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Transgenerationally inherited piRNAs trigger piRNA biogenesis by changing the chromatin of piRNA clusters and inducing precursor processing

Le Thomas, Adrien and Stuwe, Evelyn and Li, Sisi and Du, Jiamu and Marinov, Georgi K. and Rozhkov, Nikolay V. and Chen, Yung-Chia Ariel and Luo, Yucheng and Sachidanandam, Ravi and Fejes Toth, Katalin and Patel, Dinshaw and Aravin, Alexei A. (2014) Transgenerationally inherited piRNAs trigger piRNA biogenesis by changing the chromatin of piRNA clusters and inducing precursor processing. Genes and Development, 28 (15). pp. 1667-1680. ISSN 0890-9369. PMCID PMC4117942.

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Small noncoding RNAs that associate with Piwi proteins, called piRNAs, serve as guides for repression of diverse transposable elements in germ cells of metazoa. In Drosophila, the genomic regions that give rise to piRNAs, the so-called piRNA clusters, are transcribed to generate long precursor molecules that are processed into mature piRNAs. How genomic regions that give rise to piRNA precursor transcripts are differentiated from the rest of the genome and how these transcripts are specifically channeled into the piRNA biogenesis pathway are not known. We found that transgenerationally inherited piRNAs provide the critical trigger for piRNA production from homologous genomic regions in the next generation by two different mechanisms. First, inherited piRNAs enhance processing of homologous transcripts into mature piRNAs by initiating the ping-pong cycle in the cytoplasm. Second, inherited piRNAs induce installment of the histone 3 Lys9 trimethylation (H3K9me3) mark on genomic piRNA cluster sequences. The heterochromatin protein 1 (HP1) homolog Rhino binds to the H3K9me3 mark through its chromodomain and is enriched over piRNA clusters. Rhino recruits the piRNA biogenesis factor Cutoff to piRNA clusters and is required for efficient transcription of piRNA precursors. We propose that transgenerationally inherited piRNAs act as an epigenetic memory for identification of substrates for piRNA biogenesis on two levels: by inducing a permissive chromatin environment for piRNA precursor synthesis and by enhancing processing of these precursors.

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URLURL TypeDescription DOIArticle Material CentralArticle
Marinov, Georgi K.0000-0003-1822-7273
Fejes Toth, Katalin0000-0001-6558-2636
Additional Information:© 2014 Le Thomas et al.; Published by Cold Spring Harbor Laboratory Press. This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at Received May 14, 2014; revised version accepted July 9, 2014. We thank members of the Aravin laboratory for discussion.We are grateful to the staff at beamline 24-ID-E at the Argonne National Laboratory and beamline X29A at the Brookhaven National Laboratory for support in diffraction data collection. E.S. is supported by a Ph.D. fellowship of the Boehringer Ingelheim Fonds. This work was supported by grants from the National Institutes of Health (R00 HD057233, R01 GM097363, and DP2 OD007371A) and by the Searle Scholar and the Packard Fellowship Awards to A.A.A., and by funds from the Abby Rockefeller Mauze Trust, Maloris Foundation, and Starr Foundation to D.P.
Funding AgencyGrant Number
Boehringer Ingelheim FondsUNSPECIFIED
NIHR00 HD057233
NIHR01 GM097363
NIHDP2 OD007371A
Searle Scholars ProgramUNSPECIFIED
David and Lucile Packard FoundationUNSPECIFIED
Abby Rockefeller Mauze TrustUNSPECIFIED
Maloris FoundationUNSPECIFIED
Starr FoundationUNSPECIFIED
Subject Keywords:H3K9me3; epigenetics; piRNA
Issue or Number:15
PubMed Central ID:PMC4117942
Record Number:CaltechAUTHORS:20140807-085550951
Persistent URL:
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:48167
Deposited By: Jason Perez
Deposited On:07 Aug 2014 22:49
Last Modified:09 Mar 2020 13:18

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