Rapid evolution of a novel signalling mechanism by concerted duplication and divergence of a BMP ligand and its extracellular modulators

Rapid evolution of a novel signalling mechanism by concerted duplication and divergence of a BMP ligand and its extracellular modulators
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DOI:
10.1007/s00427-010-0341-5
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发表时间:
2010-12-01
影响因子:
2.4
通讯作者:
Ray, Robert P.
Ray, Robert P.
中科院分区:
生物学4区
文献类型:
--
作者:
Fritsch, Cornelia;Lanfear, Robert;Ray, Robert P.

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基因复制和分化被广泛认为是产生进化新颖性的基本机制。骨形态发生蛋白(BMPs)是在所有后生动物基因组中发现的一个多样化的信号分子家族,通过复制和分化从少数祖先类型进化而来。果蝇中存在三种bmp: Decapentaplegic (Dpp)和Glass bottom boat (Gbb),它们分别与脊椎动物BMP2/4和BMP5/6/7/8同源;Screw (Scw),在序列水平上与Dpp和Gbb具有相同的差异。最近有研究表明,Scw是由Gbb在谱系中的重复引起的,导致更高的双翅目。我们发现,自这一重复事件以来,Gbb保持了祖先BMP5/6/7/8的功能,而Scw则迅速分化。Scw的进化伴随着一套细胞外调节因子的复制和分化,这些调节因子在高等双翅目动物中继续分化。此外,Scw的受体特异性受到限制:Gbb蛋白可以通过I型受体粗静脉(Tkv)和萨克斯管(Sax)发出信号,而Scw通过Sax发出信号。因此,在相对较短的进化时间内,导致Scw的复制事件不仅产生了一种新的配体,而且产生了一种新的信号模式,在功能上与祖先的Gbb模式不同。我们的研究结果表明,BMP通路不仅在进化新的家族成员和新功能方面具有可塑性,而且通过重新部署通路中的关键调节因子,也具有新的信号模式。
Gene duplication and divergence is widely considered to be a fundamental mechanism for generating evolutionary novelties. The Bone Morphogenetic Proteins (BMPs) are a diverse family of signalling molecules found in all metazoan genomes that have evolved by duplication and divergence from a small number of ancestral types. In the fruit fly Drosophila, there are three BMPs: Decapentaplegic (Dpp) and Glass bottom boat (Gbb), which are the orthologues of vertebrate BMP2/4 and BMP5/6/7/8, respectively, and Screw (Scw), which, at the sequence level, is equally divergent from Dpp and Gbb. It has recently been shown that Scw has arisen from a duplication of Gbb in the lineage leading to higher Diptera. We show that since this duplication event, Gbb has maintained the ancestral BMP5/6/7/8 functionality while Scw has rapidly diverged. The evolution of Scw was accompanied by duplication and divergence of a suite of extracellular regulators that continue to diverge together in the higher Diptera. In addition, Scw has become restricted in its receptor specificity: Gbb proteins can signal through the Type I receptors Thick veins (Tkv) and Saxophone (Sax), while Scw signals through Sax. Thus, in a relatively short span of evolutionary time, the duplication event that gave rise to Scw produced not only a novel ligand but also a novel signalling mode that is functionally distinct from the ancestral Gbb mode. Our results demonstrate the plasticity of the BMP pathway not only in evolving new family members and new functions but also new signalling modes by redeploying key regulators in the pathway.