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piRNA-guided slicing specifies transcripts for Zucchini-dependent, phased piRNA biogenesis

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Science  15 May 2015:
Vol. 348, Issue 6236, pp. 812-817
DOI: 10.1126/science.aaa1039

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Spreading small RNAs to protect the genome

In animals, PIWI-interacting RNAs (piRNAs) are small noncoding RNAs that protect our germ lines from the ravages of transposons. To do this, piRNAs target and cleave transposon RNAs. Synthesis of piRNA is initiated by a cut made in a long, single-stranded precursor RNA. The piRNAs can also undergo a self-perpetuating amplification cycle (see the Perspective by Siomi and Siomi). Han et al. and Mohn et al. now reveal that piRNA biogenesis can also spread in a strictly phased manner from the site of initial piRNA formation. Spreading piRNA synthesis greatly increases their sequence diversity, potentially helping them to target endogenous and novel transposons more effectively.

Science, this issue p. 817, p. 812; see also p. 756

Abstract

In animal gonads, PIWI-clade Argonaute proteins repress transposons sequence-specifically via bound Piwi-interacting RNAs (piRNAs). These are processed from single-stranded precursor RNAs by largely unknown mechanisms. Here we show that primary piRNA biogenesis is a 3′-directed and phased process that, in the Drosophila germ line, is initiated by secondary piRNA-guided transcript cleavage. Phasing results from consecutive endonucleolytic cleavages catalyzed by Zucchini, implying coupled formation of 3′ and 5′ ends of flanking piRNAs. Unexpectedly, Zucchini also participates in 3′ end formation of secondary piRNAs. Its function can, however, be bypassed by downstream piRNA-guided precursor cleavages coupled to exonucleolytic trimming. Our data uncover an evolutionarily conserved piRNA biogenesis mechanism in which Zucchini plays a central role in defining piRNA 5′ and 3′ ends.

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