Overview
piRNAs keep Nanos in check
Small RNAs of the piRNA (Piwi-associated RNA) class have various functions in the germline — repressing transposable elements, maintaining germline stem cells and promoting genome stability. Rouget
et al
. have now uncovered a function for piRNAs outside the germline, in the fruit fly embryo. Specifically, piRNAs that are complementary to a sequence in the 3′-untranslated region of an mRNA for the embryonic posterior morphogen Nanos facilitate adenylation of the mRNA and its subsequent decay. Without piRNAs, Nanos accumulates and developmental defects result.
Piwi-associated RNAs (piRNAs) are small RNAs with several functions in the germline, such as repressing transposable elements and helping to maintain germline stem cells. Now, a function for piRNAs has been discovered outside the germline, in the fruitfly embryo. Specifically, piRNAs are required for the decay of the messenger RNA encoding the posterior morphogen Nanos. When piRNA-induced regulation is impaired, this mRNA is stabilized and developmental defects ensue.
Piwi-associated RNAs (piRNAs), a specific class of 24- to 30-nucleotide-long RNAs produced by the Piwi-type of Argonaute proteins, have a specific germline function in repressing transposable elements. This repression is thought to involve heterochromatin formation and transcriptional and post-transcriptional silencing
1
,
2
,
3
,
4
,
5
,
6
. The piRNA pathway has other essential functions in germline stem cell maintenance
7
and in maintaining germline DNA integrity
8
,
9
,
10
. Here we uncover an unexpected function of the piRNA pathway in the decay of maternal messenger RNAs and in translational repression in the early embryo. A subset of maternal mRNAs is degraded in the embryo at the maternal-to-zygotic transition. In
Drosophila
, maternal mRNA degradation depends on the RNA-binding protein Smaug and the deadenylase CCR4
11
,
12
,
13
, as well as the zygotic expression of a microRNA cluster
14
. Using mRNA encoding the embryonic posterior morphogen Nanos (Nos) as a paradigm to study maternal mRNA decay, we found that CCR4-mediated deadenylation of
nos
depends on components of the piRNA pathway including piRNAs complementary to a specific region in the
nos
3′ untranslated region. Reduced deadenylation when piRNA-induced regulation is impaired correlates with
nos
mRNA stabilization and translational derepression in the embryo, resulting in head development defects. Aubergine, one of the Argonaute proteins in the piRNA pathway, is present in a complex with Smaug, CCR4,
nos
mRNA and piRNAs that target the
nos
3′ untranslated region, in the bulk of the embryo. We propose that piRNAs and their associated proteins act together with Smaug to recruit the CCR4 deadenylation complex to specific mRNAs, thus promoting their decay. Because the piRNAs involved in this regulation are produced from transposable elements, this identifies a direct developmental function for transposable elements in the regulation of gene expression.
