Role of Transposon-Derived Small RNAs in the Interplay between Genomes and Parasitic DNA in Rice

Abstract

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. Transposons, which are sometimes referred to as “genomic parasites,” are a major component of eukaryotic genomes. Because transposon activity is often detrimental to host genome stability, most transposons are silenced by the host's defense machinery. The mechanisms of transposon silencing, such as RNA silencing, have been well investigated, but virtually nothing is known about the strategies that transposons have evolved to avoid silencing. In this paper, we demonstrate that a microRNA (miRNA) produced from a transposon suppresses the host's silencing machinery. Generally, small interfering RNAs (siRNAs) produced from transposons trigger silencing of those transposon loci; however, in this case, transposons escape host silencing by producing miRNA. Our analysis provides evidence for a novel mechanism by which transposons reduce host silencing, and it elucidates the front line of host genome–parasitic DNA interaction through the action of two types of small RNAs, siRNA and miRNA, produced from transposons.