Department of Biological Mechanisms and Functions, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Japan.
PLoS Genet. 2012 Sep;8(9):e1002953. doi: 10.1371/journal.pgen.1002953. Epub 2012 Sep 27.
RNA silencing is a defense system against "genomic parasites" such as transposable elements (TE), which are potentially harmful to host genomes. In plants, transcripts from TEs induce production of double-stranded RNAs (dsRNAs) and are processed into small RNAs (small interfering RNAs, siRNAs) that suppress TEs by RNA-directed DNA methylation. Thus, the majority of TEs are epigenetically silenced. On the other hand, most of the eukaryotic genome is composed of TEs and their remnants, suggesting that TEs have evolved countermeasures against host-mediated silencing. Under some circumstances, TEs can become active and increase in copy number. Knowledge is accumulating on the mechanisms of TE silencing by the host; however, the mechanisms by which TEs counteract silencing are poorly understood. Here, we show that a class of TEs in rice produces a microRNA (miRNA) to suppress host silencing. Members of the microRNA820 (miR820) gene family are located within CACTA DNA transposons in rice and target a de novo DNA methyltransferase gene, OsDRM2, one of the components of epigenetic silencing. We confirmed that miR820 negatively regulates the expression of OsDRM2. In addition, we found that expression levels of various TEs are increased quite sensitively in response to decreased OsDRM2 expression and DNA methylation at TE loci. Furthermore, we found that the nucleotide sequence of miR820 and its recognition site within the target gene in some Oryza species have co-evolved to maintain their base-pairing ability. The co-evolution of these sequences provides evidence for the functionality of this regulation. Our results demonstrate how parasitic elements in the genome escape the host's defense machinery. Furthermore, our analysis of the regulation of OsDRM2 by miR820 sheds light on the action of transposon-derived small RNAs, not only as a defense mechanism for host genomes but also as a regulator of interactions between hosts and their parasitic elements.
RNA 沉默是一种针对“基因组寄生虫”的防御系统，例如转座元件（TE），它们对宿主基因组可能有害。在植物中，TE 的转录物诱导双链 RNA（dsRNA）的产生，并被加工成小 RNA（小干扰 RNA，siRNA），通过 RNA 指导的 DNA 甲基化抑制 TE。因此，大多数 TE 被表观遗传沉默。另一方面，真核生物基因组的大部分由 TE 及其残留物组成，这表明 TE 已经进化出了对抗宿主介导沉默的对策。在某些情况下，TE 可以变得活跃并增加其拷贝数。关于宿主介导的 TE 沉默机制的知识正在积累；然而，TE 对抗沉默的机制还知之甚少。在这里，我们表明水稻中的一类 TE 产生 microRNA（miRNA）来抑制宿主沉默。microRNA820（miR820）基因家族的成员位于水稻中的 CACTA DNA 转座子内，靶向从头 DNA 甲基转移酶基因 OsDRM2，这是表观遗传沉默的组成部分之一。我们证实 miR820 负调控 OsDRM2 的表达。此外，我们发现各种 TE 的表达水平在 OsDRM2 表达降低和 TE 位点的 DNA 甲基化增加时非常敏感地增加。此外，我们发现 miR820 的核苷酸序列及其在一些 Oryza 物种中的靶基因中的识别位点已经协同进化以保持其碱基配对能力。这些序列的协同进化为这种调控的功能提供了证据。我们的研究结果展示了基因组中的寄生元件如何逃避宿主的防御机制。此外，我们对 miR820 调控 OsDRM2 的分析揭示了转座子衍生的小 RNA 的作用，不仅作为宿主基因组的防御机制，而且作为宿主与其寄生元件之间相互作用的调节剂。
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