Resistance to the Brown Planthopper Afforded by the Secondary Metabolite Coumarin in Rice

doi:10.16409/j.cnki.2095-039x.2025.09.019

Abstract

Abstract: Secondary metabolites play a crucial role in plant defense against pests and diseases. Based on previous metabolomic analyses of rice, this study employed HPLC to determine the content of the target compound coumarin. The results revealed that, when the rice plants were infested by the brown planthopper(BPH), the coumarin content in the leaf sheaths of the resistant rice line R1 was increased by 2.88 folds compared to the susceptible line S9. When coumarin was added to an artificial diet at 0.1 mg/mL and 0.5 mg/mL and fed to BPH, the survival rates of nymphs decreased by 38.89% and 80% at 7 days after treatment, respectively, compared to the control. Coumarin stress also led to a reduction in adult female body weight, an average decrease of 89 eggs in oviposition, and a 16.29% reduction in egg hatchability. The abundance of endosymbiotic fungi was decreased by 49.73% at 5 days after treatment, with significant reductions observed in fungi such as Ascomycetes and Arsenophonus in various BPH tissues. Molecular docking analysis revealed the interaction characteristics between coumarin and the candidate target protein carbonic anhydrase in BPH, providing preliminary insights into the mechanism of coumarin's effects on BPH. This study elucidates the resistance role of rice-derived coumarin against BPH and its endosymbiotic fungi, offering new clues for understanding rice insect resistance mechanisms and for the development of environmentally friendly pest management strategies.

Key words: rice, coumarin, brown planthopper, symbiotic bacteria

CLC Number:

S476

YAO Xinxuan, ZHOU Wenrun, CHEN Tongtong, YU Xiaoping, HAO Peiying. Resistance to the Brown Planthopper Afforded by the Secondary Metabolite Coumarin in Rice[J]. Chinese Journal of Biological Control, 2026, 42(3): 569-581.

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References

[1] 罗梅.水稻病虫害防治措施研究[J].世界热带农业信息, 2025(5):84-86.
[2] 韦凯通.水稻病虫害防治过程中的突出问题及其相应解决措施分析[J].种子世界, 2024(12):132-134.
[3] 金高晨,李冉.水稻与褐飞虱的分子互作研究进展[J].生命科学, 2025, 37(5):567-578.
[4] 袁龙宇,李燕芳,肖汉祥,等.褐飞虱致害性变异机制研究进展[J].环境昆虫学报, 2022, 44(2):297-304.
[5] 蒯鹏,娄永根.稻飞虱生物学、生态学及其防控技术研究进展[J].浙江大学学报(农业与生命科学版), 2022, 48(6):692-700.
[6] Roy D, Chakraborty G. Bio-efficacy of novel chemicals and tribal pesticide-based integrated modules against brown planthopper in rice[J]. International Journal of Tropical Insect Science, 2022, 10(5):1-11.
[7] 付迪,刘源,朱若男,等.褐飞虱对杀虫剂抗性研究进展[J].农业科技通讯, 2024(6):140-142.
[8] 沈炜,王圣印,汪天娜,等.褐飞虱综合防治策略[J].中国果业信息, 2025, 42(4):101-103.
[9] Martinez-Medina A, Flors V, Heil M, et al. Recognizing plant defense priming[J]. Trends in Plant Science, 2016, 21(10):818-822.
[10] Yang J, Sun X Q, Yan S Y, et al. Interaction of ferulic acid with glutathione S-transferase and carboxylesterase genes in the brown planthopper,Nilaparvata lugens[J]. Journal of Chemical Ecology, 2017, 43:693-702.
[11] Zhang Z, Cui B, Zhang Y. Electrical penetration graphs indicate that tricin is a key secondary metabolite of rice, inhibiting phloem feeding of brown planthopper, Nilaparvata lugens[J]. Entomologia Experimentalis et Applicata, 2015, 156(1):14-27.
[12] Gong G, Yuan L Y, Li Y F, et al. Salivary protein 7 of the brown planthopper functions as an effector for mediating tricin metabolism in rice plants[J].Scientific Reports, 2022, 12(1):3205.
[13] Liu M, Hong G, Li H, et al. Sakuranetin protects rice from brown planthopper attack by depleting its beneficial endosymbionts[J]. Proceedings of the National Academy of Sciences, 2023, 120(23):e2305007120.
[14] Uawisetwathana U, Chevallier O P, Xu Y, et al. Global metabolite profiles of rice brown planthopper-resistant traits reveal potential secondary metabolites for both constitutive and inducible defenses[J]. Metabolomics, 2019, 15:1-15.
[15] Kim E G, Yun S, Park J R, et al. Bio-efficacy of chrysoeriol7, a natural chemical and repellent, against brown planthopper in rice[J]. International Journal of Molecular Sciences, 2022, 23(3):1540.
[16] Xu J, Wang X, Zu H, et al. Molecular dissection of rice phytohormone signaling involved in resistance to a piercing-sucking herbivore[J]. New Phytologist, 2021, 230(4):1639-1652.
[17] Yoshida Y, Miyamoto K, Yamane H, et al. OsTGAP1 is responsible for JA-inducible diterpenoid phytoalexin biosynthesis in rice roots with biological impacts on allelopathic interaction[J]. Physiologia Plantarum, 2017, 161(4):532-544.
[18] Deng Z, Lai C, Zhang J, et al. Effects of secondary metabolites of rice on brown planthopper and its symbionts[J]. International Journal of Molecular Sciences, 2023, 25(1):386.
[19] Xia T, Liu Y, Lu Z, et al. Natural coumarin shows toxicity to Spodoptera litura by inhibiting detoxification enzymes and glycometabolism[J].International Journal of Molecular Sciences, 2023, 24(17):13177.
[20] Poudel S, Lee Y. Gustatory receptors required for avoiding the toxic compound coumarin in Drosophila melanogaster[J]. Molecules and Cells, 2016,39(4):310-315.
[21] Chen Y, Wang P C, Zhang S S, et al. Functional analysis of a bitter gustatory receptor highly expressed in the larval maxillary galea of Helicoverpa armigera[J]. PLoS Genetics, 2022, 18(10):e1010455.
[22] Pavela R, Maggi F, Benelli G. Coumarin(2H-1-benzopyran-2-one):A novel and eco-friendly aphicide[J]. Natural Product Research, 2021, 35(9):1566-1571.
[23] 王艳萍,范宇浍,马华燕,等.外源脱落酸对水稻苗期根系形态建成及其诱导化感作用的影响[J].应用与环境生物学报, 2024, 30(1):126-132.
[24] 于志超.东北天南星施肥模式及总黄酮超声提取工艺优化[D].延吉:延边大学, 2022.
[25] Fu Q, Zhang Z, Hu C, et al. A chemically defined diet enables continuous rearing of the brown planthopper, Nilaparvata lugens(Stål)(Homoptera:Delphacidae)[J]. Applied Entomology and Zoology, 2001, 36(1):111-116.
[26] 赖城玲.基于ddPCR技术的褐飞虱共生菌快速检测方法建立及其在水稻次生代谢物胁迫下的应用研究[D].杭州:中国计量大学, 2023.
[27] Sivakumar M, Roshni J, Ahmad S F, et al. Fused pyrido[3,4-D] pyrimidine moiety with phthalazinone ring accelerate dual inhibition of PARP1 and CDK4in triple-negative breast cancer:a hybrid design with computational investigation through molecular modeling and quantum mechanics[J]. Journal of Molecular Modeling, 2025, 31(7):181.
[28] Uawisetwathana U, Graham S F, Kamolsukyunyong W, et al. Quantitative 1H NMR metabolome profiling of Thai Jasmine rice(Oryza sativa)reveals primary metabolic response during brown planthopper infestation[J]. Metabolomics, 2015, 11:1640-1655.
[29] Liu Y Q, Wu H, Chen H, et al. A gene cluster encoding lectin receptor kinases confers broadspectrum and durable insect resistance in rice[J]. Nature Biotechnology, 2015, 33:301-305.
[30] Guo J, Wang H, Guan W, et al. A tripartite rheostat controls self-regulated host plant resistance to insects[J]. Nature, 2023, 618:799-807.
[31] Wang Y, Cao L M, Zhang Y X, et al. Map-based cloning and characterization of BPH29, a B3 domain-containing recessive gene conferring brown planthopper resistance in rice[J]. Journal of Experimental Botany, 2015, 66:6035-6045.
[32] Jin G, Qi J, Zu H, et al. Jasmonate-mediated gibberellin catabolism constrains growth during herbivore attack in rice[J]. Plant Cell, 2023, 35(10):3828-3844.
[33] He J, Liu Y, Yuan D, et al. An R2R3 MYB transcription factor confers brown planthopper resistance by regulating the phenylalanine ammonia-lyase pathway in rice[J]. Proceedings of the National Academy of Sciences of the United States of America, 2020, 117(1):271-277.
[34] Dai Z, Tan J, Zhou C, et al. The OsmiR396-OsGRF8-OsF3H-flavonoid pathway mediates resistance to the brown planthopper in rice(Oryza sativa)[J].Plant Biotechnology Journal, 2019, 17(8):1657-1669.
[35] Zhao Y, Huang J, Wang Z, et al. Allelic diversity in an NLR gene BPH9 enables rice to combat planthopper variation[J]. Proceedings of the National Academy of Sciences of the United States of America, 2016, 113:12850-12855.
[36] Senthil-Nathan S, Kalaivani K, Choi M Y, et al. Effects of jasmonic acid-induced resistance in rice on the plant brownhopper, Nilaparvata lugens Stål(Homoptera:Delphacidae)[J]. Pesticide Biochemistry&Physiology, 2009, 95(2):77-84.
[37] 陈宜明,戴阳朔,巩固,等.水稻抗虫次生化合物麦黄酮刺激对褐飞虱唾液腺转录组的影响[J].环境昆虫学报, 2025, 47(5):1354-1364.
[38] 凌冰,董红霞,张茂新,等.水稻麦黄酮对褐飞虱的抗性潜力[J].生态学报, 2007(4):1300-1307.
[39] Liu J, Du H, Ding X, et al. Mechanisms of callose deposition in rice regulated by exogenous abscisic acid and its involvement in rice resistance to Nilaparvata lugens Stål(Hemiptera:Delphacidae)[J]. Pest Management Science, 2017, 73(12):2559-2568.
[40] Wu D, Guo J, Zhang Q, et al. Necessity of rice resistance to planthoppers for OsEXO70H3 regulating SAMSL excretion and lignin deposition in cell walls[J]. New Phytologist, 2022, 234(3):1031-1046.
[41] Wong W S, Guo D, Wang X L, et al. Study of cis-cinnamic acid in Arabidopsis thaliana[J]. Plant Physiology and Biochemistry, 2005, 43(10/11):929-937.
[42] Alonso C, García I M, Zapata N, et al. Variability in the behavioural responses of three generalist herbivores to the most abundant coumarin in Daphne laureola leaves[J]. Entomologia experimentalis et applicata, 2009, 132(1):76-83.
[43] Cheng Y, Yang J, Li T, et al. Endosymbiotic fungal diversity and dynamics of the brown planthopper across developmental stages, tissues, and sexes revealed using circular consensus sequencing[J]. Insects, 2024, 15(2):87.
[44] Eleftherianos I, Atri J, Accetta J, et al. Endosymbiotic bacteria in insects:guardians of the immune system?[J]. Frontiers in physiology, 2013, 4:46.
[45] Qu L Y, Lou Y H, Fan H W, et al. Two endosymbiotic bacteria, Wolbachia and Arsenophonus, in the brown planthopper Nilaparvata lugens[J]. Symbiosis,2013, 61:47-53.
[46] Xu H, Song Z, Jun Y, et al. Changes in endosymbiotic bacteria of brown planthoppers during the process of adaptation to different resistant rice varieties[J]. Environmental Entomology, 2015, 44(3):582-587.
[47] Thorsson E, Jansson A, Vaga M, et al. Histochemical localisation of carbonic anhydrase in the digestive tract and salivary glands of the house cricket,Acheta domesticus[J]. Journal of Insects as Food and Feed, 2020, 6(2):191-198.
[48] Engineer C B, Ghassemian M, Anderson J C, et al. Corrigendum:Carbonic anhydrases, EPF2 and a novel protease mediate CO₂ control of stomatal development[J]. Nature, 2015, 513:246-250.