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piRNA-guided transposon cleavage initiates Zucchini-dependent, phased piRNA production

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Science  15 May 2015:
Vol. 348, Issue 6236, pp. 817-821
DOI: 10.1126/science.aaa1264

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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

PIWI-interacting RNAs (piRNAs) protect the animal germ line by silencing transposons. Primary piRNAs, generated from transcripts of genomic transposon “junkyards” (piRNA clusters), are amplified by the “ping-pong” pathway, yielding secondary piRNAs. We report that secondary piRNAs, bound to the PIWI protein Ago3, can initiate primary piRNA production from cleaved transposon RNAs. The first ~26 nucleotides (nt) of each cleaved RNA becomes a secondary piRNA, but the subsequent ~26 nt become the first in a series of phased primary piRNAs that bind Piwi, allowing piRNAs to spread beyond the site of RNA cleavage. The ping-pong pathway increases only the abundance of piRNAs, whereas production of phased primary piRNAs from cleaved transposon RNAs adds sequence diversity to the piRNA pool, allowing adaptation to changes in transposon sequence.

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