Widespread regulation of the maternal transcriptome by Nanos in Drosophila.

The translational repressor Nanos (Nos) regulates a single target, maternal hunchback ( hb) mRNA, to govern abdominal segmentation in the early Drosophila embryo. Nos is recruited specifically to sites in the 3'-UTR of hb mRNA in collaboration with the sequence-specific RNA-binding protein Pumilio (Pum); on its own, Nos has no binding specificity. Nos is expressed at other stages of development, but very few mRNA targets that might mediate its action at these stages have been described. Nor has it been clear whether Nos is targeted to other mRNAs in concert with Pum or via other mechanisms. In this report, we identify mRNAs targeted by Nos using an unorthodox approach, expressing a chimera bearing Nos fused to the nonsense mediated decay (NMD) factor Upf1, which directs mRNA degradation. We find that, in addition to hb , Upf1-Nos depletes thousands of mRNAs from the maternal transcriptome in early embryos. Virtually all of these appear to be targeted in a canonical, hb -like manner in concert with Pum. The mRNAs targeted by Upf1-Nos are hypo-adenylated and inefficiently translated at the ovary-embryo transition; many of these mRNAs are subsequently degraded in a Nos-dependent manner in the embryo after the onset of zygotic transcription. We suggest that a late ovarian burst of Nos represses a large portion of the maternal transcriptome, priming it for later degradation by other factors during the maternal-zygotic transition in the embryo.