RNA triple helix assembled by the poly(A) tail enhances retrotransposon mobilization by preventing RNA deadenylation

Abstract

Transposable elements (TEs), ubiquitous mobile DNAs, are largely repressed by cellular mechanisms such as epigenetic silencing and RNA decay, yet some retain the ability to transpose. The Arabidopsis long terminal repeat retrotransposon Copia93 , also known as Evade , exhibits exceptionally high transpositional activity, but the mechanism underlying its extraordinary mobility remains unclear. Here, we identify an Element for Nuclear Expression (ENE) motif within the 3′ UTR of Evade that forms a triple helical RNA structure with the poly(A) tail, shielding the transcript from deadenylation and degradation. Deletion of the ENE motif significantly reduces Evade transcript stability, extrachromosomal DNA levels, and de novo insertions. Furthermore, we show that the mRNA deadenylase CCR4a directly binds Evade RNA to shorten its poly(A) tail, thereby suppressing transposition. Loss of CCR4a leads to Evade upregulation, while additional deadenylases contribute to its repression in the absence of CCR4a. Our findings uncover an RNA-based strategy that enhances transposon stability and mobility, illustrating a coevolutionary arms race between host silencing pathways and TE-encoded structural elements.