Ancient and novel small RNA pathways compensate for the loss of piRNAs in multiple independent nematode lineages.
Ancient and novel small RNA pathways compensate for the loss of piRNAs in multiple independent nematode lineages.
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DOI：
10.1371/journal.pbio.1002061
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发表时间：
2015-02
期刊：
影响因子：
9.8
通讯作者：
Miska EA
中科院分区：
文献类型：
--
作者：
Sarkies P;Selkirk ME;Jones JT;Blok V;Boothby T;Goldstein B;Hanelt B;Ardila-Garcia A;Fast NM;Schiffer PM;Kraus C;Taylor MJ;Koutsovoulos G;Blaxter ML;Miska EA
小RNA通路在真核生物中防御转座元件的前线起作用。在动物中，Piwi相互作用的小RNA(PiRNAs)是这种防御的关键手臂。然而，针对转座元件的piRNAs和其他小RNA途径之间的进化关系尚未得到很好的解决。为了解决这个问题，我们对多个不同线虫物种的小RNA进行了测序，首次对小RNA途径如何进化进行了全门范围的分析。令人惊讶的是，尽管piRNAs在秀丽线虫和密切相关的线虫中显著存在，但在所有其他线虫谱系中都没有。我们发现，至少有两种进化上不同的机制来弥补piRNAs的缺失，这两种机制都涉及RNA依赖的RNA聚合酶(RdRPs)。虽然其中一条途径是线虫所特有的，但第二条途径涉及依赖于依赖RNA的DNA甲基化，这在动物中是未知的，与真菌和植物中的转座子控制机制有着惊人的相似之处。我们的结果强调了小RNA途径的快速、上下文相关的进化，并表明动物中的piRNAs可能已经取代了古老的依赖于真核RNA的RNA聚合酶途径来控制转座元件。对线虫门的调查显示，在几个谱系中丢失了Piwi/piRNA途径，但依赖于RNA的RNA聚合酶在缺乏转座子的情况下控制转座元件。转座元件是DNA片段，具有独立于宿主基因组复制自身的能力，因此对基因组的完整性构成严重威胁。生物体已经进化出限制转座元件扩散的机制，小RNA分子是最重要的防御机制之一。在动物中，主要的小RNA转座子沉默机制是piRNA途径，它似乎是广泛保守的。然而，人们对以转座子为靶标的小RNA通路是如何进化的知之甚少。为了研究这个问题，我们使用一个研究得很好的模式生物-线虫秀丽线虫-作为起点，研究了跨越线虫门的小RNA途径。令人惊讶的是，我们发现除了与线虫关系最密切的线虫外，所有线虫群体中的piRNA途径都完全丢失。这一发现提出了一个有趣的问题，即这些线虫如何能够在没有piRNA的情况下控制转座元件的动员。我们发现，在这些线虫中，还有其他针对转座元件的小RNA途径，使用RNA依赖的RNA聚合酶来使小RNA对转座元件反义。有趣的是，在最基本的线虫中发现的这些机制中，最古老的是依赖于DNA的依赖RNA的DNA甲基化途径。这一途径与植物和真菌中的转座子沉默机制有很强的相似性，表明它可能存在于所有真核生物的古老共同祖先中。我们的结果强调了小RNA途径的快速进化，并证明了在一系列进化距离上详细检查分子途径的重要性。
Small RNA pathways act at the front line of defence against transposable elements across the Eukaryota. In animals, Piwi interacting small RNAs (piRNAs) are a crucial arm of this defence. However, the evolutionary relationships among piRNAs and other small RNA pathways targeting transposable elements are poorly resolved. To address this question we sequenced small RNAs from multiple, diverse nematode species, producing the first phylum-wide analysis of how small RNA pathways evolve. Surprisingly, despite their prominence in Caenorhabditis elegans and closely related nematodes, piRNAs are absent in all other nematode lineages. We found that there are at least two evolutionarily distinct mechanisms that compensate for the absence of piRNAs, both involving RNA-dependent RNA polymerases (RdRPs). Whilst one pathway is unique to nematodes, the second involves Dicer-dependent RNA-directed DNA methylation, hitherto unknown in animals, and bears striking similarity to transposon-control mechanisms in fungi and plants. Our results highlight the rapid, context-dependent evolution of small RNA pathways and suggest piRNAs in animals may have replaced an ancient eukaryotic RNA-dependent RNA polymerase pathway to control transposable elements. A survey of the nematode phylum reveals loss of the Piwi/piRNA pathway in several lineages, but RNA-dependent RNA polymerases control transposable elements in its absence. Transposable elements are segments of DNA that have the ability to copy themselves independently of the host genome and thus pose a severe threat to the integrity of the genome. Organisms have evolved mechanisms to restrict the spread of transposable elements, with small RNA molecules being one of the most important defense mechanisms. In animals, the predominant small RNA transposon-silencing mechanism is the piRNA pathway, which appears to be widely conserved. However, little is known about how small RNA pathways that target transposons evolve. In order to study this question we investigated small RNA pathways across the nematode phylum, using a well-studied model organism—the nematode Caenorhabditis elegans—as the starting point. Surprisingly we found that the piRNA pathway has been completely lost in all groups of nematodes bar those most closely related to C. elegans. This finding raises the intriguing question of how these nematodes are able to control transposable element mobilization without piRNAs. We discovered that there are other small RNA pathways that target transposable elements in these nematodes, employing RNA-dependent RNA polymerases in order to make small RNAs antisense to transposable elements. Intriguingly, the most ancient of these mechanisms, found in the most basal nematodes, is a Dicer-dependent RNA-directed DNA methylation pathway. This pathway shares strong similarity to transposon-silencing mechanisms in plants and fungi, suggesting that it might have been present in an ancient common ancestor of all eukaryotes. Our results highlight the rapid evolution of small RNA pathways and demonstrate the importance of examining molecular pathways in detail across a range of evolutionary distances.
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