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Evolution of the endothelin pathway drove neural crest cell diversification
Nature ( IF 50.5 ) Pub Date : 2020-09-16 , DOI: 10.1038/s41586-020-2720-z
Tyler A Square 1, 2 , David Jandzik 1, 3, 4 , James L Massey 1 , Marek Romášek 1, 5 , Haley P Stein 1 , Andrew W Hansen 1 , Amrita Purkayastha 1 , Maria V Cattell 1, 6 , Daniel M Medeiros 1
Affiliation  

Neural crest cells (NCCs) are migratory, multipotent embryonic cells that are unique to vertebrates and form an array of clade-defining adult features. The evolution of NCCs has been linked to various genomic events, including the evolution of new gene-regulatory networks 1 , 2 , the de novo evolution of genes 3 and the proliferation of paralogous genes during genome-wide duplication events 4 . However, conclusive functional evidence linking new and/or duplicated genes to NCC evolution is lacking. Endothelin ligands (Edns) and endothelin receptors (Ednrs) are unique to vertebrates 3 , 5 , 6 , and regulate multiple aspects of NCC development in jawed vertebrates 7 – 10 . Here, to test whether the evolution of Edn signalling was a driver of NCC evolution, we used CRISPR–Cas9 mutagenesis 11 to disrupt edn , ednr and dlx genes in the sea lamprey, Petromyzon marinus . Lampreys are jawless fishes that last shared a common ancestor with modern jawed vertebrates around 500 million years ago 12 . Thus, comparisons between lampreys and gnathostomes can identify deeply conserved and evolutionarily flexible features of vertebrate development. Using the frog Xenopus laevis to expand gnathostome phylogenetic representation and facilitate side-by-side analyses, we identify ancient and lineage-specific roles for Edn signalling. These findings suggest that Edn signalling was activated in NCCs before duplication of the vertebrate genome. Then, after one or more genome-wide duplications in the vertebrate stem, paralogous Edn pathways functionally diverged, resulting in NCC subpopulations with different Edn signalling requirements. We posit that this new developmental modularity facilitated the independent evolution of NCC derivatives in stem vertebrates. Consistent with this, differences in Edn pathway targets are associated with differences in the oropharyngeal skeleton and autonomic nervous system of lampreys and modern gnathostomes. In summary, our work provides functional genetic evidence linking the origin and duplication of new vertebrate genes with the stepwise evolution of a defining vertebrate novelty. CRISPR–Cas9-mediated disruption of the endothelin-signalling pathway in the sea lamprey Petromyzon marinus and the frog Xenopus laevis were used to delineate ancient and lineage-specific roles of endothelin signalling and provide insights into vertebrate evolution.

中文翻译:

内皮素通路的进化驱动神经嵴细胞多样化

神经嵴细胞 (NCC) 是脊椎动物特有的迁移性多能胚胎细胞,形成一系列定义进化枝的成年特征。NCC 的进化与各种基因组事件有关,包括新基因调控网络 1、2 的进化、基因 3 的从头进化以及全基因组复制事件 4 期间旁系同源基因的增殖。然而,缺乏将新基因和/或重复基因与 NCC 进化联系起来的确凿功能证据。内皮素配体 (Edns) 和内皮素受体 (Ednrs) 是脊椎动物 3、5、6 所独有的,并且在有颌脊椎动物 7-10 中调节 NCC 发育的多个方面。在这里,为了测试 Edn 信号的进化是否是 NCC 进化的驱动因素,我们使用 CRISPR-Cas9 诱变 11 来破坏海七鳃鳗中的 edn 、 ednr 和 dlx 基因,Petromyzon marinus。七鳃鳗是无颚鱼类,它们最后与现代有颚脊椎动物共有一个共同祖先是在大约 5 亿年前 12 。因此,七鳃鳗和有颚类动物之间的比较可以确定脊椎动物发育的高度保守和进化灵活的特征。使用青蛙非洲爪蟾扩展有颌动物系统发育表征并促进并排分析,我们确定了 Edn 信号传递的古老和谱系特定作用。这些发现表明,在脊椎动物基因组复制之前,NCC 中的 Edn 信号被激活。然后,在脊椎动物茎中进行一次或多次全基因组重复后,旁系同源 Edn 通路在功能上发生分歧,导致 NCC 亚群具有不同的 Edn 信号传导需求。我们假设这种新的发育模块化促进了干脊椎动物中 NCC 衍生物的独立进化。与此一致,Edn 通路目标的差异与七鳃鳗和现代有颌动物的口咽骨骼和自主神经系统的差异有关。总之,我们的工作提供了功能遗传证据,将新脊椎动物基因的起源和复制与定义脊椎动物新事物的逐步进化联系起来。CRISPR-Cas9 介导的海七鳃鳗 Petromyzon marinus 和青蛙非洲爪蟾中内皮素信号通路的破坏被用来描绘内皮素信号传导的古老和谱系特异性作用,并提供对脊椎动物进化的见解。Edn 通路目标的差异与七鳃鳗和现代有颌动物的口咽骨骼和自主神经系统的差异有关。总之,我们的工作提供了功能遗传证据,将新脊椎动物基因的起源和复制与定义脊椎动物新事物的逐步进化联系起来。CRISPR-Cas9 介导的海七鳃鳗 Petromyzon marinus 和青蛙非洲爪蟾中内皮素信号通路的破坏被用来描绘内皮素信号传导的古老和谱系特异性作用,并提供对脊椎动物进化的见解。Edn 通路目标的差异与七鳃鳗和现代有颌动物的口咽骨骼和自主神经系统的差异有关。总之,我们的工作提供了功能遗传证据,将新脊椎动物基因的起源和复制与定义脊椎动物新事物的逐步进化联系起来。CRISPR-Cas9 介导的海七鳃鳗 Petromyzon marinus 和青蛙非洲爪蟾中内皮素信号通路的破坏被用来描绘内皮素信号传导的古老和谱系特异性作用,并提供对脊椎动物进化的见解。我们的工作提供了功能遗传证据,将新脊椎动物基因的起源和复制与定义脊椎动物新事物的逐步进化联系起来。CRISPR-Cas9 介导的海七鳃鳗 Petromyzon marinus 和青蛙非洲爪蟾中内皮素信号通路的破坏被用来描绘内皮素信号传导的古老和谱系特异性作用,并提供对脊椎动物进化的见解。我们的工作提供了功能遗传证据,将新脊椎动物基因的起源和复制与定义脊椎动物新事物的逐步进化联系起来。CRISPR-Cas9 介导的海七鳃鳗 Petromyzon marinus 和青蛙非洲爪蟾中内皮素信号通路的破坏被用来描绘内皮素信号传导的古老和谱系特异性作用,并提供对脊椎动物进化的见解。
更新日期:2020-09-16
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