Independent recruitments of a translational regulator in the evolution of self-fertile nematodes

Independent recruitments of a translational regulator in the evolution of self-fertile nematodes
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DOI:
10.1073/pnas.1108068108
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发表时间:
2011-12-06
影响因子:
11.1
通讯作者:
Haag, Eric S.
Haag, Eric S.
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Beadell, Alana V.;Liu, Qinwen;Haag, Eric S.

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多效性发育调节因子已被反复地与解剖学新奇性的进化联系在一起。已知的机制包括顺式调控DNA改变,改变调控转录模式或修饰靶基因连接。在这里,我们研究了另一种形式的调节的作用,翻译控制,在线虫自育雌雄同体的反复进化。秀丽隐杆线虫雌雄同体通过翻译抑制tra-2基因在另一个女性体内启动精子发生。这种抑制是由GLD-1介导的,GLD-1是一种rna结合蛋白,也是卵母细胞减数分裂和分化所必需的。相反,我们发现在趋同雌雄同体的briggsae Caenorhabditis中,GLD-1促进卵子发生。在这些物种中,gld-1的相反功能不是基因固有的,而是由其在每种物种中进化出的独特作用环境造成的。在秀丽隐杆线虫中,GLD-1通过tra-2 mRNA的改变和物种特异性蛋白fog2的进化,成为促进XX精子发生的必要条件。C. briggsae GLD-1成为包括Cbr-puf-8在内的精子促进基因的重要抑制因子,并没有进化出与tra-2的强烈关联。尽管在性别决定中扮演着不同的角色,但gld-1在女性减数分裂过程中的功能是古老而保守的。这种保守的作用可以解释为什么gld-1被反复招募来调节雌雄同体。我们得出的结论是,与转录因子一样,空间定位的翻译调节因子在解剖学新颖性的进化中发挥着重要作用。
Pleiotropic developmental regulators have been repeatedly linked to the evolution of anatomical novelties. Known mechanisms include cis-regulatory DNA changes that alter regulator transcription patterns or modify target-gene linkages. Here, we examine the role of another form of regulation, translational control, in the repeated evolution of self-fertile hermaphroditism in Caenorhabditis nematodes. Caenorhabditis elegans hermaphrodites initiate spermatogenesis in an otherwise female body through translational repression of the gene tra-2. This repression is mediated by GLD-1, an RNA-binding protein also required for oocyte meiosis and differentiation. By contrast, we show that in the convergently hermaphroditic Caenorhabditis briggsae, GLD-1 acts to promote oogenesis. The opposite functions of gld-1 in these species are not gene-intrinsic, but instead result from the unique contexts for its action that evolved in each. In C. elegans, GLD-1 became essential for promoting XX spermatogenesis via changes in the tra-2 mRNA and evolution of the species-specific protein FOG-2. C. briggsae GLD-1 became an essential repressor of sperm-promoting genes, including Cbr-puf-8, and did not evolve a strong association with tra-2. Despite its variable roles in sex determination, the function of gld-1 in female meiotic progression is ancient and conserved. This conserved role may explain why gld-1 is repeatedly recruited to regulate hermaphroditism. We conclude that, as with transcription factors, spatially localized translational regulators play important roles in the evolution of anatomical novelties.