Paramutation in<i>Drosophila</i>Requires Both Nuclear and Cytoplasmic Actors of the piRNA Pathway and Induces<i>Cis</i>-spreading of piRNA Production

Hermant, Catherine; Boivin, Antoine; Teysset, Laure; Delmarre, Valérie; Asif-Laidin, Amna; Beek, Marius van den; Antoniewski, Christophe; Ronsseray, Stéphane

doi:10.1534/genetics.115.180307

Cited by 45 publications

(57 citation statements)

References 71 publications

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“…However, recent research suggests that the interaction between the two biogenesis pathways is more complicated and raises the question whether true ‘primary’ piRNA biogenesis that is independent of pre-existing piRNAs and slicer-cleavage exists in nurse cells. First, it was found that piRNA biogenesis in germ cells requires maternally inherited piRNAs [44, 59, 70, 71]. In addition to initiating installment of the H3K9me3 mark on piRNA clusters (described above), they can start the ping-pong cycle, eliminating the need for ‘starter’ piRNAs formed by a different mechanism.…”

Section: Pirna Biogenesis In the Cytoplasmmentioning

confidence: 99%

piRNA Biogenesis in Drosophila melanogaster

2017

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The PIWI-interacting RNA (piRNA) pathway is a conserved defense system that protects the genome integrity of the animal germline from deleterious transposable elements. Targets of silencing are recognized by small non-coding piRNAs that are processed from long precursor molecules. Though piRNAs and other classes of small non-coding RNAs, such as miRNAs and siRNAs, interact with members of the same family of Argonaute proteins and their function in target repression is similar, the biogenesis of piRNAs differs from those of the other two small RNAs. Recently, many aspects of piRNA biogenesis have been revealed in Drosophila melanogaster. In this review, we elaborate on piRNA biogenesis in Drosophila somatic and germline cells. We focus on the mechanisms by which piRNA precursor transcription is regulated and highlight recent work that advanced our understanding of piRNA precursor processing to mature piRNAs. We finish with discussing current models to the still unresolved question of how piRNA precursors are selected and channeled into the processing machinery.

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Section: Pirna Biogenesis In the Cytoplasmmentioning

confidence: 99%

piRNA Biogenesis in Drosophila melanogaster

2017

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“…Analyses were performed as previously described (11,12). For details, see Supplementary Information.…”

Section: Small Rna Sequencing Analysesmentioning

confidence: 99%

“…Thus, when a new TE inserts into a naive genome, it will freely transpose until one copy gets inserted into a piRNA cluster leading to the production of homologous new TE piRNAs that will then repress transposition (10). In support of this idea, exogenous sequences inserted into preexisting piRNA clusters lead to the production of matching piRNAs (11)(12)(13)(14)(15). The specificity of the efficient repression mediated by piRNAs appears to be determined solely by the piRNA cluster sequences.…”

Section: Introductionmentioning

confidence: 97%

“…To address this paradox, we used the same BX2 cluster of seven P(lacW) transgenes which resulted from multiple and successive P(lacW) transposition events, thus resembling the structure of natural piRNA clusters (20). The key advantage of the BX2 locus is that it can exist in two epigenetic states for the production of germline piRNAs: 1) the inactive state (BX2 OFF ) does not produce any piRNAs and thus is unable to repress the expression of homologous sequences, and 2) the active state (BX2 ON also called BX2*) produces abundant piRNAs that functionally repress a homologous reporter transgene in the female germline (11,12). We therefore used BX2 in an inactive state to search for conditions that would convert it into an active piRNA-producing locus, without pre-existing maternal piRNAs.…”

Section: Introductionmentioning

confidence: 99%

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Environmentally-induced epigenetic conversion of a piRNA cluster

Casier¹,

Delmarre²,

Gueguen

et al. 2018

Preprint

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Transposable element (TE) activity is repressed in animal gonads by PIWI-interacting RNAs (piRNAs), a class of small RNAs produced by specific loci made of TEs insertions and fragments. Current models propose that these loci are functionally defined by the maternal inheritance of piRNAs produced during the previous generation, raising the question of their first activation in the absence of piRNAs. Taking advantage of an inactive cluster of P-element derived transgene insertions, we show here that raising flies at high temperature (29°C) instead of 25°C results in a rare but invasive epigenetic conversion of this locus into an active piRNAs producing one. The newly acquired epigenetic state is stable over many generations even when flies are switch back to 25°C. The silencing capacities, piRNA production and chromatin modifications of the cluster are all identical whether conversion occurred by maternal piRNA inheritance or by high temperature. We also demonstrate that in addition to high temperature, a single homologous transgene inserted elsewhere in the genome is required to activate the locus.We thus have identified a minimal system of three components to create a stable piRNA producing locus: 1) a locus with multiple TE derived sequences; 2) an euchromatic copy of these sequences and 3) elevated temperature. Altogether, these data report the first case of the establishment of an active piRNA cluster by environmental changes. It highlights how such variations of species natural habitat can become heritable and shape their epigenome. SIGNIFICANCE STATEMENTRecently, we have witnessed great progress in our understanding of the silencing of Transposable Elements (TEs) by piRNAs, a class of small RNAs produced by piRNA clusters. At each generation, piRNA clusters are supposed to be activated by homologous piRNAs inherited from the mother raising the question of the making of the first piRNAs. Here, we report the birth of a stable and functional piRNA cluster induced by high temperature without maternal inheritance of homologous piRNAs. We propose a minimal system to create a piRNA cluster: a sufficient number of repeated sequences, a euchromatic copy of these sequences and an increase in the production of antisense RNA. Casier et al. -Thermic activation of a piRNA cluster 3

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“…piRNA pathway-silenced loci are often paramutagenic (Ashe et al, 2012; de Vanssay et al, 2012; Hermant et al, 2015; Sapetschnig et al, 2015; Shirayama et al, 2012). In paramutation, an allele’s expression state can stably alter the expression of a homologous locus in trans (Chandler, 2010).…”

Section: Introductionmentioning

confidence: 99%

Stable Heritable Germline Silencing Directs Somatic Silencing at an Endogenous Locus

Minkina

Hunter

2017

Molecular Cell

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Summary The importance of transgenerationally inherited epigenetic states to organismal fitness remains unknown as well-documented examples are often not amenable to mechanistic analysis or rely on artificial reporter loci. Here we describe an induced silenced state at an endogenous locus that persists, at 100% transmission without selection, for up to 13 generations. This unusually persistent silencing enables a detailed molecular genetic analysis of an inherited epigenetic state. We find that silencing is dependent on germline nuclear RNAi factors and post-transcriptional mechanisms. Consistent with these later observations, inheritance does not require the silenced locus, and we provide genetic evidence that small RNAs embody the inherited silencing signal. Notably, heritable germline silencing directs somatic epigenetic silencing. Somatic silencing does not require somatic nuclear RNAi but instead requires both maternal germline nuclear RNAi and chromatin modifying activity. Coupling inherited germline silencing to somatic silencing may enable selection for physiologically important traits.

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Paramutation inDrosophilaRequires Both Nuclear and Cytoplasmic Actors of the piRNA Pathway and InducesCis-spreading of piRNA Production

Cited by 45 publications

References 71 publications

piRNA Biogenesis in Drosophila melanogaster

piRNA Biogenesis in Drosophila melanogaster

Environmentally-induced epigenetic conversion of a piRNA cluster

Stable Heritable Germline Silencing Directs Somatic Silencing at an Endogenous Locus

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