Abstract
Small RNAs are central players in RNA silencing, yet their cytoplasmic compartmentalization and the effects it may have on their activities have not been studied at the genomic scale. Here we report that Arabidopsis microRNAs (miRNAs) and small interfering RNAs (siRNAs) are distinctly partitioned between the endoplasmic reticulum (ER) and cytosol. All miRNAs are associated with membrane-bound polysomes (MBPs) as opposed to polysomes in general. The MBP association is functionally linked to a deeply conserved and tightly regulated activity of miRNAs - production of phased siRNAs (phasiRNAs) from select target RNAs. The phasiRNA precursor RNAs, thought to be noncoding, are on MBPs and are occupied by ribosomes in a manner that supports miRNA-triggered phasiRNA production, suggesting that ribosomes on the rough ER impact siRNA biogenesis. This study reveals global patterns of cytoplasmic partitioning of small RNAs and expands the known functions of ribosomes and ER.
Highlights
RNA silencing is a conserved posttranscriptional gene regulatory mechanism in eukaryotes
We found that the integral endoplasmic reticulum (ER) membrane protein AMP1 is required for the translational repression activity of plant miRNAs, suggesting that the rough ER is the site of miRNA-mediated translational repression (Li et al, 2013)
A few miRNAs and their target transcripts were found to be associated with membrane-bound polysomes (MBPs) (Li et al, 2013), but the scale of the MBP-association of miRNAs and their target transcripts was unknown
Summary
RNA silencing is a conserved posttranscriptional gene regulatory mechanism in eukaryotes. Many observations document the membrane association of plant and animal AGO proteins (Brodersen et al, 2012; Cikaluk et al, 1999; Gibbings et al, 2009; Jouannet et al, 2012; Lee et al, 2009; Li et al, 2013; Stalder et al, 2013; Wu et al, 2013), but the cytoplasmic location where miRNAs or siRNAs repress target RNAs is largely unexplored and is perhaps presumed to be the cytosol. A well-documented feature of RNA silencing in plants and C. elegans is signal amplification, in which primary siRNAs from transgenes or viruses guide the production of secondary siRNAs from target RNAs through the activities of RNA-dependent RNA polymerases (RdRP)
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