Maelstrom Represses Canonical Polymerase II Transcription within Bi-directional piRNA Clusters in Drosophila melanogaster

Chang, Timothy H.; Mattei, Eugenio; Gainetdinov, Ildar; Colpan, Cansu; Weng, Zhiping; Zamore, Phillip D.

doi:10.1016/j.molcel.2018.10.038

Cited by 36 publications

(42 citation statements)

References 89 publications

(117 reference statements)

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“…Competition between canonical and non-canonical transcription appears have a central role in controlling piRNA biogenesis (Andersen et al, 2017;Chang et al, 2019), and is particularly critical to piRNA production from euchromatic transposon insertions. The majority of germline clusters do not have flaking canonical promoters, and CtBP knock down does not significantly alter piRNA production from these loci.…”

Section: Sim-cuff Captures Pirna Precursor Transcription Factorsmentioning

confidence: 99%

“…Formation of these "mini-clusters", through an uncharacterized epigenetic mechanism, provides an independent adaptation mechanism. In Drosophila, germline piRNA clusters and transposon mini-clusters are bound by the RDC complex, which is composed of the HP1 homolog Rhino (Rhi), which co-localizes with the linker protein Deadlock (Del) and the Rai1 homolog Cutoff (Cuff) (Chang et al, 2019;Chen et al, 2016; Le Thomas et al, 2014;Mohn et al, 2014;Pane et al, 2011;Parhad et al, 2017;Yu et al, 2015;Zhang et al, 2018;Zhang et al, 2014). The three components of the RDC are co-dependent for localization to clusters, and essential to germline piRNA production.…”

Section: Introductionmentioning

confidence: 99%

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Adaptive evolution targets a piRNA precursor transcription network

Parhad

Zhang

et al. 2019

Preprint

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In Drosophila, transposon-silencing piRNAs are derived from heterochromatic clusters and a subset of euchromatic transposon insertions, which are transcribed from internal non-canonical initiation sites and flanking canonical promoters. Rhino binds to Deadlock, which recruits TRF2 to promote non-canonical transcription of these loci. Cuff co-localizes with Rhino and Del. The role of Cuff is less well understood, but the cuff gene shows hallmarks of adaptive evolution, which frequently targets functional interactions within host defense systems. We show that Drosophila simulans cuff is a dominant negative allele when expressed in Drosophila melanogaster, where it traps Deadlock, TRF2 and the transcriptional co-repressor CtBP in stable nuclear complexes. Cuff promotes Rhino and Deadlock localization, driving non-canonical transcription. CtBP, by contrast, suppresses canonical cluster and transposon transcription, which interferes with downstream non-canonical transcription and piRNA production. Cuff, TRF2 and CtBP thus form a network that balances canonical and non-canonical piRNA precursor transcription.

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Section: Sim-cuff Captures Pirna Precursor Transcription Factorsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Adaptive evolution targets a piRNA precursor transcription network

Parhad

Zhang

et al. 2019

Preprint

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“…This suggests that the role of Mael is different from that of other Piwi cofactors. A recent study showed that Mael represses canonical transcription in the germ line by piRNA-dependent and piRNAindependent processes (19). However, the functions of Mael in these pathways remain unclear.…”

Section: Introductionmentioning

confidence: 99%

Piwi suppresses transcription of Brahma-dependent transposons via Maelstrom in ovarian somatic cells

et al. 2020

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Drosophila Piwi associates with PIWI-interacting RNAs (piRNAs) and represses transposons transcriptionally through heterochromatinization; however, this process is poorly understood. Here, we identify Brahma (Brm), the core adenosine triphosphatase of the SWI/SNF chromatin remodeling complex, as a new Piwi interactor, and show Brm involvement in activating transcription of Piwi-targeted transposons before silencing. Bioinformatic analyses indicated that Piwi, once bound to target RNAs, reduced the occupancies of SWI/SNF and RNA polymerase II (Pol II) on target loci, abrogating transcription. Artificial piRNA-driven targeting of Piwi to RNA transcripts enhanced repression of Brm-dependent reporters compared with Brm-independent reporters. This was dependent on Piwi cofactors, Gtsf1/Asterix (Gtsf1), Panoramix/Silencio (Panx), and Maelstrom (Mael), but not Eggless/dSetdb (Egg)–mediated H3K9me3 deposition. The λN-box B–mediated tethering of Mael to reporters repressed Brm-dependent genes in the absence of Piwi, Panx, and Gtsf1. We propose that Piwi, via Mael, can rapidly suppress transcription of Brm-dependent genes to facilitate heterochromatin formation.

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“…The chromatin of piRNA clusters is enriched in a common heterochromatic histone mark, trimethylated lysine 9 of histone H3 (H3K9me3) and by two chromodomain-containing proteins, heterochromatic protein 1 (HP1) and its germline-specific ortholog Rhino (Rhi) [4,7,8,9]. The protein Maelstrom represses canonical transcription from TEs and neighbouring gene promoters in dual-strand piRNA clusters [10]. Instead, noncanonical convergent transcription from both genomic strands initiated at multiple random sites facilitates the transcription of piRNA precursors from dual strand piRNA clusters [6,7].…”

Section: Introductionmentioning

confidence: 99%

The Integrity of piRNA Clusters is Abolished by Insulators in the Drosophila Germline

Radion

Ryazansky

Komarov

et al. 2019

Genes

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Piwi-interacting RNAs (piRNAs) control transposable element (TE) activity in the germline. piRNAs are produced from single-stranded precursors transcribed from distinct genomic loci, enriched by TE fragments and termed piRNA clusters. The specific chromatin organization and transcriptional regulation of Drosophila germline-specific piRNA clusters ensure transcription and processing of piRNA precursors. TEs harbour various regulatory elements that could affect piRNA cluster integrity. One of such elements is the suppressor-of-hairy-wing (Su(Hw))-mediated insulator, which is harboured in the retrotransposon gypsy. To understand how insulators contribute to piRNA cluster activity, we studied the effects of transgenes containing gypsy insulators on local organization of endogenous piRNA clusters. We show that transgene insertions interfere with piRNA precursor transcription, small RNA production and the formation of piRNA cluster-specific chromatin, a hallmark of which is Rhino, the germline homolog of the heterochromatin protein 1 (HP1). The mutations of Su(Hw) restored the integrity of piRNA clusters in transgenic strains. Surprisingly, Su(Hw) depletion enhanced the production of piRNAs by the domesticated telomeric retrotransposon TART, indicating that Su(Hw)-dependent elements protect TART transcripts from piRNA processing machinery in telomeres. A genome-wide analysis revealed that Su(Hw)-binding sites are depleted in endogenous germline piRNA clusters, suggesting that their functional integrity is under strict evolutionary constraints.

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Maelstrom Represses Canonical Polymerase II Transcription within Bi-directional piRNA Clusters in Drosophila melanogaster

Abstract: Highlights d Maelstrom represses canonical transcription within fly dualstrand piRNA clusters d Maelstrom also represses canonical transcription in conventional heterochromatin d Maelstrom can be guided to its targets both by piRNAs and piRNA-independent mechanisms

Cited by 36 publications

References 89 publications

Adaptive evolution targets a piRNA precursor transcription network

Adaptive evolution targets a piRNA precursor transcription network

Piwi suppresses transcription of Brahma-dependent transposons via Maelstrom in ovarian somatic cells

The Integrity of piRNA Clusters is Abolished by Insulators in the Drosophila Germline

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