{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T17:16:28Z","timestamp":1788455788967,"version":"build-2803163510"},"reference-count":46,"publisher":"American Chemical Society (ACS)","issue":"34","license":[{"start":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T00:00:00Z","timestamp":1787270400000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-029"},{"start":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T00:00:00Z","timestamp":1787270400000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-037"},{"start":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T00:00:00Z","timestamp":1787270400000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-045"}],"funder":[{"DOI":"10.13039\/100010097","name":"China Association for Science and Technology","doi-asserted-by":"publisher","award":["2023QNRC001"],"award-info":[{"award-number":["2023QNRC001"]}],"id":[{"id":"10.13039\/100010097","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32120103009"],"award-info":[{"award-number":["32120103009"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32372548"],"award-info":[{"award-number":["32372548"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100006407","name":"Natural Science Foundation of Henan Province","doi-asserted-by":"publisher","award":["252300421146"],"award-info":[{"award-number":["252300421146"]}],"id":[{"id":"10.13039\/501100006407","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100006407","name":"Natural Science Foundation of Henan Province","doi-asserted-by":"publisher","award":["252300423086"],"award-info":[{"award-number":["252300423086"]}],"id":[{"id":"10.13039\/501100006407","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["2024YFD1401000"],"award-info":[{"award-number":["2024YFD1401000"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/na","name":"Project of Science and Technology Plan of Henan Province","doi-asserted-by":"publisher","award":["252102110210"],"award-info":[{"award-number":["252102110210"]}],"id":[{"id":"10.13039\/na","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2026,9,2]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Insect herbivores rely on glutathione S-transferases (GST) to cope with host-derived secondary metabolites, yet the specific role of individual GST isoforms in mediating host adaptation remains poorly understood. Here, we characterized the sigma-class GST gene NlGSTs3 and its role in host plant adaptation of the brown planthopper Nilaparvata lugens. NlGSTs3 was predominantly expressed in the fat body and testes. RNAi-mediated knockdown of NlGSTs3 significantly reduced survival and feeding performance on rice plants and specifically increased susceptibility to ferulic acid and resorcinol. Molecular docking predicted favorable interactions between NlGSTs3 and these two compounds, which was further supported by in vitro catalytic assays showing recombinant NlGSTs3 mediates the depletion of ferulic acid and resorcinol. This work demonstrates that NlGSTs3 contributes to the adaptation of N. lugens to rice chemical defenses through the substrate-specific metabolism of ferulic acid and resorcinol, suggesting that NlGSTs3 may be a promising target for RNAi-mediated BPH management.<\/jats:p>","DOI":"10.1021\/acs.jafc.6c05863","type":"journal-article","created":{"date-parts":[[2026,8,22]],"date-time":"2026-08-22T02:03:59Z","timestamp":1787364239000},"page":"27002-27012","source":"Crossref","is-referenced-by-count":0,"title":["<i>NlGSTs3<\/i>\n                    Facilitates Adaptation of\n                    <i>Nilaparvata lugens<\/i>\n                    to Rice by Metabolizing Ferulic\nAcid and Resorcinol"],"prefix":"10.1021","volume":"74","author":[{"given":"Yimeng","family":"Li","sequence":"first","affiliation":[{"name":"Henan University , , ,","place":["Kaifeng, China, 475004"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1804-7731","authenticated-orcid":true,"given":"Qingsong","family":"Liu","sequence":"additional","affiliation":[{"name":"Henan University , , ,","place":["Kaifeng, China, 475004"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qiuyu","family":"Tian","sequence":"additional","affiliation":[{"name":"Henan University , , ,","place":["Kaifeng, China, 475004"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jie","family":"Li","sequence":"additional","affiliation":[{"name":"Henan University , , ,","place":["Kaifeng, China, 475004"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yu","family":"Xue","sequence":"additional","affiliation":[{"name":"Henan University , , ,","place":["Kaifeng, China, 475004"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yumeng","family":"Zhang","sequence":"additional","affiliation":[{"name":"Henan University , , ,","place":["Kaifeng, China, 475004"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shengli","family":"Jing","sequence":"additional","affiliation":[{"name":"Xinyang Normal University , , ,","place":["Xinyang, China, 464000"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yunhe","family":"Li","sequence":"additional","affiliation":[{"name":"Henan University , , ,","place":["Kaifeng, China, 475004"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2026,8,21]]},"reference":[{"issue":"2","key":"2026090311503425800_cit1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2302251120","article-title":"Tissue-specific\nplant toxins and adaptation in a specialist\nroot herbivore","volume":"120","author":"Agrawal","year":"2023","journal-title":"Proc. Natl. Acad. Sci. U. S.\nA."},{"issue":"9","key":"2026090311503425800_cit2","doi-asserted-by":"publisher","first-page":"2441","DOI":"10.1093\/molbev\/msu201","article-title":"Evolution in an ancient\ndetoxification pathway is coupled with a transition to herbivory in\nthe Drosophilidae","volume":"31","author":"Gloss","year":"2014","journal-title":"Mol. Biol. Evol."},{"key":"2026090311503425800_cit3","doi-asserted-by":"publisher","first-page":"431","DOI":"10.1146\/annurev-arplant-042110-103854","article-title":"Plant defense against herbivores: Chemical aspects","volume":"63","author":"Mithofer","year":"2012","journal-title":"Annu. Rev. Plant Biol."},{"key":"2026090311503425800_cit4","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1146\/annurev.arplant.59.032607.092825","article-title":"Plant immunity to insect\nherbivores","volume":"59","author":"Howe","year":"2008","journal-title":"Annu. Rev. Plant Biol."},{"key":"2026090311503425800_cit5","doi-asserted-by":"publisher","first-page":"549","DOI":"10.1146\/annurev-arplant-042110-103814","article-title":"Convergent\nevolution in plant specialized metabolism","volume":"62","author":"Pichersky","year":"2011","journal-title":"Annu.\nRev. Plant Biol."},{"issue":"1","key":"2026090311503425800_cit6","doi-asserted-by":"publisher","first-page":"6772","DOI":"10.1038\/s41467-021-27021-0","article-title":"Cooperative herbivory\nbetween two important pests of rice","volume":"12","author":"Liu","year":"2021","journal-title":"Nat. Commun."},{"key":"2026090311503425800_cit7","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1016\/j.cois.2015.02.004","article-title":"Molecular mechanisms\nof insect adaptation to plant secondary compounds","volume":"8","author":"Heidel-Fischer","year":"2015","journal-title":"Curr. Opin. Insect Sci."},{"key":"2026090311503425800_cit8","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1146\/annurev-ento-062821-062319","article-title":"Sequestration of plant defense compounds\nby insects:\nFrom mechanisms to insect-plant coevolution","volume":"67","author":"Beran","year":"2022","journal-title":"Annu. Rev. Entomol."},{"issue":"6","key":"2026090311503425800_cit9","doi-asserted-by":"publisher","first-page":"298","DOI":"10.1016\/j.tree.2007.02.010","article-title":"The evolutionary\necology of insect\nresistance to plant chemicals","volume":"22","author":"Despres","year":"2007","journal-title":"Trends Ecol.\nEvol."},{"issue":"15","key":"2026090311503425800_cit10","doi-asserted-by":"publisher","first-page":"5713","DOI":"10.7150\/ijbs.77141","article-title":"Functional and structural diversity\nof insect glutathione S-transferases in xenobiotic adaptation","volume":"18","author":"Koirala BK","year":"2022","journal-title":"Int. J. Biol. 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Food Chem."},{"issue":"1","key":"2026090311503425800_cit17","doi-asserted-by":"publisher","first-page":"931","DOI":"10.1038\/s42003-025-08346-8","article-title":"Multiple glutathione-S-transferases\ndetoxify diverse\nglucosinolate-based defenses of Brassicales plants in a generalist\nlepidopteran herbivore (Spodoptera littoralis)","volume":"8","author":"Sun","year":"2025","journal-title":"Commun. Biol."},{"issue":"11","key":"2026090311503425800_cit18","doi-asserted-by":"publisher","first-page":"867","DOI":"10.3390\/insects15110867","article-title":"Identification\nand functional analysis of three NlCstF genes in Nilaparvata lugens","volume":"15","author":"Jing","year":"2024","journal-title":"Insects"},{"key":"2026090311503425800_cit19","doi-asserted-by":"publisher","first-page":"125","DOI":"10.1146\/annurev.ento.49.061802.123310","article-title":"Mechanisms\nof hopperburn: An overview\nof insect taxonomy, behavior, and physiology","volume":"50","author":"Backus","year":"2005","journal-title":"Annu. Rev. Entomol."},{"issue":"12","key":"2026090311503425800_cit20","doi-asserted-by":"publisher","first-page":"3093","DOI":"10.1111\/jipb.70035","article-title":"Metabolome\nstudy of rice population and resistance\nto brown planthopper","volume":"67","author":"Li","year":"2025","journal-title":"J. Integr. Plant Biol."},{"key":"2026090311503425800_cit21","doi-asserted-by":"publisher","first-page":"14","DOI":"10.1016\/j.cois.2020.11.005","article-title":"Genetic and\nmolecular understanding of host rice resistance\nand Nilaparvata lugens adaptation","volume":"45","author":"Zheng","year":"2021","journal-title":"Curr. Opin. Insect Sci."},{"issue":"9","key":"2026090311503425800_cit22","doi-asserted-by":"publisher","first-page":"652","DOI":"10.3390\/insects15090652","article-title":"Virulence\nadaptation by rice planthoppers and leafhoppers to resistance genes\nand loci: A review","volume":"15","author":"Horgan","year":"2024","journal-title":"Insects"},{"issue":"6","key":"2026090311503425800_cit23","doi-asserted-by":"publisher","first-page":"1428","DOI":"10.3390\/agronomy15061428","article-title":"Metabolomic profiling\nof pyramiding rice and its implications for brown planthopper resistance","volume":"15","author":"Hu","year":"2025","journal-title":"Agronomy"},{"issue":"12","key":"2026090311503425800_cit24","doi-asserted-by":"publisher","first-page":"8333","DOI":"10.1002\/ps.70134","article-title":"Isovitexin and schaftoside\nfrom rice\nplants have antifeedant activity on brown planthoppers","volume":"81","author":"Duan","year":"2025","journal-title":"Pest Manage. Sci."},{"key":"2026090311503425800_cit25","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1016\/j.jinsphys.2018.10.001","article-title":"Metabolic\nresponses of brown planthoppers\nto IR56 resistant rice cultivar containing multiple resistance genes","volume":"113","author":"Yue","year":"2019","journal-title":"J. Insect Physiol."},{"key":"2026090311503425800_cit26","doi-asserted-by":"publisher","first-page":"102577","DOI":"10.1016\/j.pbi.2024.102577","article-title":"Disarming\nthe defenses: Insect detoxification of plant\ndefense-related specialized metabolites","volume":"81","author":"Kshatriya","year":"2024","journal-title":"Curr.\nOpin. Plant Biol."},{"issue":"1","key":"2026090311503425800_cit27","doi-asserted-by":"publisher","first-page":"682","DOI":"10.1186\/s12864-019-6049-7","article-title":"Combining next-generation sequencing and single-molecule sequencing\nto explore brown planthopper responses to contrasting genotypes of\njaponica rice","volume":"20","author":"Zhang","year":"2019","journal-title":"BMC Genomics"},{"key":"2026090311503425800_cit28","doi-asserted-by":"publisher","first-page":"972","DOI":"10.3389\/fphys.2017.00972","article-title":"Functional\nstudy of cytochrome P450\nenzymes from the brown planthopper (Nilaparvata lugens St\u00e5l) to analyze its adaptation to BPH-resistant rice","volume":"8","author":"Peng","year":"2017","journal-title":"Front. Physiol."},{"key":"2026090311503425800_cit29","doi-asserted-by":"publisher","first-page":"1055","DOI":"10.3390\/insects12121055","article-title":"The key\nglutathione S-transferase family genes involved in the detoxification\nof rice gramine in brown planthopper Nilaparvata lugens","volume":"12","author":"Yang","year":"2021","journal-title":"Insects"},{"issue":"7","key":"2026090311503425800_cit30","doi-asserted-by":"publisher","first-page":"693","DOI":"10.1007\/s10886-017-0859-3","article-title":"Interaction of ferulic acid with glutathione S-transferase\nand carboxylesterase genes in the brown planthopper, Nilaparvata lugens","volume":"43","author":"Yang","year":"2017","journal-title":"J. Chem. Ecol."},{"issue":"12","key":"2026090311503425800_cit31","doi-asserted-by":"publisher","first-page":"992","DOI":"10.3390\/insects15120992","article-title":"Comparative transcriptome analysis highlights\nthe role of NlABCG14 in the honeydew production of\nvirulent brown planthoppers\n(Nilaparvata lugens St\u00e5l) to resistant rice\nvariety","volume":"15","author":"Jing","year":"2024","journal-title":"Insects"},{"key":"2026090311503425800_cit32","doi-asserted-by":"publisher","first-page":"1366515","DOI":"10.3389\/fpls.2024.1366515","article-title":"Combined miRNA and mRNA sequencing reveals\nthe defensive strategies\nof resistant YHY15 rice against differentially virulent brown planthoppers","volume":"15","author":"Yu","year":"2024","journal-title":"Front. Plant Sci."},{"issue":"10","key":"2026090311503425800_cit33","doi-asserted-by":"publisher","first-page":"2731","DOI":"10.1093\/molbev\/msr121","article-title":"MEGA5: Molecular evolutionary\ngenetics analysis using maximum likelihood,\nevolutionary distance, and maximum parsimony methods","volume":"28","author":"Tamura","year":"2011","journal-title":"Mol. Biol. Evol."},{"issue":"4","key":"2026090311503425800_cit34","doi-asserted-by":"publisher","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis\nof relative gene expression data using real-time\nquantitative PCR and the 2\u2013\u0394\u0394CT method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"2026090311503425800_cit35","doi-asserted-by":"publisher","first-page":"104207","DOI":"10.1016\/j.ibmb.2024.104207","article-title":"Male-specific lethal-3 gene is critical for survival and fecundity in rice\nbrown planthopper, Nilaparvata lugens","volume":"175","author":"Jing","year":"2024","journal-title":"Insect Biochem. Mol. Biol."},{"key":"2026090311503425800_cit36","doi-asserted-by":"publisher","first-page":"104346","DOI":"10.1016\/j.ibmb.2025.104346","article-title":"NlAgo3 and NlBiwi are essential\nfor piRNAs biogenesis and female reproduction in Nilaparvata lugens","volume":"182","author":"Jing","year":"2025","journal-title":"Insect Biochem. Mol. Biol."},{"issue":"2","key":"2026090311503425800_cit37","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0056604","article-title":"Genomic\ninsights into the glutathione S-transferase gene family of two rice\nplanthoppers, Nilaparvata lugens (St\u00e5l) and Sogatella furcifera (Horva\u0301th) (Hemiptera: Delphacidae)","volume":"8","author":"Zhou","year":"2013","journal-title":"PLoS One"},{"issue":"12","key":"2026090311503425800_cit38","doi-asserted-by":"publisher","first-page":"4828","DOI":"10.1002\/ps.7681","article-title":"The brown planthopper NlDHRS11 is\ninvolved in the detoxification of rice secondary compounds","volume":"79","author":"Yang","year":"2023","journal-title":"Pest Manage. Sci."},{"issue":"1","key":"2026090311503425800_cit39","doi-asserted-by":"publisher","first-page":"20","DOI":"10.1673\/031.007.2001","article-title":"Tissue\nand life stage specificity\nof glutathione S-transferase expression in the Hessian fly, Mayetiola destructor: Implications for resistance to host\nallelochemicals","volume":"7","author":"Mittapalli","year":"2007","journal-title":"J. Insect Sci."},{"issue":"2","key":"2026090311503425800_cit40","doi-asserted-by":"publisher","first-page":"885","DOI":"10.1002\/ps.7824","article-title":"Characterization of three glutathione\nS-transferases potentially associated with adaptation of the wheat\nblossom midge Sitodiplosis mosellana to host plant\ndefense","volume":"80","author":"Zhang","year":"2024","journal-title":"Pest Manage. Sci."},{"key":"2026090311503425800_cit41","doi-asserted-by":"publisher","first-page":"104860","DOI":"10.1016\/j.pestbp.2021.104860","article-title":"Functional\nidentification and characterization of GST genes in the Asian gypsy\nmoth in response to poplar secondary metabolites","volume":"176","author":"Ma","year":"2021","journal-title":"Pestic. Biochem. Physiol."},{"issue":"9","key":"2026090311503425800_cit42","doi-asserted-by":"publisher","first-page":"2939","DOI":"10.1073\/pnas.0308691101","article-title":"Structural and functional\ndivergence of insect CYP6B proteins: From specialist to generalist\ncytochrome P450","volume":"101","author":"Li","year":"2004","journal-title":"Proc. Natl. Acad. Sci. U. S.\nA."},{"issue":"11","key":"2026090311503425800_cit43","doi-asserted-by":"publisher","first-page":"1307","DOI":"10.1038\/nbt1352","article-title":"Silencing a cotton\nbollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval\ntolerance of gossypol","volume":"25","author":"Mao","year":"2007","journal-title":"Nat. Biotechnol."},{"key":"2026090311503425800_cit44","doi-asserted-by":"publisher","first-page":"100061","DOI":"10.1016\/j.ncrops.2024.100061","article-title":"The development and prospects of\ninsect-resistant crops expressing double-strand RNAs","volume":"2","author":"Zhang","year":"2025","journal-title":"New Crops"},{"key":"2026090311503425800_cit45","doi-asserted-by":"publisher","first-page":"10","DOI":"10.1016\/j.ibmb.2018.05.008","article-title":"Targeting detoxification genes by\nphloem-mediated RNAi: A new approach for controlling phloem-feeding\ninsect pests","volume":"100","author":"Eakteiman","year":"2018","journal-title":"Insect Biochem. Mol. Biol."},{"issue":"1","key":"2026090311503425800_cit46","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1127\/entomologia\/2023\/2207","article-title":"Target genes for RNAi\nin pest control: A comprehensive overview","volume":"44","author":"Lu","year":"2024","journal-title":"Entomol.\nGen."}],"container-title":["Journal of Agricultural and Food Chemistry"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pubs.acs.org\/doi\/pdf\/10.1021\/acs.jafc.6c05863","content-type":"application\/pdf","content-version":"vor","intended-application":"unspecified"},{"URL":"https:\/\/pubs.acs.org\/jafcau\/article-pdf\/74\/34\/27002\/66954582\/acs.jafc.6c05863.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/pubs.acs.org\/jafcau\/article-pdf\/74\/34\/27002\/66954582\/acs.jafc.6c05863.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T16:24:38Z","timestamp":1788452678000},"score":1,"resource":{"primary":{"URL":"https:\/\/pubs.acs.org\/jafcau\/article\/74\/34\/27002\/5283363\/NlGSTs3-Facilitates-Adaptation-of-Nilaparvata"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,8,21]]},"references-count":46,"journal-issue":{"issue":"34","published-online":{"date-parts":[[2026,8,21]]},"published-print":{"date-parts":[[2026,9,2]]}},"URL":"https:\/\/doi.org\/10.1021\/acs.jafc.6c05863","relation":{},"ISSN":["0021-8561","1520-5118"],"issn-type":[{"value":"0021-8561","type":"print"},{"value":"1520-5118","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,8,21]]}}}