Dataset Information

The comprehensive epigenome map of piRNA clusters.

ABSTRACT: PIWI-interacting RNA (piRNA) clusters act as anti-transposon/retrovirus centers. Integration of selfish jumping elements into piRNA clusters generates de novo piRNAs, which in turn exert trans-silencing activity against these elements in animal gonads. To date, neither genome-wide chromatin modification states of piRNA clusters nor a mode for piRNA precursor transcription have been well understood. Here, to understand the chromatin landscape of piRNA clusters and how piRNA precursors are generated, we analyzed the transcriptome, transcription start sites (TSSs) and the chromatin landscape of the BmN4 cell line, which harbors the germ-line piRNA pathway. Notably, our epigenomic map demonstrated the highly euchromatic nature of unique piRNA clusters. RNA polymerase II was enriched for TSSs that transcribe piRNA precursors. piRNA precursors possessed 5'-cap structures as well as 3'-poly A-tails. Collectively, we envision that the euchromatic, opened nature of unique piRNA clusters or piRNA cluster-associated TSSs allows piRNA clusters to capture new insertions efficiently.

SUBMITTER: Kawaoka S

PROVIDER: S-EPMC3561999 | biostudies-literature | 2013 Feb

REPOSITORIES: biostudies-literature

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The comprehensive epigenome map of piRNA clusters.

Kawaoka Shinpei S Hara Kahori K Shoji Keisuke K Kobayashi Maki M Shimada Toru T Sugano Sumio S Tomari Yukihide Y Suzuki Yutaka Y Katsuma Susumu S

Nucleic acids research 20121220 3

PIWI-interacting RNA (piRNA) clusters act as anti-transposon/retrovirus centers. Integration of selfish jumping elements into piRNA clusters generates de novo piRNAs, which in turn exert trans-silencing activity against these elements in animal gonads. To date, neither genome-wide chromatin modification states of piRNA clusters nor a mode for piRNA precursor transcription have been well understood. Here, to understand the chromatin landscape of piRNA clusters and how piRNA precursors are generat ...[more]

PMID: 23258708

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Project description:Animal genomes are parasitized by a horde of transposable elements (TEs) whose mutagenic activity can have catastrophic consequences. The piRNA pathway is a conserved mechanism to repress TE activity in the germline via a specialized class of small RNAs associated with effector Piwi proteins called piwi-associated RNAs (piRNAs). piRNAs are produced from discrete genomic regions called piRNA clusters (piCs). While piCs are generally enriched for TE sequences and the molecular processes by which they are transcribed and regulated are relatively well understood in Drosophila melanogaster , much less is known about the origin and evolution of piCs in this or any other species. To investigate piC evolution, we use a population genomics approach to compare piC activity and sequence composition across 8 geographically distant strains of D. melanogaster with high quality long-read genome assemblies. We perform extensive annotations of ovary piCs and TE content in each strain and test predictions of two proposed models of piC evolution. The 'de novo' model posits that individual TE insertions can spontaneously attain the status of a small piC to generate piRNAs silencing the entire TE family. The 'trap' model envisions large and evolutionary stable genomic clusters where TEs tend to accumulate and serves as a long-term "memory" of ancient TE invasions and produce a great variety of piRNAs protecting against related TEs entering the genome. It remains unclear which model best describes the evolution of piCs. Our analysis uncovers extensive variation in piC activity across strains and signatures of rapid birth and death of piCs in natural populations. Most TE families inferred to be recently or currently active show an enrichment of strain-specific insertions into large piCs, consistent with the trap model. By contrast, only a small subset of active LTR retrotransposon families is enriched for the formation of strain-specific piCs, suggesting that these families have an inherent proclivity to form de novo piCs. Thus, our findings support aspects of both 'de novo' and 'trap' models of piC evolution. We propose that these two models represent two extreme stages along an evolutionary continuum, which begins with the emergence of piCs de novo from a few specific LTR retrotransposon insertions that subsequently expand by accretion of other TE insertions during evolution to form larger 'trap' clusters. Our study shows that piCs are evolutionarily labile and that TEs themselves are the major force driving the formation and evolution of piCs.

Dataset Information

The comprehensive epigenome map of piRNA clusters.

Publications

The comprehensive epigenome map of piRNA clusters.

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