Unicellular Origin of the Animal MicroRNA Machinery.

Unicellular Origin of the Animal MicroRNA Machinery.
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DOI:
10.1016/j.cub.2018.08.018
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发表时间:
2018-10-22
期刊:
Current biology : CB
影响因子:
--
通讯作者:
Shalchian-Tabrizi K
Shalchian-Tabrizi K
中科院分区:
其他
文献类型:
--
作者:
Bråte J;Neumann RS;Fromm B;Haraldsen AAB;Tarver JE;Suga H;Donoghue PCJ;Peterson KJ;Ruiz-Trillo I;Grini PE;Shalchian-Tabrizi K

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多细胞动物的出现与表型复杂性的增加以及空间细胞分化和胚胎发育的获得有关。矛盾的是,这种表型转变与潜在的发育工具和调控网络的重大变化并不平行。事实上,这些系统大多是古老的,在动物的单细胞祖先中就已经建立起来了。相比之下,对于动物体内microRNA (miRNA)生物发生至关重要的微处理器蛋白质机制,以及由该微处理器产生的miRNA基因本身,尚未在动物王国之外被发现。因此,含有关键蛋白Pasha和Drosha的微处理器被认为是动物的创新。在这里,我们通过基因组和转录组学分析研究动物的单细胞姐妹谱系,挑战了这种进化情景。我们在Ichthyosporea中发现了Drosha和Pasha(脊椎动物中的DGCR8),这表明微处理器复合物的进化早于动物最后的共同祖先,与大多数动物发育基因元件的前后生动物起源一致。通过小RNA测序,我们还发现在几种携带微处理器的鱼孢子虫物种中表达了真正的miRNA基因。微处理器和mirna的深层、前后生动物起源符合一种观点,即多细胞动物的起源与这些关键调控成分的创新没有直接联系。动物特异性miRNA微处理器在单细胞鱼孢子虫中被发现,动物miRNA机制的起源独立于动物多细胞,微处理器在栉水母中丢失,并不是动物祖先的特征,一些鱼孢子虫携带微处理器表达真正的miRNA。在动物中,microrna和miRNA生物发生机制对正确的生物体发育至关重要。bramatte等人证明,这种机器的核心,微处理器,不是动物的创新,而是起源于它们的单细胞亲戚。一些含有微处理器的单细胞物种也表达真正的mirna。
The emergence of multicellular animals was associated with an increase in phenotypic complexity and with the acquisition of spatial cell differentiation and embryonic development. Paradoxically, this phenotypic transition was not paralleled by major changes in the underlying developmental toolkit and regulatory networks. In fact, most of these systems are ancient, established already in the unicellular ancestors of animals. In contrast, the Microprocessor protein machinery, which is essential for microRNA (miRNA) biogenesis in animals, as well as the miRNA genes themselves produced by this Microprocessor, have not been identified outside of the animal kingdom. Hence, the Microprocessor, with the key proteins Pasha and Drosha, is regarded as an animal innovation. Here, we challenge this evolutionary scenario by investigating unicellular sister lineages of animals through genomic and transcriptomic analyses. We identify in Ichthyosporea both Drosha and Pasha (DGCR8 in vertebrates), indicating that the Microprocessor complex evolved long before the last common ancestor of animals, consistent with a pre-metazoan origin of most of the animal developmental gene elements. Through small RNA sequencing, we also discovered expressed bona fide miRNA genes in several species of the ichthyosporeans harboring the Microprocessor. A deep, pre-metazoan origin of the Microprocessor and miRNAs comply with a view that the origin of multicellular animals was not directly linked to the innovation of these key regulatory components. The animal-specific miRNA Microprocessor is discovered in unicellular Ichthyosporea The origin of the animal miRNA machinery was independent of animal multicellularity The Microprocessor is lost in ctenophores and is not an ancestral animal trait Several ichthyosporeans harboring the Microprocessor express bona fide miRNAs In animals, microRNAs and the miRNA biogenesis machinery are essential for correct organismal development. Bråte et al. demonstrate that the core of this machinery, the Microprocessor, is not an animal innovation but originated among their unicellular relatives. Several unicellular species harboring the Microprocessor also express bona fide miRNAs.
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