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Putzig safeguards genome integrity by contributing to the Piwi-mediated repression of transposon activity in the female germline of Drosophila in a two-tiered fashion

ABSTRACT: Genome integrity in the germline is jeopardized by the activity of transposable elements (TEs). Transposon activity is kept in check by the Piwi-piRNA pathway, which silences TEs post-transcriptionally in the cytoplasm as well as co-transcriptionally in the nucleus. piRNAs derive from long precursor transcripts originating at piRNA-loci by non-conventional transcription. They are processed in the cytoplasm and loaded into Piwi-piRNA complexes that then enter the nucleus to bind to the target RNA and direct local heterochromatin formation at TE loci, involving several downstream effectors. In this work, we have analyzed the role of Putzig (Pzg) in Piwi-mediated TE silencing in the female germline. Pzg has multi-facetted roles during Drosophila development and is important for DNA integrity, germ cell differentiation and survival. Here, we provide evidence for a two-tier activity of Pzg by serving as a hub for various Piwi-pathway members. Firstly, Pzg assists transcription initiation at piRNA clusters by coupling the Trf2-Moonshiner transcription initiation complex to the Rhino-Deadlock-Cutoff complex, thereby promoting formation of piRNA-precursor transcripts. Secondly, in the context of co-transcriptional gene silencing, Pzg licences heterochromatin formation by linking the Piwi-piRNA silencing machinery and the histone demethylase Lsd1, involved in promoter inactivation.

INSTRUMENT(S):

ORGANISM(S): Drosophila Melanogaster (fruit Fly)

TISSUE(S): Ovary

SUBMITTER: Lea Hüttinger

LAB HEAD: Anja Nagel

PROVIDER: PXD075330 | Pride | 2026-03-11

REPOSITORIES: Pride

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Dynamic co-evolution of transposable elements and the piRNA pathway in East African cichlid fishes

Project description:East African cichlid fishes have radiated in an explosive fashion. The (epi)genetic basis for the abundant phenotypic diversity of these fishes remains largely unknown. As transposable elements (TEs) contribute extensively to genome evolution, we reasoned that TEs may have fuelled cichlid radiations. While TE-derived genetic and epigenetic variability has been associated with phenotypic traits, TE expression and epigenetic silencing remain unexplored in cichlids. Here, we profiled TE expression in African cichlids, and describe dynamic expression patterns during embryogenesis and according to sex. Most TE silencing factors are conserved and expressed in cichlids. We describe an expansion of two truncated Piwil1 genes in Lake Malawi/Nyasa cichlids, encoding a Piwi domain with catalytic potential. To further dissect epigenetic silencing of TEs, we focused on small RNA-driven epigenetic silencing. We detect a small RNA population in gonads consistent with an active Piwi-interacting RNA (piRNA) pathway targeting TEs. We uncover fluid genomic origins of piRNAs in closely related cichlid species. This, along with signatures of positive selection in piRNA pathway factors, points towards fast co-evolution of TEs and the piRNA pathway. Our study is the first step to understand the contribution of ongoing TE-host arms races to the cichlid radiations in Africa.

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Project description:Transposable element (TE) silencing in the germline is crucial for preserving genome integrity; its absence results in sterility and diminished developmental robustness. The Piwi-interacting RNA (piRNA) pathway is the primary small non-coding RNA mechanism by which TEs are silenced in the germline. Three piRNA binding proteins promote the piRNA pathway function in the germline– P-element-induced wimpy testis (Piwi), Aubergine (Aub), and Argonaute 3 (Ago3). Piwi mediates transcriptional silencing of TEs by promoting the deposition of the heterochromatin mark Histone 3 lysine nine trimethylation (H3K9me3) at TE genomic sites. Aub and Ago3 facilitate post-transcriptional silencing of TEs. Proteins and mechanisms that promote piRNA function in TE silencing are still being discovered. This study demonstrates that the Drosophila Modulo protein, a homolog of mammalian Nucleolin and an epigenetic regulator, is crucial for the enrichment of H3K9me3 at TEs. We show that Modulo interacts with Piwi and operates downstream of the Piwi-piRNA complex's entry into the nucleus. Lack of Modulo function impairs Piwi-interacting protein Panoramix's ability to target transposon RNAs. Furthermore, the reduced function of Modulo in the mother undermines developmental robustness and exacerbates neomorphic Kr[If-1]-induced ectopic eye outgrowths in the offspring. Maternal Modulo enhances developmental robustness by inhibiting TE activation and transcriptome variability associated with intrinsic genetic variation. Thus, Modulo is an essential component of the mechanism that operates in the maternal germline to facilitate TE silencing and ensure developmental robustness in the ensuing generation.

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Project description:The control of transposable element (TE) activity in germ cells provides genome integrity over generations. A distinct small RNA-mediated pathway utilizing Piwi-interacting RNAs (piRNAs) suppresses TE expression in gonads of metazoans. In the fly, primary piRNAs derive from so-called piRNA clusters, which are enriched in damaged repeated sequences. These piRNAs launch a cycle of TE and piRNA cluster transcript cleavages resulting in the amplification of piRNA and TE silencing. Using genome-wide comparison of TE insertions and ovarian small RNA libraries from two Drosophila strains, we found that individual TEs inserted into euchromatic loci form novel dual-stranded piRNA clusters. Formation of the piRNA-generating loci by active individual TEs provides a more potent silencing response to the TE expansion. Like all piRNA clusters, individual TEs are also capable of triggering the production of endogenous small interfering (endo-si) RNAs. Small RNA production by individual TEs spreads into the flanking genomic regions including coding cellular genes. We show that formation of TE-associated small RNA clusters can down-regulate expression of nearby genes in ovaries. Integration of TEs into the 3' untranslated region of actively transcribed genes induces piRNA production towards the 3'-end of transcripts, causing the appearance of genic piRNA clusters, a phenomenon that has been reported in different organisms. These data suggest a significant role of TE-associated small RNAs in the evolution of regulatory networks in the germline. The fractions of small RNAs (19-29 nt) from ovaries of y[1]; cn[1] bw[1] sp[1] line of Drosophila melanogaster were sequenced using Illumina HiSeq 2000.

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putzig safeguards genome integrity by contributing to the Piwi-mediated repression of transposon activity in the female germline of Drosophila in a two-tiered fashion

Project description:Genome integrity in the germline is jeopardized by the activity of transposable elements (TEs). Transposon activity is kept in check by the Piwi-piRNA pathway, which silences TEs post-transcriptionally in the cytoplasm as well as co-transcriptionally in the nucleus. piRNAs derive from long precursor transcripts originating at piRNA-loci by non-conventional transcription. They are processed in the cytoplasm and loaded into Piwi-piRNA complexes that then enter the nucleus to bind to the target RNA and direct local heterochromatin formation at TE loci, involving several downstream effectors. In this work, we have analyzed the role of Putzig (Pzg) in Piwi-mediated TE silencing in the female germline. Pzg has multi-facetted roles during Drosophila development and is important for DNA integrity, germ cell differentiation and survival. Here, we provide evidence for a two-tier activity of Pzg by serving as a hub for various Piwi-pathway members. Firstly, Pzg assists transcription initiation at piRNA clusters by coupling the Trf2-Moonshiner transcription initiation complex to the Rhino-Deadlock-Cutoff complex, thereby promoting formation of piRNA-precursor transcripts. Secondly, in the context of co-transcriptional gene silencing, Pzg licences heterochromatin formation by linking the Piwi-piRNA silencing machinery and the histone demethylase Lsd1, involved in promoter inactivation.

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