Solenodon genome reveals convergent evolution of venom in eulipotyphlan mammals

Solenodon genome reveals convergent evolution of venom in eulipotyphlan mammals
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DOI:
10.1073/pnas.1906117116
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发表时间:
2019-12-17
影响因子:
11.1
通讯作者:
Turvey, Samuel T.
Turvey, Samuel T.
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Casewell, Nicholas R.;Petras, Daniel;Turvey, Samuel T.

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毒液系统是在整个生命树中进化的关键适应,通常有助于捕食或防御。尽管毒液是研究各种进化和生理过程的模型系统,但许多分类学群体仍然研究不足,包括有毒哺乳动物。在Eulipotyphla目中,许多种类的鼩 鼱和管齿蜥都有口腔毒液系统。尽管其传递系统的形态变化,目前还不清楚毒液是否代表这一组的祖先状态或多个独立的起源的结果。我们调查的起源和进化的毒液在eulipotyphlans的特点,毒系统的濒危Hispaniolan solenodon paradoxus(Solenodon paradoxus)。我们构建了一个基因组来支持Solenodon毒液毒素的蛋白质组学鉴定,然后对这些成分进行进化分析,并对分泌的毒液进行功能评估。我们的研究结果表明,solenodon毒液由多种旁系同源的激肽释放酶1(KLK 1)丝氨酸蛋白酶,在体内引起的肿胀效应,似乎已经进化到促进脊椎动物猎物捕获。比较分析提供了令人信服的证据,solenodons和鼩的口腔毒液系统已经趋同进化,与4个独立的毒液来源eulipotyphlans超过所有其他毒液来源的哺乳动物。我们发现,KLK1已独立增选到毒液的鼩和solenodons后,他们的分歧在白垩纪晚期,这表明进化的限制可能会对这些基因。因此,我们的研究结果代表了趋同分子进化的一个引人注目的例子,并表明不同的结构背景可以产生等效的功能。
Venom systems are key adaptations that have evolved throughout the tree of life and typically facilitate predation or defense. Despite venoms being model systems for studying a variety of evolutionary and physiological processes, many taxonomic groups remain understudied, including venomous mammals. Within the order Eulipotyphla, multiple shrew species and solenodons have oral venom systems. Despite morphological variation of their delivery systems, it remains unclear whether venom represents the ancestral state in this group or is the result of multiple independent origins. We investigated the origin and evolution of venom in eulipotyphlans by characterizing the venom system of the endangered Hispaniolan solenodon (Solenodon paradoxus). We constructed a genome to underpin proteomic identifications of solenodon venom toxins, before undertaking evolutionary analyses of those constituents, and functional assessments of the secreted venom. Our findings show that solenodon venom consists of multiple paralogous kallikrein 1 (KLK1) serine proteases, which cause hypotensive effects in vivo, and seem likely to have evolved to facilitate vertebrate prey capture. Comparative analyses provide convincing evidence that the oral venom systems of solenodons and shrews have evolved convergently, with the 4 independent origins of venom in eulipotyphlans outnumbering all other venom origins in mammals. We find that KLK1s have been independently coopted into the venom of shrews and solenodons following their divergence during the late Cretaceous, suggesting that evolutionary constraints may be acting on these genes. Consequently, our findings represent a striking example of convergent molecular evolution and demonstrate that distinct structural backgrounds can yield equivalent functions.