{"title":"变形基因在两个互补的性别决定位点下调节蚂蚁的雌性化","authors":"Misato Okamoto Miyakawa, Hitoshi Miyakawa","doi":"10.1016/j.ibmb.2023.103938","DOIUrl":null,"url":null,"abstract":"<div><p>Organisms that reproduce sexually have evolved well-organized mechanisms to determine two sexes. Some hymenopterans (such as ants, bees, and wasps) have a complementary sex-determination system in which heterozygosity at one CSD locus induces female development, whereas hemi- or homozygosity at the locus induces male development. This system can generate a high cost of inbreeding, as individuals that are homozygous at the locus become sterile, diploid males. On the other hand, some hymenopterans have evolved a multi-locus, complementary, sex-determination system in which heterozygosity in at least one CSD locus induces female development. This system effectively reduces the proportion of sterile diploid males; however, how these multiple\u2028primary signals based on CSD pass through a molecular cascade to regulate downstream genes has remained unclear. To clarify this matter, we used a backcross to investigate the molecular cascade in the ant, <em>Vollenhovia emeryi</em>, with two CSD loci. Here we show by gene disruption that <em>transformer</em> (<em>tra</em>) is necessary for proper feminization. Expression analysis of <em>tra</em> and <em>doublesex</em> (<em>dsx</em>) showed that heterozygosity in at least one of the two CSD loci is sufficient to promote female sex determination. Analysis of overexpression suggested that female-type Tra protein promotes splicing of <em>tra</em> pre-mRNA to female isoform by a positive-regulatory-feedback loop. Our data also showed that <em>tra</em> affects splicing of <em>dsx</em>. We conclude that two-loci sex determination system in <em>V. emeryi</em> evolved based on <em>tra</em>-<em>dsx</em> splicing cascade that is well conserved in other insect species. Finally, we suggest a cascade model to arrive at a binary determination of sex under multiple primary signals.</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":"0","resultStr":"{\"title\":\"Transformer gene regulates feminization under two complementary sex determination loci in the ant, Vollenhovia emeryi\",\"authors\":\"Misato Okamoto Miyakawa, Hitoshi Miyakawa\",\"doi\":\"10.1016/j.ibmb.2023.103938\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<div><p>Organisms that reproduce sexually have evolved well-organized mechanisms to determine two sexes. Some hymenopterans (such as ants, bees, and wasps) have a complementary sex-determination system in which heterozygosity at one CSD locus induces female development, whereas hemi- or homozygosity at the locus induces male development. This system can generate a high cost of inbreeding, as individuals that are homozygous at the locus become sterile, diploid males. On the other hand, some hymenopterans have evolved a multi-locus, complementary, sex-determination system in which heterozygosity in at least one CSD locus induces female development. This system effectively reduces the proportion of sterile diploid males; however, how these multiple\\u2028primary signals based on CSD pass through a molecular cascade to regulate downstream genes has remained unclear. To clarify this matter, we used a backcross to investigate the molecular cascade in the ant, <em>Vollenhovia emeryi</em>, with two CSD loci. Here we show by gene disruption that <em>transformer</em> (<em>tra</em>) is necessary for proper feminization. Expression analysis of <em>tra</em> and <em>doublesex</em> (<em>dsx</em>) showed that heterozygosity in at least one of the two CSD loci is sufficient to promote female sex determination. Analysis of overexpression suggested that female-type Tra protein promotes splicing of <em>tra</em> pre-mRNA to female isoform by a positive-regulatory-feedback loop. Our data also showed that <em>tra</em> affects splicing of <em>dsx</em>. We conclude that two-loci sex determination system in <em>V. emeryi</em> evolved based on <em>tra</em>-<em>dsx</em> splicing cascade that is well conserved in other insect species. Finally, we suggest a cascade model to arrive at a binary determination of sex under multiple primary signals.</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\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Insect Biochemistry and Molecular Biology\",\"FirstCategoryId\":\"97\",\"ListUrlMain\":\"https://www.sciencedirect.com/science/article/pii/S0965174823000322\",\"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}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Insect Biochemistry and Molecular Biology","FirstCategoryId":"97","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0965174823000322","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}
Transformer gene regulates feminization under two complementary sex determination loci in the ant, Vollenhovia emeryi
Organisms that reproduce sexually have evolved well-organized mechanisms to determine two sexes. Some hymenopterans (such as ants, bees, and wasps) have a complementary sex-determination system in which heterozygosity at one CSD locus induces female development, whereas hemi- or homozygosity at the locus induces male development. This system can generate a high cost of inbreeding, as individuals that are homozygous at the locus become sterile, diploid males. On the other hand, some hymenopterans have evolved a multi-locus, complementary, sex-determination system in which heterozygosity in at least one CSD locus induces female development. This system effectively reduces the proportion of sterile diploid males; however, how these multiple primary signals based on CSD pass through a molecular cascade to regulate downstream genes has remained unclear. To clarify this matter, we used a backcross to investigate the molecular cascade in the ant, Vollenhovia emeryi, with two CSD loci. Here we show by gene disruption that transformer (tra) is necessary for proper feminization. Expression analysis of tra and doublesex (dsx) showed that heterozygosity in at least one of the two CSD loci is sufficient to promote female sex determination. Analysis of overexpression suggested that female-type Tra protein promotes splicing of tra pre-mRNA to female isoform by a positive-regulatory-feedback loop. Our data also showed that tra affects splicing of dsx. We conclude that two-loci sex determination system in V. emeryi evolved based on tra-dsx splicing cascade that is well conserved in other insect species. Finally, we suggest a cascade model to arrive at a binary determination of sex under multiple primary signals.
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.