Cytoplasmic polyadenylation is a widespread mechanism to regulate mRNA translation. In vertebrates, this process requires two sequence elements in target 3' UTRs: the U-rich cytoplasmic polyadenylation element and the AAUAAA hexanucleotide. In Drosophila melanogaster, cytoplasmic polyadenylation of Toll mRNA occurs independently of these canonical elements and requires a machinery that remains to be characterized. Here we identify Dicer-2 as a component of this machinery. Dicer-2, a factor previously involved in RNA interference (RNAi), interacts with the cytoplasmic poly(A) polymerase Wispy. Depletion of Dicer-2 from polyadenylation-competent embryo extracts and analysis of wispy mutants indicate that both factors are necessary for polyadenylation and translation of Toll mRNA. We further identify r2d2 mRNA, encoding a Dicer-2 partner in RNAi, as a Dicer-2 polyadenylation target. Our results uncover a novel function of Dicer-2 in activation of mRNA translation through cytoplasmic polyadenylation.

This work was supported by MINECO and the European Regional Development Fund (ERDF) under BFU2012-37135, BFU2015-68741, and Consolider CSD2009-00080 grants to F.G., and by the CNRS UMR9002, ANR (ANR-2010-BLAN-1201-01 and ANR-15-CE12-0019-01), and FRM (Equipe FRM 2013 DEQ20130326534) to M.S. We acknowledge support of MINECO “Centro de Excelencia Severo Ochoa 2013-2017,” SEV-2012-0208.