Parallel evolution of chordate cis-regulatory code for development.

Parallel evolution of chordate cis-regulatory code for development.
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DOI:
10.1371/journal.pgen.1003904
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发表时间:
2013-11
期刊:
影响因子:
4.5
通讯作者:
Elgar G
Elgar G
中科院分区:
生物学2区
文献类型:
--
作者:
Doglio L;Goode DK;Pelleri MC;Pauls S;Frabetti F;Shimeld SM;Vavouri T;Elgar G

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尾索动物是脊椎动物的近亲,在幼虫阶段,具有特征性的双侧脊索动物身体平面。在脊椎动物中,编排胚胎模式的基因部分由高度保守的非编码元件(CNE)调节,但这些元件尚未在尾索动物基因组中被鉴定。因此,进化的顺式调节代码的尿脊索动物的发展仍然在很大程度上没有特点。在这里,我们使用C.和C. Savignyi以鉴定推定的尾索动物顺式调节序列。玻璃海鞘保守非编码元件(ciCNEs)与脊椎动物CNEs基本上相同的关键调控基因相关。此外,一些测试的ciCNE能够激活斑马鱼和玻璃海鞘胚胎中的报告基因表达,尽管缺乏序列同一性,但其模式至少部分与它们相关的基因的模式重叠。我们还表明,在脊椎动物胚胎中,ciCNE上调基因表达的能力在某些情况下可以局限于短的子序列,这表明功能性串扰可能是由祖先调控逻辑的小区域定义的,尽管功能性子序列也可能分散在整个元件中。我们的结论是,脊椎动物和尾索动物之间的顺式调控模块的结构和组织是非常不同的,反映了他们各自的进化历史。然而,功能性串扰仍然存在,因为相同的转录因子库可能引导它们的平行进化,利用相似的结合位点集,但以不同的组合。脊椎动物与我们最接近的脊索动物祖先被囊动物在早期发育的许多方面是相同的。然而,虽然编排发育的基因库在两个谱系中基本相同,但调节这些基因的基因组密码似乎非常不同,尽管它在脊椎动物本身中高度保守。使用比较基因组学,我们已经确定了一个平行的发育代码在被囊类动物,并证实,这个代码,尽管缺乏序列保守性,与类似的基因库。然而,在空间上的代码的组织是非常不同的两个谱系,强烈表明,它的大部分独立出现在脊椎动物和被囊动物,在大多数情况下,缺乏任何直接的序列祖先。我们已经分析了被囊动物编码的元素,发现其中至少有一些可以调节斑马鱼胚胎中的基因表达。我们的研究结果表明,调控代码已经出现在不同的动物谱系独立,但具有一些共同的功能,因为它的进化已经由一个类似的队列的发展转录因子。我们的工作有助于阐明复杂、稳定的基因调控网络是如何进化并在谱系内固定下来的。
Urochordates are the closest relatives of vertebrates and at the larval stage, possess a characteristic bilateral chordate body plan. In vertebrates, the genes that orchestrate embryonic patterning are in part regulated by highly conserved non-coding elements (CNEs), yet these elements have not been identified in urochordate genomes. Consequently the evolution of the cis-regulatory code for urochordate development remains largely uncharacterised. Here, we use genome-wide comparisons between C. intestinalis and C. savignyi to identify putative urochordate cis-regulatory sequences. Ciona conserved non-coding elements (ciCNEs) are associated with largely the same key regulatory genes as vertebrate CNEs. Furthermore, some of the tested ciCNEs are able to activate reporter gene expression in both zebrafish and Ciona embryos, in a pattern that at least partially overlaps that of the gene they associate with, despite the absence of sequence identity. We also show that the ability of a ciCNE to up-regulate gene expression in vertebrate embryos can in some cases be localised to short sub-sequences, suggesting that functional cross-talk may be defined by small regions of ancestral regulatory logic, although functional sub-sequences may also be dispersed across the whole element. We conclude that the structure and organisation of cis-regulatory modules is very different between vertebrates and urochordates, reflecting their separate evolutionary histories. However, functional cross-talk still exists because the same repertoire of transcription factors has likely guided their parallel evolution, exploiting similar sets of binding sites but in different combinations. Vertebrates share many aspects of early development with our closest chordate ancestors, the tunicates. However, whilst the repertoire of genes that orchestrate development is essentially the same in the two lineages, the genomic code that regulates these genes appears to be very different, even though it is highly conserved within vertebrates themselves. Using comparative genomics, we have identified a parallel developmental code in tunicates and confirmed that this code, despite a lack of sequence conservation, associates with a similar repertoire of genes. However, the organisation of the code spatially is very different in the two lineages, strongly suggesting that most of it arose independently in vertebrates and tunicates, and in most cases lacking any direct sequence ancestry. We have assayed elements of the tunicate code, and found that at least some of them can regulate gene expression in zebrafish embryos. Our results suggest that regulatory code has arisen independently in different animal lineages but possesses some common functionality because its evolution has been driven by a similar cohort of developmental transcription factors. Our work helps illuminate how complex, stable gene regulatory networks evolve and become fixed within lineages.
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