G., Zhang, Y., and Wang, C., The crosstalks between jasmonic acid and other plant hormone signaling highlight the involvement of jasmonic acid as a core component in plant response to biotic and abiotic stresses, Front. Plant Sci., 2019, vol. 10, p. 1349. https://doi.org/10.3389/fpls.2019.01349
Wang, Y., Mostafa, S., Zeng, W., and Jin, B., Function and mechanism of jasmonic acid in plant responses to abiotic and biotic stresses, Int. J. Mol. Sci., 2021, vol. 22, p. 8568. https://doi.org/10.3390/ijms22168568
Peng, X., Hu, Y., Tang, X., Zhou, P., Deng, X., Wang, H., and Guo, Z., Constitutive expression of rice WRKY30 gene increases the endogenous jasmonic acid accumulation, PR gene expression and resistance to fungal pathogens in rice, Planta, 2012, vol. 236, p.1485. https://doi.org/10.1007/s00425-012-1698-7
Wang, H., Meng, J., Peng, X., Tang, X., Zhou, P., Xiang, J., and Deng, X., Rice WRKY4 acts as a transcriptional activator mediating defense responses toward Rhizoctonia solani, the causing agent of rice sheath blight, Plant Mol. Biol., 2015, vol. 89, p. 157. https://doi.org/10.1007/s11103-015-0360-8
Peng, X., Wang, H., Jang, J.C., Xiao, T., He, H., Jiang, D., and Tang, X., OsWRKY80-OsWRKY4 module as a positive regulatory circuit in rice resistance against Rhizoctonia solani, Rice, 2016, vol. 9, p. 1. https://doi.org/10.1186/s12284-016-0137-y
Moosa, A., Sahi, S.T., Khan, S.A., and Malik, A.U., Salicylic acid and jasmonic acid can suppress green and blue moulds of citrus fruit and induce the activity of polyphenol oxidase and peroxidase, Folia Hortic., 2019, vol. 31, p. 195. https://doi.org/10.2478/fhort-2019-0014
Motallebi, P., Niknam, V., Ebrahimzadeh, H., Hashemi, M., and Enferadi, S.T., Exogenous methyl jasmonate treatment induces defense response against Fusarium culmorum in wheat seedlings, J. Plant Growth Regul., 2017, vol. 36, p. 71. https://doi.org/10.1007/s00344-016-9620-3
Li, Y., Qiu, L., Zhang, Q., Zhuansun, X., Li, H., Chen, X., Krugman, T., Sun, Q., and Xie, C., Exogenous sodium diethyldithiocarbamate, a Jasmonic acid biosynthesis inhibitor, induced resistance to powdery mildew in wheat, Plant Direct, 2020, vol. 4, p. e00212. https://doi.org/10.1002/pld3.212
El Oirdi, M., El Rahman, T.A., Rigano, L., El Hadrami, A., Rodriguez, M.C., Daayf, F., Vojnov, A., and Bouarab, K., Botrytis cinerea manipulates the antagonistic effects between immune pathways to promote disease development in tomato, The Plant Cell, 2011, vol. 23, p. 2405. https://doi.org/10.1105/tpc.111.083394
Rahman, T.A.E., Oirdi, M.E., Gonzalez-Lamothe, R., and Bouarab, K., Necrotrophic pathogens use the salicylic acid signaling pathway to promote disease development in tomato, Mol. Plant-Microbe Interact., 2012, vol. 25, p. 1584. https://doi.org/10.1094/MPMI-07-12-0187-R
Mur, L.A., Kenton, P., Atzorn, R., Miersch, O., and Wasternack, C., The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death, Plant Physiol., 2006, vol. 140, p. 249. https://doi.org/10.1104/pp.105.072348
Kazan, K. and Manners, J.M., Jasmonate signaling: toward an integrated view, Plant Physiol., 2008, vol. 146, p. 1459. https://doi.org/10.1104/pp.107.115717
Park, D.S., Sayler, R.J., Hong, Y.G., Nam, M.H., and Yang, Y., A method for inoculation and evaluation of rice sheath blight disease, Plant Dis., 2008, vol. 92, p. 25. https://doi.org/10.1094/PDIS-92-1-0025
Xie, J.H., Chai, T.T., Xu, R., Liu, D., Yang, Y.X., Deng, Z.C., Jin, H., and He, H., Induction of defense-related enzymes in patchouli inoculated with virulent Ralstonia solanacearum, Electron. J. Biotechnol., 2017, vol. 27, p. 63. https://doi.org/10.1016/j.ejbt.2017.03.007
Rao, M.V., Paliyath, G., and Ormrod, D.P., Ulteraviolet-B and ozone- induced biochemical changes in antioxidant enzymes of Arabidopsis thalina, Plant Physiology, 1996, vol. 110, p. 125. https://doi.org/10.1104/pp.110.1.125
Aili Jiang, Shiping Tian, and Yazhuo Xu, Effect of controlled atmospheres with high O2 or high CO2 concentrations on postharvest physiology and storability of “Napoleon” sweet cherry, J. Integr. Plant Biol., 2002, vol. 44, p. 925.
Pan, S.Q., Ye, X.S., and Kuć, J., Association of β-1,3-glucanase activity and isoform pattern with systemic resistance to blue mould in tobacco induced by stem injection with Peronospora tabacina or leaf inoculation with tobacco mosaic virus, Physiol. Mol. Plant Pathol., 1991, vol. 39, p. 25. https://doi.org/10.1016/0885-5765(91)90029-H
Stewart, R.R. and Bewley, J.D., Lipid peroxidation associated with accelerated aging of soybean axes, Plant Physiol., 1980, vol. 65, p. 245. https://doi.org/10.1104/pp.65.2.245
Liao, C.M., Li, J., Liu, X.H., and Zhang, Y.S., An effective method for extracting total RNA from Dioscorea opposita Thunb., Genet. Mol. Res., 2014, vol. 13, p. 462. https://doi.org/10.4238/2014.January.21.15
Livak, K.J. and Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method, Methods, 2001, vol. 25, p. 402. https://doi.org/10.1006/meth.2001.1262
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, p. 1442. https://doi.org/10.1093/pcp/pch165
Tonnessen, B.W., Manosalva, P., Lang, J.M., Baraoidan, M., Bordeos, A., Mauleon, R., Oard, J., Hulbert, S., Leung, H., and Leach, J.E., Rice phenylalanine ammonia-lyase gene OsPAL4 is associated with broad spectrum disease resistance, Plant Mol. Biol., 2015, vol. 87, p. 273. https://doi.org/10.1007/s11103-014-0275-9
Agrawal, G.K., Rakwal, R., Jwa, N.S., and Agrawal, V.P., Signalling molecules and blast pathogen attack activates rice OsPR1a and OsPR1b genes: A model illustrating components participating during defence/stress response, Plant Physiol. Biochem., 2001, vol. 39, p. 1095. https://doi.org/10.1016/S0981-9428(01)01333-X
Taheri, P. and Tarighi, S., Riboflavin induces resistance in rice against Rhizoctonia solani via jasmonate-mediated priming of phenylpropanoid pathway, J. Plant Physiol., 2010, vol. 167, p. 201. https://doi.org/10.1016/j.jplph.2009.08.003
Zalewski, K., Lahuta, L.B., Martysiak-Żurowska, D., Okorski, A., Nitkiewicz, B., and Zielonka, Ł., Effect of exogenous application of methyl jasmonate on the lipid and carbohydrate content and composition of winter triticale (Triticosecale Wittm.) grain and the severity of fungal infections in triticale plants and grain, J. Agric. Food Chem., 2019, vol. 67, p. 5932. https://doi.org/10.1021/acs.jafc.9b00799
Singh, V., Singh, D., Gautam, J.K., and Nandi, A.K., RSI1/FLD is a positive regulator for defense against necrotrophic pathogens, Physiol. Mol. Plant Pathol., 2019, vol. 107, p. 40. https://doi.org/10.1016/j.pmpp.2019.04.005
Yang, Y.X., J Ahammed, G., Wu, C., Fan, S.Y., and Zhou, Y.H., Crosstalk among jasmonate, salicylate and ethylene signaling pathways in plant disease and immune responses, Curr. Protein Pept. Sci., 2015, vol. 16, p. 450. https://doi.org/10.2174/1389203716666150330141638
Liu, D., Zhao, Q., Cui, X., Chen, R., Li, X., Qiu, B., and Ge, F., A transcriptome analysis uncovers Panax notoginseng resistance to Fusarium solani induced by methyl jasmonate, Genes Genomics, 2019, vol. 41, p. 1383. https://doi.org/10.1007/s13258-019-00865-z
Alon, M., Malka, O., Eakteiman, G., Elbaz, M., Moyal Ben Zvi, M., Vainstein, A., and Morin, S., Activation of the phenylpropanoid pathway in Nicotiana tabacum improves the performance of the whitefly Bemisia tabaci via reduced jasmonate signaling, PloS One, 2013, vol. 8, p. e76619. https://doi.org/10.1371/journal.pone.0076619
Kumari, G.J., Reddy, A.M., Naik, S.T., Kumar, S.G., Prasanthi, J., Sriranganayakulu, G., Reddy, P.C., and Sudhakar, C., Jasmonic acid induced changes in protein pattern, antioxidative enzyme activities and peroxidase isozymes in peanut seedlings, Biol. Plant., 2006, vol. 50, p. 219. https://doi.org/10.1007/s10535-006-0010-8
Maksimov, I.V., Abizgildina, P.P., Sorokan, A.V., and Burkhanova, G.F., Regulation of peroxidase activity under the influence of signaling molecules and Bacillus subtilis 26D in potato plants infected with Phytophthora infestans, Appl. Biochem. Microbiol., 2014, vol. 50, p. 173. https://doi.org/10.1134/S0003683814020136
ACKNOWLEDGMENTS
The authors would like to thank Northeast Agricultural University, Harbin, China for their support. The authors are grateful to Prof. Zhang Junhua for his support and continuous encouragement.
Funding
This research has been supported by Natura Fund Project, Heilongjiang, China, grant number C2017032, Major project of Applied Technology research and development program of Heilongjiang, grant Number GA19B104, and National Science and Technology project of grain high yield (2018YFD0300105-5).
Author information
Authors and Affiliations
Contributions
Haseeb Younis designed the experiments. Zhong Qingyan, Liu Lian Fu, Yang Songrun and Peng Lili collected samples and performed the experiments. Mukadasi Rexiti, Yang Shuo, Shu Yu Wei, Faisal Siddique and Wang Meng, drafted the manuscript. Zhang Junhua supervised the research and all authors revised it.
Corresponding author
Ethics declarations
COMPLIANCE WITH ETHICAL STANDARDS
The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants as the object of research.
CONFLICT OF INTEREST
The authors declare that they have no conflict of interest.
Additional information
Abbreviations: ET—ethylene; JA—jasmonic acid; MDA—malondialdehyde; MeJA—methyl jasmonate; PAL—phenylalanine ammonia lyase; POD—peroxidase; PPO—polyphenol oxidase; qRT‑PCR—quantitative real-time PCR; SA—salicylic acid.
Supplementary Information
Rights and permissions
About this article
Cite this article
Younis, H., Qingyan, Z., Fu, L.L. et al. Exogenous Application of Jasmonic Acid Triggers the Rice Defense Mechanisms against Rhizoctonia solani Kühn. Russ J Plant Physiol 69, 167 (2022). https://doi.org/10.1134/S1021443722601665
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1134/S1021443722601665