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Limited impact of the siRNA pathway on transposable element expression in Aedes aegypti [ncRNA-seq]

ABSTRACT: Transposable elements (TEs) are DNA sequences that can change their position within a genome. In the germline of arthropods, post-transcriptional regulation of TE expression is mainly mediated by the Piwi-interacting RNA (piRNA) pathway. piRNAs are small RNAs of 24-30 nucleotides (nt) in length produced from genomic precursor transcripts as well as through a ‘ping-pong’ amplification cycle. In somatic tissues, certain insects, such as Drosophila, instead rely on the small interfering RNA (siRNA) pathway as a key regulator of TE expression. siRNAs are 21nt small RNAs produced from double-stranded RNA by the endonuclease Dicer2, which guides an RNA-induced silencing complex to degrade a complementary RNA. However, whether the siRNA pathway also regulates TE expression in the mosquito Aedes aegypti, a medically significant vector species with abundant somatic piRNAs, is unknown. To address this question, we investigated the expression of TEs and small RNAs in both somatic and gonadal tissues of a Dicer2 mutant line of Ae. aegypti and its wild-type counterpart. Our results show a modified pattern of TE expression and a decrease in TE-derived 21nt small RNAs in the Dicer2 mutant, but no major shift of TE transcript abundance. The lack of a functional siRNA pathway also causes perturbations in piRNA ping-pong signatures and the expression of certain piRNA-associated genes, but without clear evidence for compensation by increased piRNA pathway activity. We conclude that the mosquito Ae. aegypti produces siRNAs targeting TEs but these lack a critical role in the regulation of TE expression both in somatic and in gonadal tissues.

ORGANISM(S): Aedes aegypti

PROVIDER: GSE275903 | GEO | 2025/04/09

REPOSITORIES: GEO

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Limited impact of the siRNA pathway on transposable element expression in Aedes aegypti [RNA-seq]

Project description:Transposable elements (TEs) are DNA sequences that can change their position within a genome. In the germline of arthropods, post-transcriptional regulation of TE expression is mainly mediated by the Piwi-interacting RNA (piRNA) pathway. piRNAs are small RNAs of 24-30 nucleotides (nt) in length produced from genomic precursor transcripts as well as through a ‘ping-pong’ amplification cycle. In somatic tissues, certain insects, such as Drosophila, instead rely on the small interfering RNA (siRNA) pathway as a key regulator of TE expression. siRNAs are 21nt small RNAs produced from double-stranded RNA by the endonuclease Dicer2, which guides an RNA-induced silencing complex to degrade a complementary RNA. However, whether the siRNA pathway also regulates TE expression in the mosquito Aedes aegypti, a medically significant vector species with abundant somatic piRNAs, is unknown. To address this question, we investigated the expression of TEs and small RNAs in both somatic and gonadal tissues of a Dicer2 mutant line of Ae. aegypti and its wild-type counterpart. Our results show a modified pattern of TE expression and a decrease in TE-derived 21nt small RNAs in the Dicer2 mutant, but no major shift of TE transcript abundance. The lack of a functional siRNA pathway also causes perturbations in piRNA ping-pong signatures and the expression of certain piRNA-associated genes, but without clear evidence for compensation by increased piRNA pathway activity. We conclude that the mosquito Ae. aegypti produces siRNAs targeting TEs but these lack a critical role in the regulation of TE expression both in somatic and in gonadal tissues.

2025-04-09 | GSE275899 | GEO

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

Next-generation sequencing analysis of Piwi-interacting RNAs (piRNAs) in Drosophila wild-type and bel mutant ovaries

Project description:Belle has been known to be co-localized with piRNA-related proteins at the nuage of germline cells during Drosophila oogenesis. However, its role in piRNA biogenesis remains unclear. To reveal whether Belle is involved in regulating piRNA expression, we performed next-generation sequencing analysis of small non-coding RNAs on ovaries harvested from the wild type (W1118) and trans-heterozygous bel[74407/neo30] mutant. Small RNA-seq experiments were performed on three individual ovary samples with the same genotype. For piRNA expression analysis, we performed mapping of three sets of small RNA sequencing reads for each genotype to previously identified eight distinct piRNA clusters located in four different Drosophila chromosomes (from X to 4). Analysis of the piRNA expression profiling from these piRNA cluster loci indicates that some specific piRNA populations were either upregulated or downregulated in bel mutant ovaries compared with wild-type ovaries. Furthermore, we performed systematic analysis by mapping piRNA sequencing reads to sequences of all identified Drosophila transposable elements (TEs) to classify and measure piRNA reads based on their TE targets. Among 124 TE-classified piRNA populations, 9 and 20 of them were upregulated and downregulated (≥2 folds), respectively, in bel74407/neo30 mutant ovaries compared with those from wild-type ovaries. To examine the effect of the bel[74407/neo30] mutation on the ping-pong cycle for secondary piRNA biogenesis, analysis of the ping-pong signature of piRNAs specifically mapped to the retro-element Burdock was performed. The ping-pong signature for the generation of secondary piRNAs was not significantly altered in bel mutants compared with the wild type. These results, taken together, indicate that Bel is not required for primary and secondary piRNA biogenesis, but it is involved in regulating expression of specific subsets of piRNA populations.

2017-09-01 | GSE65565 | GEO

piRNA-mediated transgenerational inheritance of an acquired trait

Project description:The maintenance of genome integrity is an essential trait to the successful transmission of genetic information. In animal germ cells, piRNAs guide PIWI proteins to silence transposable elements (TEs) in order to maintain genome integrity. In insects, most of TE silencing in the germline is achieved by secondary piRNAs that are produced by a feed-forward loop (the ping-pong cycle), which requires the piRNA-directed cleavages of two types of RNAs: mRNAs of functional euchromatic TEs and heterochromatic transcripts that contain defective TE sequences. The first cleavage which initiates such amplification loop remains poorly understood. Taking advantage of the existence of strains that are devoid of functional copies of the LINE-like I-element, we report that in such Drosophila ovaries, the initiation of a ping-pong cycle is achieved only by secondary I-element piRNAs that are produced in the ovary and deposited in the embryonic germline. This unusual secondary piRNA biogenesis, detected in the absence of functional I-element copies, results from the processing of sense and antisense transcripts of several different defective I-elements. Once acquired, for instance after ancestor aging, this capacity to produce heterochromatic-only secondary piRNAs is partially transmitted through generations via maternal piRNAs. Furthermore, such piRNAs acting as ping-pong initiators in a chromatin-independent manner confer to the progeny a high capacity to repress the I-element mobility. Our study explains at the molecular level the basis for epigenetic memory of maternal immunity that protects females from hybrid dysgenesis caused by transposition of paternally inherited functional I-elements. Comparison of Drosophila small RNA populations in ovaries and/or eggs from 3-day-old or 25-day-old females.

2012-04-13 | E-GEOD-34506 | biostudies-arrayexpress

piRNA-mediated transgenerational inheritance of an acquired trait

2012-04-13 | GSE34506 | GEO

An mRNA/3' UTR-directed primary piRNA pathway in Drosophila ovarian somatic cells

Project description:Piwi-interacting RNAs (piRNAs) are ~24-30 nucleotide regulatory RNAs that are abundantly expressed in gonads. The most well-understood piRNAs mediate post-transcriptional defense against transposable elements (TEs), and derive from sense or antisense strands as a consequence of "ping-pong" amplification of complementary sequences of active TEs and piRNA master control transcripts. Another class of piRNAs, such as those expressed in pachytene testis, derive from large intergenic clusters that are strictly single-stranded. Here, we report a third substrate that generates abundant primary piRNAs. In somatic follicle cells of Drosophila ovaries, we cloned >1 million piRNAs from thousands of messenger RNAs, and these were quite preferentially derived from 3' untranslated regions. This segregation implies a competition between the translation machinery and primary piRNA biogenesis machinery for mRNA access. 3 replicates.

2010-01-03 | E-GEOD-15825 | biostudies-arrayexpress

Krimper enforces an antisense bias on piRNA pools by binding AGO3 in the Drosophila germline

Project description:Piwi-interacting RNAs (piRNAs) suppress transposon activity in animal germ cells. In the Drosophila ovary, primary Aubergine (Aub)-bound antisense piRNAs initiate the ping-pong cycle to produce secondary AGO3-bound sense piRNAs. This increases the number of secondary Aub-bound antisense piRNAs that can act to destroy transposon mRNAs. Here we show that Krimper (Krimp), a Tudor-domain protein, directly interacts with piRNA-free AGO3 to promote symmetrical dimethylarginine (sDMA) modification, ensuring sense piRNA-loading onto sDMA-modified AGO3. In aub mutant ovaries, AGO3 associates with ping-pong signature piRNAs, suggesting AGO3’s compatibility with primary piRNA loading. Krimp sequesters ectopically expressed AGO3 within Krimp bodies in cultured ovarian somatic cells (OSCs), in which only the primary piRNA pathway operates. Upon krimp-RNAi in OSCs, AGO3 loads with piRNAs, further showing the capacity of AGO3 for primary piRNA loading. We propose that Krimp enforces an antisense bias on piRNA pools by binding AGO3 and blocking its access to primary piRNAs. In order to investigate function of Krimp in piRNA pathway, sequencing of Piwi subfamily protein associated small RNAs was performed using adult Drosophila ovaries and Ovarian Somatic Cells (OSCs) depleted for Krimp or Aub.

2015-05-28 | E-GEOD-69293 | biostudies-arrayexpress

Shutdown is a component of the Drosophila piRNA biogenesis machinery (RNA-seq)

Project description:In animals, the piRNA pathway preserves the integrity of gametic genomes, guarding them against the activity of mobile genetic elements. This innate immune mechanism relies on distinct genomic loci, termed piRNA clusters, to provide a molecular definition of transposons, enabling their discrimination from genes. piRNA clusters give rise to long, single-stranded precursors which are processed into primary piRNAs through an unknown mechanism. These can engage in an adaptive amplification loop, the ping-pong cycle, to optimize the content of small RNA populations via the generation of secondary piRNAs. Many proteins have been ascribed functions in either primary biogenesis or the ping-pong cycle, though for the most part the molecular functions of proteins implicated in these pathways remain obscure. Here, we link shutdown, a gene previously shown to be required for fertility in Drosophila, to the piRNA pathway. Analysis of knockdown phenotypes in both the germline and somatic compartments of the ovary demonstrate important roles for shutdown in both primary biogenesis and the ping-pong cycle. shutdown is a member of the FKBP family of immunophilins. Shu contains domains implicated in peptidyl-prolyl cis-trans isomerase activity and in the binding of HSP90-family chaperones, though the relevance of these domains to piRNA biogenesis is unknown.

2012-07-01 | GSE38090 | GEO

Euchromatic transposon insertions trigger production of novel pi- and endo-siRNAs at the target sites in the Drosophila germline

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.

2014-02-07 | E-GEOD-46105 | biostudies-arrayexpress

Shutdown is a component of the Drosophila piRNA biogenesis machinery (smallRNA)

Project description:In animals, the piRNA pathway preserves the integrity of gametic genomes, guarding them against the activity of mobile genetic elements. This innate immune mechanism relies on distinct genomic loci, termed piRNA clusters, to provide a molecular definition of transposons, enabling their discrimination from genes. piRNA clusters give rise to long, single-stranded precursors which are processed into primary piRNAs through an unknown mechanism. These can engage in an adaptive amplification loop, the ping-pong cycle, to optimize the content of small RNA populations via the generation of secondary piRNAs. Many proteins have been ascribed functions in either primary biogenesis or the ping- pong cycle, though for the most part the molecular functions of proteins implicated in these pathways remain obscure. Here, we link shutdown, a gene previously shown to be required for fertility in Drosophila, to the piRNA pathway. Analysis of knockdown phenotypes in both the germ line and somatic compartments of the ovary demonstrate important roles for shutdown in both primary biogenesis and the ping-pong cycle. shutdown is a member of the FKBP family of immunophilins, with domains implicated in peptidyl-prolyl cis-trans isomerase activity and in the binding of HSP90-family chaperones. Though the relevance of these domains to piRNA biogenesis is unknown, evolutionary comparisons raise questions about the integrity of these functions in the shutdown protein. Examination of small RNA levels from nos-GAL4 or tj-GAL4 driven UAS-dsRNA knockdowns of white, shu and piwi in ovaries of Drosophila melanogaster by deep sequencing (using Illumina GAII).

2012-06-30 | E-GEOD-38089 | biostudies-arrayexpress

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