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Identifying critical genes or proteins regulating fertility is essential for sustainable pest control and a research hotspot in insect physiology. MicroRNAs (miRNAs) are short RNAs that do not directly participate in protein translation, but instead function in post\u2010transcriptional regulation of gene expression involved in male fertility.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>We found that miR\u2010927\u20105p is highly expressed in the testes and investigated its function in spermatogenesis in <jats:italic>Z.\u2009cucurbitae<\/jats:italic>. Fluorescence <jats:italic>in situ<\/jats:italic> hybridization (FISH) showed miR\u2010927\u20105p in the transformation and maturation region of the testis, and overexpression of miR\u2010927\u20105p reduced the number of sperms by 53%. In continuation, we predicted 12 target genes of miR\u2010927\u20105p using bioinformatics combined with transcriptome sequencing data, and found that miR\u2010927\u20105p targets the new gene <jats:italic>Stalky<\/jats:italic> in insects, which was validated by quantitative real\u2010time\u00a0PCR, RNA pull\u2010down and dual luciferase reporter assays. FISH also confirmed the co\u2010localization of miR\u2010927\u20105p and the transcript <jats:italic>Stalky_1<\/jats:italic> in the testis. Moreover, silencing of <jats:italic>Stalky_1<\/jats:italic> by RNA interference reduced the number of sperms by 32% and reduced sperm viability by 39% in physiologically mature male adults. Meanwhile, the silencing of <jats:italic>Stalky_1<\/jats:italic> also resulted in low hatchability.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusion<\/jats:title><jats:p>Our work not only presents a new, so far unreported mechanism regulating spermatogenesis by miR\u2010927\u20105p targeting a new unknown target, <jats:italic>Stalky<\/jats:italic>, which is providing new knowledge on the regulatory network of insect spermatogenesis, but also lays a foundation for the development of SIT against important tephritid fly pests. \u00a9 2024 Society of Chemical Industry.<\/jats:p><\/jats:sec>","DOI":"10.1002\/ps.8044","type":"journal-article","created":{"date-parts":[[2024,2,26]],"date-time":"2024-02-26T07:45:30Z","timestamp":1708933530000},"page":"3412-3422","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Overexpression of <scp>miR<\/scp>\u2010927\u20105p suppresses <i>stalky<\/i> expression and negatively reduces the spermatid production in <i>Zeugodacus cucurbitae<\/i>"],"prefix":"10.1002","volume":"80","author":[{"given":"Hong\u2010Liang","family":"Han","sequence":"first","affiliation":[{"name":"Chongqing Key Laboratory of Entomology and Pest Control Engineering, College of Plant Protection Southwest University  Chongqing China"},{"name":"International Joint Laboratory of China\u2010Belgium on Sustainable Crop Pest Control, Academy of Agricultural Sciences Southwest University  Chongqing China"},{"name":"Key Laboratory of Agricultural Biosafety and Green Production of Upper Yangtze River (Ministry of Education) Southwest University  Chongqing China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jing\u2010Ming","family":"Li","sequence":"additional","affiliation":[{"name":"Chongqing Key Laboratory of Entomology and Pest Control Engineering, College of Plant Protection Southwest University  Chongqing China"},{"name":"International Joint Laboratory of China\u2010Belgium on 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