Magnaporthe oryzae infection triggers rice resistance to brown planthopper through the influence of jasmonic acid on the flavonoid biosynthesis pathway

Su Chen , Zhihuan Tao , Yanjie Shen , Rui Yang , Siyuan Yan , Zixu Chen , Bo Sun , Xiaofang Yang

Insect Science ›› 2025, Vol. 32 ›› Issue (1) : 243 -259.

PDF
Insect Science ›› 2025, Vol. 32 ›› Issue (1) : 243 -259. DOI: 10.1111/1744-7917.13378
ORIGINAL ARTICLE

Magnaporthe oryzae infection triggers rice resistance to brown planthopper through the influence of jasmonic acid on the flavonoid biosynthesis pathway

Author information +
History +
PDF

Abstract

In agroecosystems, plants are constantly exposed to attack from diverse herbivorous insects and microbes, and infestation with one species may change the plant defense response to other species. In our investigation of the relationships among rice plants, the brown planthopper Nilaparvata lugens (Stål) and the rice blast fungus Magnaporthe oryzae, we observed a significant increase in the resistance of rice treated with rice blast to N. lugens, as evidenced by improved plant survival rates in a small population resistance study. Subsequent transcriptome data analysis revealed that the rice blast fungus can induce the expression of genes in the jasmonic acid (JA) and flavonoid pathways. Similar to the flavonoid pathway, the JA pathway also contains 2 types of genes that exhibit similar and opposite trends in response to N. lugens and rice blast. Among these genes, the osjaz1 mutant and the osmyc2 mutant were phenotypically confirmed to positively and negatively regulate rice resistance to N. lugens and rice blast, respectively. Subsequent mass spectrometry and quantification experiments showed that the exogenous application of methyl jasmonate (MeJA) can induce the accumulation of eriodictyol, naringenin and quercetin, as well as the expression of OsF3H,Os4CL5 and OsCHI in the flavonoid pathway. This suggests a close connection between the JA pathway and the flavonoid pathway. However,OsF3’H, which negatively regulates rice resistance to N. lugens and rice blast, did not show increased expression. Phenotypic and molecular experiments confirmed that OsMYC2 can bind to and inhibit the expression of OsF3’H, thus revealing the mechanism of rice resistance to N. lugens after treatment with rice blast. These findings will deepen our understanding of the interactions among rice,N. lugens and rice blast.

Keywords

flavonoid / jasmonic acid / Nilaparvata lugens / rice / rice blast

Cite this article

Download citation ▾
Su Chen, Zhihuan Tao, Yanjie Shen, Rui Yang, Siyuan Yan, Zixu Chen, Bo Sun, Xiaofang Yang. Magnaporthe oryzae infection triggers rice resistance to brown planthopper through the influence of jasmonic acid on the flavonoid biosynthesis pathway. Insect Science, 2025, 32(1): 243-259 DOI:10.1111/1744-7917.13378

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Abramovitch, R.,Anderson, J. and Martin, G. (2006) Bacterial elicitation and evasion of plant innate immunity. Nature Reviews Molecular Cell Biology,7,601–611.

[2]

Bai, Q.X.,Duan, B.B.,Ma, J.C.,Fen, Y.N.,Sun, S.J.,Long, Q.M. et al. (2019) Coexpression of PalbHLH1 and PalMYB90 genes from Populus alba enhances pathogen resistance in poplar by increasing the flavonoid content. Frontiers in Plant Science,10,1772.

[3]

Boutrot, F. and Zipfel, C. (2017) Function, discovery, and exploitation of plant pattern recognition receptors for broad-spectrum disease resistance. Annual Review of Phytopathology,55,257–286.

[4]

Cai, Q.,Yuan, Z.,Chen, M.J.,Yin, C.S.,Luo, Z.J.,Zhao, X.X. et al. (2014) Jasmonic acid regulates spikelet development in rice. Nature Communications,5,3476.

[5]

Campos, L.,García, J. and San, B. (2012) The arbuscular mycorrhizal symbiosis promotes the systemic induction of regulatory defence-related genes in rice leaves and confers resistance to pathogen infection. Molecular Plant Pathology,13,579–592.

[6]

Chen, S.,Sun, B.,Shi, Z.Y.,Miao, X.X. and Li, H.C. (2022) Identification of the rice genes and metabolites involved in dual resistance against brown planthopper and rice blast fungus. Plant Cell Environment,45,1914–1929.

[7]

Couto, D. and Zipfel, C. (2016) Regulation of pattern recognition receptor signalling in plants. Nature Reviews Immunology,16,537–552.

[8]

Deng, Y.W. and He, Z.H. (2023) The seesaw action: balancing plant immunity and growth. Science Bulletin,69,3–6.

[9]

Flores, G.,Blanch, G.P. and Del Castillo, M.L.R. (2015) Postharvest treatment with (-) and (+)-methyl jasmonate stimulates anthocyanin accumulation in grapes. LWT – Food Science and Technology,62,807–812.

[10]

Fofana, B.,McNally, D.J.,Labbé C.,Boulanger, R.,Benhamou, N.,Séguin, A. et al. (2002) Milsana-induced resistance in powdery mildew-infected cucumber plants correlates with the induction of chalcone synthase and chalcone isomerase. Physiological and Molecular Plant Pathology,61,121–132.

[11]

Ge, Y.F.,Han, J.Y.,Zhou, G.X.,Xu, Y.M.,Ding, Y.,Shi, M. et al. (2018) Silencing of miR156 confers enhanced resistance to brown planthopper in rice. Planta,248,813–826.

[12]

Guo, J.P.,Xu, C.X.,Wu, D.,Zhao, Y.,Qiu, Y.F.,Wang, X.X. et al. (2018) Bph6 encodes an exocyst-localized protein and confers broad resistance to planthoppers in rice. Nature Genetics,50,297–306.

[13]

Havsteen, B.H. (2002) The biochemistry and medical significance of the flavonoids. Pharmacology & Therapeutics,96,67–202.

[14]

He, J.,Liu, Y.Q.,Yuan, D.Y.,Duan, M.J.,Liu, Y.L.,Shen, Z.J. et al. (2020) An R2R3 MYB transcription factor confers brown planthopper resistance by regulating the phenylalanine ammonia-lyase pathway in rice. Proceedings of the National Academy of Sciences USA,117,271–277.

[15]

Huang, X.J.,Li, J.,Shang, H.L. and Meng, X. (2015) Effect of methyl jasmonate on the anthocyanin content and antioxidant activity of blueberries during cold storage. Journal of the Science of Food and Agriculture,95,337–343.

[16]

Jiang, N.,Doseff, A.I. and Grotewold, E. (2016) Flavones: from biosynthesis to health benefits. Plants,5,27.

[17]

Jin, G.C.,Qi, J.F.,Zu, H.Y.,Liu, S.T.,Gershenzon, J.,Lou, Y.G. et al. (2023) Jasmonate-mediated gibberellin catabolism constrains growth during herbivore attack in rice. Plant Cell,35,3828–3844.

[18]

John, B. (2009) Jasmonate passes muster: a receptor and targets for the defense hormone. Annual Review of Plant Biology,60,183–205.

[19]

Jones, J. and Dangl, J. (2006) The plant immune system. Nature,444,323–329.

[20]

Kang, K.,Yue, L.,Xia, X.,Liu, K. and Zhang, W.Q. (2019) Comparative metabolomics analysis of different resistant rice varieties in response to the brown planthopper Nilaparvata lugens (Hemiptera: Delphacidae). Metabolomics,15,62.

[21]

Kanno, H.,Satoh, M.,Kimura, T. and Fujita, Y. (2005) Some aspects of induced resistance to rice blast fungus,Magnaporthe grisea, in rice plant infested by white-backed planthopper,Sogatella furcifera. Applied Entomology and Zoology,40,91–97.

[22]

Kano, M.,Takayanagi, T.,Harada, K.,Makino, K. and Ishikawa, F. (2005) Antioxidative activity of anthocyanins from purple sweet potato,Ipomoera batatas cultivar Ayamurasaki. Bioscience, Biotechnology, and Biochemistry,69,979–988.

[23]

Kruger, W.,Kroger, N.,Togel, F.,Badbaran, A.,Renges, H.,Gieseking, F. et al. (2001) Influence of preharvest tumor cell contamination in bone marrow or blood does not predict resultant tumor cell contamination of granulocyte colony-stimulating factor mobilized stem cells. Journal of Hematotherapy & Stem Cell Research,10,303–307.

[24]

Li, Y.,Chen, Y.,Zhou, L.,You, S.J.,Deng, H.,Chen, Y. et al. (2020) MicroTom metabolic network: rewiring tomato metabolic regulatory network throughout the growth cycle. Molecular Plant,13,1203–1218.

[25]

Liu, M.Y.,Hong, G.J.,Li, H.J.,Bing, X.L.,Chen, Y.M.,Jing, X.F. et al. (2023) Sakuranetin protects rice from brown planthopper attack by depleting its beneficial endosymbionts. Proceedings of the National Academy of Sciences USA,120,e2305007120.

[26]

Ma, X.L.,Zhang, Q.Y.,Zhu, Q.L.,Liu, W.,Chen, Y.,Qiu, R. et al. (2015) A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Molecular Plant,8,1274–1284.

[27]

Nalley, L.,Tsiboe, F.,Durand-Morat, A.,Shew, A. and Thoma, G. (2016) Economic and environmental impact of rice blast pathogen (Magnaporthe oryzae) alleviation in the United States. PLoS ONE,11,e0167295.

[28]

Perez, A.G.,Sanz, C.,Olias, R. and Olias, J.M. (1997) Effect of methyl jasmonate on in vitro strawberry ripening. Journal of Agricultural and Food Chemistry,45,3733–3737.

[29]

Qi, J.F.,Zhou, G.X.,Yang, L.J.,Erb, M.,Lu, Y.H.,Sun, X.L. et al. (2011) The chloroplast-localized phospholipases D alpha4 and alpha5 regulate herbivore-induced direct and indirect defenses in rice. Plant Physiology,157,1987–1999.

[30]

Qiu, J.H.,Xie, J.H.,Chen, Y.,Shen, Z.N.,Shi, H.B.,Naqvi, N.I. et al. (2022) Warm temperature compromises JA-regulated basal resistance to enhance Magnaporthe oryzae infection in rice. Molecular Plant,15,723–739.

[31]

Riemann, M.,Haga, K.,Shimizu, T.,Okada, K.,Ando, S.,Mochizuki, S. et al. (2013) Identification of rice allene oxide cyclase mutants and the function of jasmonate for defence against Magnaporthe oryzae. Plant Journal,74,226–238.

[32]

Salwan, R.,Sharma, M.,Sharma, A. and Sharma, V. (2023) Insights into plant beneficial microorganism-triggered induced systemic resistance. Plant Stress,7,100–140.

[33]

Savary, S.,Willocquet, L.,Pethybridge, S.J.,Esker, P.,Mcroberts, N. and Nelson, A. (2019) The global burden of pathogens and pests on major food crops. Nature Ecology & Evolution,3,430–439.

[34]

Su, P.S.,Zhao, L.F.,Li, W.,Zhao, J.X.,Yan, J.,Ma, X. et al. (2021) Integrated metabolo-transcriptomics and functional characterization reveals that the wheat auxin receptor TIR1 negatively regulates defense against Fusarium graminearum. Journal of Integrative Plant Biology,63,340–352.

[35]

Taniguchi, S.,Miyoshi, S.,Tamaoki, D.,Yamada, S.,Tanaka, K.,Uji, Y. et al. (2014) Isolation of jasmonate-induced sesquiterpene synthase of rice: product of which has an antifungal activity against Magnaporthe oryzae. Journal of Plant Physiology,171,625–632.

[36]

Uji, Y.,Taniguchi, S.,Tamaoki, D.,Shishido, H.,Akimitsu, K. and Gomi, K. (2016) Overexpression of OsMYC2 results in the up-regulation of early JA-responsive genes and bacterial blight resistance in rice. Plant and Cell Physiology,57,1814–1827.

[37]

Vos, M.,Oosten, V.,Jander, G.,Dicke, M. and Pieterse, C., (2007) Plants under attack: multiple interactions with insects and microbes. Plant Signaling & Behavior,2,527–529.

[38]

Wang, L.L.,Xu, G.J.,Li, L.H.,Ruan, M.Y.,Bennion, A.,Wang, G.L. et al. (2023) The OsBDR1-MPK3 module negatively regulates blast resistance by suppressing the jasmonate signaling and terpenoid biosynthesis pathway. Proceedings of the National Academy of Sciences USA,120,e2211102120.

[39]

Wang, Q.,Li, J.C.,Hu, L.F.,Zhang, T.F.,Zhang, G.R. and Lou, Y.G. (2013) OsMPK3 positively regulates the JA signaling pathway and plant resistance to a chewing herbivore in rice. Plant Cell Reports,32,1075–1084.

[40]

Wang, S.C.,Alseekh, S.,Fernie, A.R. and Luo, J. (2019) The structure and function of major plant metabolite modifications. Molecular Plant,12,899–919.

[41]

Wang, S.Y.,Bowman, L. and Ding, M. (2008) Methyl jasmonate enhances antioxidant activity and flavonoid content in blackberries (Rubus sp.) and promotes antiproliferation of human cancer cells. Food Chemistry,107,1261–1269.

[42]

Wasternack, C. and Song, S. (2017) Jasmonates: biosynthesis, metabolism, and signaling by proteins activating and repressing transcription. Journal of Experimental Botany,68,1303–1321.

[43]

Winkel-Shirley, B. (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiology,126,485–493.

[44]

Xiao, Y.,Gao, S.H.,Di, P.,Chen, J.F.,Chen, W.S. and Zhang, L. (2009) Methyl jasmonate dramatically enhances the accumulation of phenolic acids in Salvia miltiorrhiza hairy root cultures. Physiologia Plantarum,137,1–9.

[45]

Xu, J.,Wang, X.J.,Zu, H.Y.,Zeng, X.,Baldwin, I.T.,Lou, Y.G. et al. (2021) Molecular dissection of rice phytohormone signaling involved in resistance to a piercing-sucking herbivore. New Phytologist,230,1639–1652.

[46]

Yan, J.B.,Yao, R.F.,Chen, L.,Li, S.H.,Gu, M.,Nan, F.J. et al. (2018) Dynamic perception of jasmonates by the F-Box protein COI1. Molecular Plant,11,1237–1247.

[47]

Yang, Z.Y.,Li, N.N.,Kitano, T.,Li, P.,Spindel, J.E.,Wang, L.S. et al. (2021) Genetic mapping identifies a rice naringenin O-glucosyltransferase that influences insect resistance. Plant Journal,106,1401–1413.

[48]

Yuan, M.H.,Ngou, B.,Ding, P.T. and Xin, X.F. (2021) PTI-ETI crosstalk: an integrative view of plant immunity. Current Opinion in Plant Biology,62,102030.

[49]

Zeng, J.M.,Zhang, T.F.,Hang, J.Y.,Li, R. and Lou, Y.G. (2021) Both allene oxide synthases genes are involved in the biosynthesis of herbivore-induced jasmonic acid and herbivore resistance in rice. Plants,10,442.

[50]

Zhang, K.L.,Liu, Q.S.,Kang, H.X.,Liu, X.,Chen, X.M.,Peng, Y.F. et al. (2020) Herbivore-induced rice resistance against rice blast mediated by salicylic acid. Insect Science,27,49–57.

[51]

Zhang, J.,Guan, W.,Huang, C.M.,Hu, Y.X.,Chen, Y.,Guo, J.P. et al. (2019) Combining next-generation sequencing and single-molecule sequencing to explore brown plant hopper responses to contrasting genotypes of japonica rice. BMC Genomics,20,682.

[52]

Zhou, G.X.,Ren, N.,Qi, J.F.,Lu, J.,Xiang, C.Y.,Ju, H.P. et al. (2014) The 9-lipoxygenase Osr9-LOX1 interacts with the 13-lipoxygenase-mediated pathway to regulate resistance to chewing and piercing-sucking herbivores in rice. Physiologia Plantarum,152,59–69.

RIGHTS & PERMISSIONS

2024 The Authors. Insect Science published by John Wiley & Sons Australia, Ltd on behalf of Institute of Zoology, Chinese Academy of Sciences.

AI Summary AI Mindmap
PDF

292

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/