Center for Bioscience Research and Education, Utsunomiya University, 350, Minemachi, Utsunomiya, Tochigi, 321-8505, Japan.
Center for Bioscience Research and Education, Utsunomiya University, 350, Minemachi, Utsunomiya, Tochigi, 321-8505, Japan.
Insect Biochem Mol Biol. 2023 May;156:103938. doi: 10.1016/j.ibmb.2023.103938. Epub 2023 Apr 5.
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.
有性繁殖的生物进化出了组织良好的机制来确定两种性别。一些膜翅目昆虫（如蚂蚁、蜜蜂和黄蜂）具有互补的性别决定系统，其中一个 CSD 基因座的杂合性诱导雌性发育，而该基因座的半合子或纯合子诱导雄性发育。该系统会产生较高的近交成本，因为该基因座纯合的个体成为不育的二倍体雄性。另一方面，一些膜翅目昆虫进化出了多基因座、互补的性别决定系统，至少一个 CSD 基因座的杂合性诱导雌性发育。该系统有效地降低了不育二倍体雄性的比例；然而，这些基于 CSD 的多个主要信号如何通过分子级联来调控下游基因仍然不清楚。为了阐明这一问题，我们使用回交方法研究了具有两个 CSD 基因座的蚂蚁 Vollenhovia emeryi 的分子级联。在这里，我们通过基因敲除表明 transformer（tra）对于适当的雌性化是必要的。tra 和 doublesex（dsx）的表达分析表明，至少在两个 CSD 基因座中的一个基因座的杂合性足以促进雌性性别决定。过表达分析表明，雌性型 Tra 蛋白通过正反馈环促进 tra 前体 mRNA 向雌性同工型的剪接。我们的数据还表明 tra 影响 dsx 的剪接。我们得出结论，V. emeryi 的双基因座性别决定系统是基于 tra-dsx 剪接级联进化而来的，该级联在其他昆虫物种中得到了很好的保守。最后，我们提出了一个级联模型，以在多个主要信号下实现二元性别决定。
