In plants, decapping prevents RDR6-dependent production of small interfering RNAs from endogenous mRNAs

Background: Cytoplasmic degradation of endogenous RNAs is an integral part of RNA quality control (RQC) and often relies on the removal of the 5'' cap structure and their subsequent 5' to 3' degradation. In parallel, many eukaryotes degrade exogenous and selected endogenous RNAs through post-transcriptional gene silencing (PTGS). In plants, PTGS depends on small interfering (si)RNAs produced after the conversion of single-stranded RNAs to double-stranded RNAs by the cellular RNA DEPENDENT RNA POLYMERASE 6 (RDR6). PTGS and RQC compete for transgene-derived RNAs, but it is unknown whether this competition also occurs for endogenous transcripts. Results: We show that that upon decapping impairment hundreds of endogenous mRNAs give rise to a new class of siRNAs, a subset of which depends on RDR6 for their production. Conclusions: Our results suggest that the decapping of aberrant endogenous RNA in P-bodies limits their entry into the PTGS pathway and prevents the subsequent deleterious consequences arising from this entry. We anticipate that the siRNAs identified in decapping mutants represent a subset of a larger ensemble of endogenous siRNAs that we coin rqc-siRNAs because they accumulate when RQC processes are impaired. Overall design: Small RNA-seq experiments performed in duplicates for each condition.