{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T13:16:45Z","timestamp":1787318205234,"version":"build-2736575974"},"reference-count":40,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2025,2,23]],"date-time":"2025-02-23T00:00:00Z","timestamp":1740268800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Key Research and Development Program of China","award":["2021YFD1400700"],"award-info":[{"award-number":["2021YFD1400700"]}]},{"name":"National Key Research and Development Program of China","award":["2022TSYCCX0084"],"award-info":[{"award-number":["2022TSYCCX0084"]}]},{"name":"Tian-Shan Talent Program","award":["2021YFD1400700"],"award-info":[{"award-number":["2021YFD1400700"]}]},{"name":"Tian-Shan Talent Program","award":["2022TSYCCX0084"],"award-info":[{"award-number":["2022TSYCCX0084"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Insects, as the most diverse and numerous group in the animal kingdom, are at least partly dependent on the reproduction process, which is strictly regulated by the \u2018classic\u2019 insect hormones: juvenile hormone (JH), and 20-hydroxyecdysone (20E). However, the regulatory mechanism governing the reproduction of JH and 20E in Spodoptera frugiperda remains unclear. In this study, ovarian development and ovulation in female S. frugiperda were assessed through dissection of the ovaries following treatment with JH analog (JHA) and 20E. Moreover, the expression patterns of the JH-signal and 20E-signal-related genes were determined by quantitative PCR (qPCR), and RNA interference (RNAi) was used to investigate the role of JH and 20E-induced genes. Ovarian development was observed by microdissection, and JH and 20E titers were determined by ELISA. Kr-h1, Vg, and USP expression were determined by qPCR. Dissection and qPCR results showed that JHA and 20E promoted ovarian development, egg maturation, and egg laying by upregulating Methoprene-Tolerant (Met) and Ecdysone Receptor (EcR)expression. Additionally, the RNAi results showed that the injection of dsMet and dsEcR markedly delayed ovarian development, inhibited egg maturation, and halted egg production. Knockdown of Met and EcR significantly reduced JH and 20E content and inhibited the transcription of Kr-h1 and USP. These results indicate that JH and 20E facilitate adult reproduction through the methoprene-tolerant gene and ecdysone receptor gene in female S. frugiperda.<\/jats:p>","DOI":"10.3390\/ijms26051914","type":"journal-article","created":{"date-parts":[[2025,2,24]],"date-time":"2025-02-24T06:47:17Z","timestamp":1740379637000},"page":"1914","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Juvenile Hormone and Ecdysteroids Facilitate the Adult Reproduction Through the Methoprene-Tolerant Gene and Ecdysone Receptor Gene in the Female Spodoptera frugiperda"],"prefix":"10.3390","volume":"26","author":[{"given":"Yan","family":"Zhang","sequence":"first","affiliation":[{"name":"State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China"},{"name":"State Key Laboratory of Resource Insects, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100193, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kui-Ting","family":"Ding","sequence":"additional","affiliation":[{"name":"State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6014-3383","authenticated-orcid":false,"given":"Nian-Wan","family":"Yang","sequence":"additional","affiliation":[{"name":"State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhi-Chuang","family":"Lv","sequence":"additional","affiliation":[{"name":"State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6866-440X","authenticated-orcid":false,"given":"Zhen-Ying","family":"Wang","sequence":"additional","affiliation":[{"name":"State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yong-Jun","family":"Zhang","sequence":"additional","affiliation":[{"name":"State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wan-Xue","family":"Liu","sequence":"additional","affiliation":[{"name":"State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0003-7759-0811","authenticated-orcid":false,"given":"Jian-Yang","family":"Guo","sequence":"additional","affiliation":[{"name":"State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,2,23]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1146\/annurev-ento-020117-043258","article-title":"Regulatory pathways controlling female insect reproduction","volume":"63","author":"Roy","year":"2018","journal-title":"Annu. Rev. Entomol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1111\/j.1365-2826.2004.01222.x","article-title":"Neuroendocrinological and molecular aspects of insect reproduction","volume":"16","author":"Simonet","year":"2004","journal-title":"J. Neuroendocrinol."},{"key":"ref_3","first-page":"967361","article-title":"Juvenile hormone biosynthesis in insects: What is new, what do we know, and what questions remain?","volume":"2014","author":"Noriega","year":"2014","journal-title":"Int. Sch. Res. Notices."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/j.cois.2018.07.010","article-title":"Juvenile hormone signaling in insect oogenesis","volume":"31","author":"Santos","year":"2019","journal-title":"Curr. Opin. Insect Sci."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1016\/S0065-2806(08)60043-0","article-title":"Structure and regulation of the corpus allatum","volume":"Volume 18","author":"Tobe","year":"1985","journal-title":"Advances in Insect Physiology"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1146\/annurev-ento-120811-153700","article-title":"The juvenile hormone signaling pathway in insect development","volume":"58","author":"Jindra","year":"2013","journal-title":"Annu. Rev. Entomol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1146\/annurev.ento.53.103106.093334","article-title":"Gonadal ecdysteroidogenesis in Arthropoda: Occurrence and regulation","volume":"54","author":"Brown","year":"2009","journal-title":"Annu. Rev. Entomol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1016\/0040-8166(93)90019-H","article-title":"Induction of choriogenesis by 20-hydroxyecdysone in the German cockroach","volume":"25","author":"Cassier","year":"1993","journal-title":"Tissue Cell"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Khalid, M.Z., Ahmad, S., Ngegba, P.M., and Zhong, G. (2021). Role of endocrine system in the regulation of female insect reproduction. Biology, 10.","DOI":"10.3390\/biology10070614"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Cruz, J., Maestro, O., Franch-Marro, X., and Mart\u00edn, D. (2022). Ecdysone signaling controls early embryogenesis in the short-germ hemimetabolous insect Blattella germanica. bioRxiv.","DOI":"10.1101\/2022.03.10.483750"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"e2109381118","DOI":"10.1073\/pnas.2109381118","article-title":"Epoxidation of juvenile hormone was a key innovation improving insect reproductive fitness","volume":"118","author":"Nouzova","year":"2021","journal-title":"Proc. Nat. Acad. Sci. USA"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"21128","DOI":"10.1073\/pnas.1116123109","article-title":"Ligand-binding properties of a juvenile hormone receptor, Methoprene-tolerant","volume":"108","author":"Charles","year":"2011","journal-title":"Proc. Nat. Acad. Sci. USA"},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Jindra, M., Uhlirova, M., Charles, J.P., Smykal, V., and Hill, R.J. (2015). Genetic evidence for function of the bHLH-PAS protein Gce\/Met as a juvenile hormone receptor. PLoS Genet., 11.","DOI":"10.1371\/journal.pgen.1005394"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1146\/annurev-ento-120220-102548","article-title":"Spodoptera frugiperda: Ecology, evolution, and management options of an invasive species","volume":"68","author":"Tay","year":"2023","journal-title":"Annu. Rev. Entomol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"664","DOI":"10.1016\/S2095-3119(19)62839-X","article-title":"Case study on the first immigration of fall armyworm, Spodoptera frugiperda invading into China","volume":"20","author":"Sun","year":"2021","journal-title":"J. Integr. Agr."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1007\/s13238-020-00795-7","article-title":"Genomic and transcriptomic analysis unveils population evolution and development of pesticide resistance in fall armyworm Spodoptera frugiperda","volume":"13","author":"Gui","year":"2022","journal-title":"Protein Cell"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"407","DOI":"10.1146\/annurev.en.41.010196.002203","article-title":"The role of nourishment in oogenesis","volume":"41","author":"Wheeler","year":"1996","journal-title":"Annu. Rev. Entomol."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Han, S., Wang, D., Song, P., Zhang, S., and He, Y. (2022). Molecular characterization of vitellogenin and its receptor in Spodoptera frugiperda (JE Smith, 1797), and Their Function in Reproduction of Female. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms231911972"},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Chen, X., and Palli, S.R. (2022). Identification of species-specific juvenile hormone response elements in the fall armyworm, Spodoptera frugiperda. Insect Biochem. Mol. Biol., 151.","DOI":"10.1016\/j.ibmb.2022.103860"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1016\/j.cois.2015.09.006","article-title":"Juvenile hormone and ecdysteroids as major regulators of brain and behavior in bees","volume":"12","author":"Pandey","year":"2015","journal-title":"Curr. Opin. Insect Sci."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"600","DOI":"10.1111\/1744-7917.12614","article-title":"Juvenile hormone signaling\u2014A mini review","volume":"26","author":"Li","year":"2019","journal-title":"Insect Sci."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1023","DOI":"10.1007\/s10340-022-01476-6","article-title":"Reproductive interference and satyrisation: Mechanisms, outcomes and potential use for insect control","volume":"95","author":"Mitchell","year":"2022","journal-title":"J. Pest Sci."},{"key":"ref_23","unstructured":"Liu, N., Ling, X., Wang, W., and Chen, H. (2022). Regulation pattern of juvenile. Genetic Diversity and Metamorphosis of White Wax Scale Insects, Cambridge Scholars Publishing."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1016\/j.ibmb.2016.05.004","article-title":"Juvenile hormone facilitates the antagonism between adult reproduction and diapause through the methoprene-tolerant gene in the female Colaphellus bowringi","volume":"74","author":"Liu","year":"2016","journal-title":"Insect Biochem. Mol. Biol."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Czosnek, H., and Ghanim, M. (2016). Hormonal regulation of development and reproduction. Management of Insect Pests to Agriculture, Springer.","DOI":"10.1007\/978-3-319-24049-7"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1016\/0012-1606(87)90150-3","article-title":"Involvement of ecdysone in the control of meiotic reinitiation in oocytes of Locusta migratoria (Insecta, Orthoptera)","volume":"121","author":"Lanot","year":"1987","journal-title":"Dev. Biol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"e2202932119","DOI":"10.1073\/pnas.2202932119","article-title":"Essential functions of mosquito ecdysone importers in development and reproduction","volume":"119","author":"Hun","year":"2022","journal-title":"Proc. Nat. Acad. Sci. USA"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Wang, Y., Buer, B., Goodman, C.L., Kang, D., Reall, T., Dohn, S., Ringbauer, J., Li, Y., Geibel, S., and Stanley, D. (2024). Indomethacin and 20-hydroxyecdysone influence protein expression in a Spodoptera frugiperda nervous system cell line. Arch. Insect Biochem. Physiol., 115.","DOI":"10.1002\/arch.22089"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Liu, P.-C., Wang, J.-X., Song, Q.-S., and Zhao, X.-F. (2011). The participation of calponin in the cross talk between 20-hydroxyecdysone and juvenile hormone signaling pathways by phosphorylation variation. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0019776"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"2712","DOI":"10.1242\/jeb.014878","article-title":"Hormonal regulation of the humoral innate immune response in Drosophila melanogaster","volume":"211","author":"Flatt","year":"2008","journal-title":"J. Exp. Biol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"492","DOI":"10.1111\/imb.12389","article-title":"Dissecting the role of Kr\u00fcppel homolog 1 in the metamorphosis and female reproduction of the cotton bollworm, Helicoverpa armigera","volume":"27","author":"Zhang","year":"2018","journal-title":"Insect Mol. Biol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/j.jinsphys.2015.04.006","article-title":"RXR\/USP and EcR are critical for the regulation of reproduction and the control of JH biosynthesis in Diploptera punctata","volume":"80","author":"Hult","year":"2015","journal-title":"J. Insect Physiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2369","DOI":"10.1093\/jee\/toz155","article-title":"Molecular characterization of primary juvenile hormone responders Methoprene-tolerant (Met) and Kr\u00fcppel homolog 1 (Kr-h1) in Grapholita molesta (Lepidoptera: Tortricidae) with clarification of their roles in metamorphosis and reproduction","volume":"112","author":"Zhang","year":"2019","journal-title":"J. Econ. Entomol."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Lenaerts, C., Marchal, E., Peeters, P., and Vanden Broeck, J. (2019). The ecdysone receptor complex is essential for the reproductive success in the female desert locust, Schistocerca gregaria. Sci. Rep., 9.","DOI":"10.1038\/s41598-018-36763-9"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Choi, D.Y., Mo, H.h., and Park, Y. (2024). Different development and fecundity between Spodoptera frugiperda USA and China populations, influenced by ecdysone-related genes. Arch. Insect Biochem. Physiol., 115.","DOI":"10.1002\/arch.22074"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Guo, S., Tian, Z., Wu, Q.-W., King-Jones, K., Liu, W., Zhu, F., and Wang, X.-P. (2021). Steroid hormone ecdysone deficiency stimulates preparation for photoperiodic reproductive diapause. PLoS Genet., 17.","DOI":"10.1371\/journal.pgen.1009352"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Kamruzzaman, A., Mikani, A., Mohamed, A.A., Elgendy, A.M., and Takeda, M. (2020). Crosstalk among indoleamines, neuropeptides and JH\/20E in regulation of reproduction in the American cockroach, Periplaneta americana. Insects, 11.","DOI":"10.3390\/insects11030155"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"2471","DOI":"10.1016\/S2095-3119(20)63298-1","article-title":"Stability evaluation of reference genes for real-time quantitative PCR normalization in Spodoptera frugiperda (Lepidoptera: Noctuidae)","volume":"20","author":"Shu","year":"2021","journal-title":"J. Integr. Agr."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and the 2\u2212\u0394\u0394CT method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1002\/ps.7212","article-title":"Temperature and metal ions regulate larval diapause termination via the 20-hydroxyecdysone and juvenile hormone pathways in Monochamus alternatus","volume":"79","author":"Yang","year":"2023","journal-title":"Pest Manag. Sci."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/26\/5\/1914\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T16:40:47Z","timestamp":1760028047000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/26\/5\/1914"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,2,23]]},"references-count":40,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2025,3]]}},"alternative-id":["ijms26051914"],"URL":"https:\/\/doi.org\/10.3390\/ijms26051914","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,2,23]]}}}