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The transcription factor Traffic jam orchestrates the somatic piRNA pathway in Drosophila ovaries [RNA-seq]

ABSTRACT: The PIWI-interacting RNA (piRNA) pathway is essential for transposable element (TE) silencing in animal gonads. While the transcriptional regulation of piRNA pathway components in germ cells has been documented in mice and flies, their control in somatic cells of Drosophila ovaries remains unresolved. Here, we demonstrate that Traffic jam (Tj), the Drosophila orthologue of large Maf transcription factors in mammals, is a master regulator of the somatic piRNA pathway. Tj binds to regulatory regions of somatic piRNA factors and the major piRNA cluster flamenco, which carries a Tj-bound enhancer downstream of its promoter. Depletion of Tj in somatic follicle cells causes downregulation of piRNA factors, loss of flam expression and de-repression of gypsy-family TEs. We propose that the arms race between the host and TEs led to the co-evolution of promoters in piRNA pathway genes as well as TE regulatory regions that both rely on a shared transcription factor.

ORGANISM(S): Drosophila melanogaster

PROVIDER: GSE287891 | GEO | 2026/01/23

REPOSITORIES: GEO

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Transcriptional factor Tj is the master regulator of the somatic piRNA pathway in the Drosophila ovarian follicle cells [smallRNA-seq]

Project description:Transposable elements (TEs) pose a threat to genome integrity, and the piRNA pathway in animal gonads plays a crucial role in silencing TE activity. While the transcriptional regulation of piRNA pathway components in germline cells is well understood, the mechanisms orchestrating the transcriptional program of the somatic piRNA pathway in surrounding somatic cells remains poorly defined. Here, we demonstrate that Traffic Jam (Tj), an orthologue of a large Maf transcription factor in mammals, is a master regulator of the somatic piRNA pathway playing a crucial role in maintaining TE silencing and genomic integrity in somatic tissues . We show that Tj directly binds to the promoters of piRNA factors such as fs(1)Yb, nxf2, panx, and armi, as well as the flamenco piRNA cluster, a major locus for TE silencing in somatic cells. Knockdown of Tj in somatic follicle cells results in significant downregulation of these piRNA factors, a complete loss of flam expression, and derepression of TEs. We have identified an enhancer downstream of the flam promoter, including TJ binding sites, essential for high and specific flam expression in ovarian follicle cells in adult ovaries. This work uncovers a previously unappreciated layer of transcriptional regulation oc the piRNA pathway and we propose that Tj evolved to orchestrate the somatic piRNA pathway expression, ensuring efficient TE silencing in somatic cells that support germ cells, thereby preventing instability from being transmitted to the offspring.

2025-04-11 | GSE282039 | GEO

Transcriptional factor Tj is the master regulator of the somatic piRNA pathway in the Drosophila ovarian follicle cells [RNA-seq]

2025-04-11 | GSE275646 | GEO

Traffic Jam activates the Flamenco piRNA cluster locus and the Piwi pathway to ensure transposon silencing and Drosophila fertility

Project description:Flamenco (Flam) is the most prominent piRNA cluster locus expressed in Drosophila ovarian follicle cells, and it is required for female fertility to silence gypsy/mdg4 transposons. To determine how Flam is regulated, we used promoter-bashing reporter assays in OSS cells to uncover novel enhancer sequences within the first exons of Flam. We confirmed the enhancer sequence relevance in vivo with new Drosophila Flam deletion mutants of these regions that compromised Flam piRNA expression and lowered female fertility from activated transposons. Our proteomic analysis of proteins associated with these enhancer sequences discovered the transcription factor Traffic Jam (TJ). Tj knockdowns in OSS cells caused a decrease in Flam transcripts, Flam piRNAs, and multiple Piwi pathway genes. A TJ ChIP-seq analysis from whole flies and OSS cells confirmed TJ binding exactly at the enhancer that was deleted in the new Flam mutant as well as at multiple Piwi pathway gene enhancers. Interestingly, TJ also bound the Long Terminal Repeats of transposons that had decreased expression after Tj knockdowns in OSS cells. Our study reveals the integral role TJ plays in the on-going arms race between selfish transposons and their suppression by the host Piwi pathway and the Flam piRNA cluster locus.

2025-02-02 | GSE286025 | GEO

Traffic jam directly regulates the Drosophila piRNA cluster flamenco and the Piwi pathway gene network to ensure transposon silencing and female fertility.

Project description:The flamenco (flam) locus is the most prominent piRNA cluster locus expressed in Drosophila ovarian follicle cells that is required for female fertility and silencing of gypsy/mdg4 transposons. Although P-element insertions in the flam promoter region disrupts flam piRNAs and cause female infertility, the flam enhancer architecture is still poorly understood. To illuminate flam’s regulation, we uncovered novel shadow enhancer (SE) sequences within the first exons of flam via promoter-bashing assays in OSS cells. We confirmed the SE relevance in vivo with new Drosophila flam deletion mutants of these regions that compromised flam piRNA expression and lowered female fertility from unleashed transposon expression. In a proteomic analysis of proteins associated with these SE sequences, the MAF transcription factor Traffic jam (Tj) emerged as the most prominent binding candidate. With Tj knockdowns in OSS cells, we see a coordinated loss of flam transcripts and piRNAs as well as a decreased expression of many Piwi pathway genes including piwi, which then also coincided with increased transposon RNA levels. We conducted ChIP-seq of Tj’s interaction at Piwi pathway gene promoters and hundreds of other genes important for follicle cell development. Lastly, we utilized transient Tj knockdown in the fly ovary to support our conclusions of how Tj orchestrates the complex Piwi pathway network in Drosophila follicle cells.

2025-04-01 | PXD052946 | Pride

Unistrand piRNA clusters are an evolutionarily conserved mechanism to suppress endogenous retroviruses across the Drosophila genus [ATAC-Seq]

Project description:The PIWI-interacting RNA (piRNA) pathway plays a crucial role in preventing endogenous genomic parasites, transposable elements (TEs), from damaging the genetic material of animal gonadal cells. Specific regions in the genome, called piRNA clusters, define each species’ piRNA repertoire and therefore its capacity to recognize and silence transposons. In the somatic cells of the Drosophila melanogaster ovary, the flamenco (flam) unistrand cluster is the main source of piRNAs and primarily regulates Gypsy family TEs that are able to form virus-like particles and infect neighbouring germ cells. Disruption of the flam locus or failure to process flam precursor transcripts into piRNAs results in sterility, yet it remains unknown whether this silencing mechanism is employed widely across Drosophilidae. Here, using both synteny-based analyses and de novo TE annotation, we identify candidate loci sharing both their organisation and TE targeting repertoire with flam in widely divergent Drosophila species groups. Small RNA-sequencing validated these loci as bona-fide unistrand piRNA clusters and revealed their predominant expression in somatic cells of the ovary, likely to counter TE mobilisation in this tissue. This study provides compelling evidence of co-evolution between virus-like Gypsy family transposons and a host defence mechanism in form of soma-expressed, unistrand piRNA clusters.

2023-09-26 | GSE240910 | GEO

Unistrand piRNA clusters are an evolutionarily conserved mechanism to suppress endogenous retroviruses across the Drosophila genus [RNA-Seq]

2023-09-26 | GSE225887 | GEO

Unistrand piRNA clusters are an evolutionarily conserved mechanism to suppress endogenous retroviruses across the Drosophila genus [small RNA-Seq]

2023-09-26 | GSE225888 | GEO

HITS-CLIP analysis of Yb binding sites in Drosophila ovary cell line

Project description:piRNAs direct Piwi to repress transposons to maintain genome integrity in Drosophila ovarian somatic cells. piRNA maturation and association with Piwi occur at perinuclear Yb bodies, the centers of piRNA biogenesis. Here, we show that piRNA intermediates arising from the piRNA cluster flamenco (flam) concentrate into perinuclear foci adjacent to Yb bodies, termed Flam bodies. Although flam expression is not required for Yb body formation, Yb, the core component of Yb bodies, is required for Flam body formation. Abolishment of the RNA-binding activity of Yb disrupts both Yb bodies and Flam bodies. Loss of Zucchini, an endoribonuclease necessary for piRNA maturation, enlarges Flam bodies, which now superimpose with Yb bodies. Yb directly binds flam, but not neighboring protein-coding gene, transcripts. Thus, Yb integrates piRNA processing factors and piRNA intermediates into Yb bodies and Flam bodies, respectively, through direct binding to enhance piRNA biogenesis and formation of piRNA-inducing silencing complexes. HITS-CLIP was performed using OSC (Ovarian Somatic Cells). The antibody for Drosophila Yb, which was generated in this study, was used. Obtained CLIP tags were analyzed using illumina HiSeq200.

2014-06-24 | E-GEOD-54875 | biostudies-arrayexpress

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.

2024-04-02 | PXD047439 | Pride

PIWI-piRNA pathway mediated transposon repression in Hydra somatic stem cells

Project description:Transposable elements (TEs) can damage genomes, thus organisms employ a variety of mechanisms to repress TE expression. The PIWI-piRNA pathway is a small RNA pathway that represses TE expression in the germline of animals. Here we explore the function of the pathway in the somatic stem cells of Hydra, a long-lived freshwater cnidarian. Hydra have three stem cell populations, all of which express PIWI proteins; endodermal and ectodermal epithelial stem cells are somatic, whereas the interstitial stem cells have germline competence. To study somatic function of the pathway we isolated piRNAs from Hydra that lack the interstitial lineage and found that these somatic piRNAs map predominantly to TE transcripts and display the conserved sequence signatures typical of germline piRNAs. Three lines of evidence suggest that the PIWI-piRNA pathway represses TEs in Hydra epithelial stem cells. First, epithelial knockdown of the Hydra piwi gene hywi resulted in upregulation of TE expression. Second, degradome sequencing revealed evidence of PIWI-mediated cleavage of TE RNAs in epithelial cells using the ping-pong mechanism. Finally, we demonstrated a direct association between Hywi protein and TE transcripts in epithelial cells using RNA immunoprecipitation. Altogether, our data reveal that the PIWI-piRNA pathway represses TE expression in the somatic cell lineages of Hydra, which we propose contributes to the extreme longevity of the organism. Furthermore, our results, in combination with others, suggest that somatic TE repression is an ancestral function of the PIWI-piRNA pathway.

2019-08-07 | GSE135440 | GEO

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