Environmental sex determination in the branchiopod crustacean Daphnia magna: deep conservation of a Doublesex gene in the sex-determining pathway.

Environmental sex determination in the branchiopod crustacean Daphnia magna: deep conservation of a Doublesex gene in the sex-determining pathway.
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DOI:
10.1371/journal.pgen.1001345
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发表时间:
2011-03
期刊:
影响因子:
4.5
通讯作者:
Iguchi T
Iguchi T
中科院分区:
生物学2区
文献类型:
--
作者:
Kato Y;Kobayashi K;Watanabe H;Iguchi T

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性别决定机制在动物谱系中是多样的,可以大致分为两大类:遗传和环境。相对于遗传性别决定(GSD),环境性别决定(ESD)的分子机制知之甚少。Dsx基因在控制线虫、昆虫和脊椎动物等性别决定生物的两性异形中起着重要作用。在这里,我们报告了两个DSX基因的鉴定大型蚤,淡水鳃足类甲壳动物,孤雌生殖产生男性在环境的线索。这些基因之一,指定DapmaDsx1,是负责男性性状的发展时,在环境性别决定表达。DapmaDsx 1的结构域组织类似于昆虫的Dsx,昆虫被认为是鳃足类甲壳动物的姐妹群。有趣的是,DapmaDsx1的性二态表达的分子基础与昆虫不同。DapmaDsx1在其转录本的丰度上表现出性别二态性差异,而不是在编码区的前mRNA剪接水平上受到性别特异性调控。在胚胎发生过程中,DapmaDsx 1的表达增加,只在男性和其成绩单主要检测到男性特定的结构。在雄性胚胎中敲低DapmaDsx1导致雌性性状的产生,包括卵巢成熟,而在雌性胚胎中异位表达DapmaDsx1导致雄性样表型的发育。另一种D.大Dsx基因DapmaDsx 2与DapmaDsx 1相似,但该基因的沉默和过表达并没有引起任何明显的表型变化。这些结果确立了DapmaDsx1作为雄性表型的关键调节因子。我们的研究结果揭示了ESD是如何通过选择性表达一种基本的遗传成分来实现的,这种遗传成分在使用GSD的动物中是功能保守的。我们推断,在遗传和环境性别决定之间存在着一种古老的、以前未被发现的联系。性别决定是一个基本的生物学过程,可以大致分为两大类。在遗传性别决定(GSD)中,性别特异性分化是由雄性和雌性之间的内在遗传差异引起的,而环境性别决定(ESD)则依赖于环境信号来诱导雄性或雌性的性别决定。与利用GSD系统的模式生物相比,环境性别决定生物是较差的遗传模型。因此,尽管在脊椎动物中发现了参与ESD的候选基因,但它们的功能在很大程度上仍然未知,这削弱了我们对ESD的理解,并使两个系统之间的性别决定基因的比较变得困难。在这里,我们报告的基因负责生产过程中的环境性别决定的甲壳类水蚤的男性的鉴定。该基因与在使用GSD的动物中功能保守的Doublemex基因同源。Doubletex的表达主要在男性特异性结构中增加。获得和丧失功能的分析表明,Daphnia Doubriex基因是一个主要的效应器,调节水蚤的雄性表型。我们推断,在遗传和环境性别决定之间存在着一种古老的、以前未被发现的联系。
Sex-determining mechanisms are diverse among animal lineages and can be broadly divided into two major categories: genetic and environmental. In contrast to genetic sex determination (GSD), little is known about the molecular mechanisms underlying environmental sex determination (ESD). The Doublesex (Dsx) genes play an important role in controlling sexual dimorphism in genetic sex-determining organisms such as nematodes, insects, and vertebrates. Here we report the identification of two Dsx genes from Daphnia magna, a freshwater branchiopod crustacean that parthenogenetically produces males in response to environmental cues. One of these genes, designated DapmaDsx1, is responsible for the male trait development when expressed during environmental sex determination. The domain organization of DapmaDsx1 was similar to that of Dsx from insects, which are thought to be the sister group of branchiopod crustaceans. Intriguingly, the molecular basis for sexually dimorphic expression of DapmaDsx1 is different from that of insects. Rather than being regulated sex-specifically at the level of pre–mRNA splicing in the coding region, DapmaDsx1 exhibits sexually dimorphic differences in the abundance of its transcripts. During embryogenesis, expression of DapmaDsx1 was increased only in males and its transcripts were primarily detected in male-specific structures. Knock-down of DapmaDsx1 in male embryos resulted in the production of female traits including ovarian maturation, whereas ectopic expression of DapmaDsx1 in female embryos resulted in the development of male-like phenotypes. Expression patterns of another D. magna Dsx gene, DapmaDsx2, were similar to those of DapmaDsx1, but silencing and overexpression of this gene did not induce any clear phenotypic changes. These results establish DapmaDsx1 as a key regulator of the male phenotype. Our findings reveal how ESD is implemented by selective expression of a fundamental genetic component that is functionally conserved in animals using GSD. We infer that there is an ancient, previously unidentified link between genetic and environmental sex determination. Sex determination is a fundamental biological process that can be broadly divided into two major categories. In genetic sex determination (GSD), sex-specific differentiation results from intrinsic genetic differences between males and females, whereas environmental sex determination (ESD) relies on environmental signals to induce male or female sex determination. In contrast to model organisms that utilize GSD system, environmental sex-determining organisms are poor genetic models. Therefore, although candidate genes involved in ESD have been found in vertebrates, their functions have remained largely unknown, impairing our understanding of ESD and making the comparison of sex-determining genes between both systems difficult. Here, we report the identification of a gene responsible for the production of males during environmental sex determination in the crustacean Daphnia. This gene is homologous to the Doublesex gene that is functionally conserved in animals that use GSD. Expression of Doublesex was increased primarily in male-specific structures. Gain- and loss-of-function analyses established that Daphnia Doublesex gene is a major effector that regulates the male phenotype in Daphnia. We infer that there is an ancient, previously unidentified link between genetic and environmental sex determination.
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