{"title":"Masculinizer is not post-transcriptionally regulated by female-specific piRNAs during sex determination in the Asian corn borer, Ostrinia furnacalis","authors":"Takahiro Fukui , Keisuke Shoji , Takashi Kiuchi , Yutaka Suzuki , Susumu Katsuma","doi":"10.1016/j.ibmb.2023.103946","DOIUrl":null,"url":null,"abstract":"<div><p>Lepidopteran insects are heterogametic in females, although most insect species are heterogametic in males. In a lepidopteran model species, the silkworm <em>Bombyx mori</em> (Bombycoidea), the uppermost sex determinant <em>Feminizer</em> (<em>Fem</em>) has been identified on the female-specific W chromosome. <em>Fem</em> is a precursor of PIWI-interacting small RNA (piRNA). <em>Fem</em> piRNA forms a complex with Siwi, one of the two <em>B</em>. <em>mori</em> PIWI-clade Argonaute proteins. In female embryos, <em>Fem</em> piRNA–Siwi complex cleaves the mRNA of the male-determining gene <em>Masculinizer</em> (<em>Masc</em>), directing the female-determining pathway. In male embryos, <em>Masc</em> activates the male-determining pathway in the absence of <em>Fem</em> piRNA. Recently, W chromosome-derived piRNAs complementary to <em>Masc</em> mRNA have also been identified in the diamondback moth <em>Plutella xylostella</em> (Yponomeutoidea), indicating the convergent evolution of piRNA-dependent sex determination in Lepidoptera. Here, we show that this is not the case in the Asian corn borer, <em>Ostrinia furnacalis</em> (Pyraloidea). Although our previous studies demonstrated that <em>O</em>. <em>furnacalis Masc</em> (<em>OfMasc</em>) has a masculinizing function in the embryonic stage, the expression level of <em>OfMasc</em> was indistinguishable between the sexes at the timing of sex determination. Deep sequencing analysis identified no female-specific small RNAs mapped onto <em>OfMasc</em> mRNA. Embryonic knockdown of two <em>PIWI</em> genes did not affect the expression level of <em>OfMasc</em> in either sex. These results demonstrated that piRNA-dependent reduction of <em>Masc</em> mRNA in female embryos is not a common strategy of sex determination, which suggests the possibility of divergent evolution of sex determinants across the order Lepidoptera.</p></div>","PeriodicalId":330,"journal":{"name":"Insect Biochemistry and Molecular Biology","volume":null,"pages":null},"PeriodicalIF":3.2000,"publicationDate":"2023-05-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"2","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Insect Biochemistry and Molecular Biology","FirstCategoryId":"97","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0965174823000401","RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 2
Abstract
Lepidopteran insects are heterogametic in females, although most insect species are heterogametic in males. In a lepidopteran model species, the silkworm Bombyx mori (Bombycoidea), the uppermost sex determinant Feminizer (Fem) has been identified on the female-specific W chromosome. Fem is a precursor of PIWI-interacting small RNA (piRNA). Fem piRNA forms a complex with Siwi, one of the two B. mori PIWI-clade Argonaute proteins. In female embryos, Fem piRNA–Siwi complex cleaves the mRNA of the male-determining gene Masculinizer (Masc), directing the female-determining pathway. In male embryos, Masc activates the male-determining pathway in the absence of Fem piRNA. Recently, W chromosome-derived piRNAs complementary to Masc mRNA have also been identified in the diamondback moth Plutella xylostella (Yponomeutoidea), indicating the convergent evolution of piRNA-dependent sex determination in Lepidoptera. Here, we show that this is not the case in the Asian corn borer, Ostrinia furnacalis (Pyraloidea). Although our previous studies demonstrated that O. furnacalis Masc (OfMasc) has a masculinizing function in the embryonic stage, the expression level of OfMasc was indistinguishable between the sexes at the timing of sex determination. Deep sequencing analysis identified no female-specific small RNAs mapped onto OfMasc mRNA. Embryonic knockdown of two PIWI genes did not affect the expression level of OfMasc in either sex. These results demonstrated that piRNA-dependent reduction of Masc mRNA in female embryos is not a common strategy of sex determination, which suggests the possibility of divergent evolution of sex determinants across the order Lepidoptera.
期刊介绍:
This international journal publishes original contributions and mini-reviews in the fields of insect biochemistry and insect molecular biology. Main areas of interest are neurochemistry, hormone and pheromone biochemistry, enzymes and metabolism, hormone action and gene regulation, gene characterization and structure, pharmacology, immunology and cell and tissue culture. Papers on the biochemistry and molecular biology of other groups of arthropods are published if of general interest to the readership. Technique papers will be considered for publication if they significantly advance the field of insect biochemistry and molecular biology in the opinion of the Editors and Editorial Board.