The posttranscriptional addition of nucleotides to the 3′ end of RNA regulates the maturation, function, and stability of RNA species in all domains of life. Here, we show that in flies, 3′ terminal RNA uridylation triggers the processive, 3′‐to‐5′ exoribonucleolytic decay via the RNase II/R enzyme CG16940, a homolog of the human Perlman syndrome exoribonuclease Dis3l2. Together with the TUTase Tailor, dmDis3l2 forms the cytoplasmic, terminal RNA uridylation‐mediated processing (TRUMP) complex that functionally cooperates in the degradation of structured RNA. RNA immunoprecipitation and high‐throughput sequencing reveals a variety of TRUMP complex substrates, including abundant non‐coding RNA, such as 5S rRNA, tRNA, snRNA, snoRNA, and the essential RNase MRP. Based on genetic and biochemical evidence, we propose a key function of the TRUMP complex in the cytoplasmic quality control of RNA polymerase III transcripts. Together with high‐throughput biochemical characterization of dmDis3l2 and bacterial RNase R, our results imply a conserved molecular function of RNase II/R enzymes as “readers” of destabilizing posttranscriptional marks—uridylation in eukaryotes and adenylation in prokaryotes—that play important roles in RNA surveillance.
The identification of an enzyme complex degrading aberrant RNA in flies deepens our understanding of cytoplasmic RNA surveillance and sheds light on the emerging role for RNA modifications.
This work reports the identification of a cytoplasmic terminal RNA uridylation‐mediated processing (TRUMP) complex in Drosophila.
The TRUMP complex regulates precursor‐microRNA maturation in flies.
The TRUMP complex degrades aberrant, structured, cellular non‐coding RNA.
The TRUMP complex functions in the quality control of RNA polymerase III transcripts.
RNase II/R enzymes act as conserved molecular readers of evolutionarily divergent epitranscriptomic marks.
- Received July 20, 2016.
- Revision received September 10, 2016.
- Accepted September 14, 2016.
- © 2016 The Authors