Transcriptional and chromatin changes accompanying de novo formation of transgenic piRNA clusters

Akulenko, Natalia; Ryazansky, Sergei; Morgunova, Valeriya; Komarov, Pavel A; Olovnikov, Ivan; Vaury, Chantal; Jensen, Silke; Kalmykova, Alla

doi:10.1261/rna.062851.117

Cited by 27 publications

(34 citation statements)

References 37 publications

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“…This is sustained by our ChIP experiments showing that H3K9me3 levels on BX2 OFF are slightly below the H3K9me3 level of piRNA producing states (BX2 ON and BX2 Θ FIG 2D). The same observation can be made for Rhino (FIG 2E) suggesting that Rhino may be already present on the BX2 OFF locus but below the threshold required for piRNA production as suggested by (41). Thus, a locus made of repeated sequences and being likely heterochromatic (H3K9me3, Rhino) is a necessary but not sufficient condition to specify an active piRNA cluster.…”

Section: Discussionsupporting

confidence: 64%

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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Section: Discussionsupporting

confidence: 64%

Environmentally-induced epigenetic conversion of a piRNA cluster

Casier¹,

Delmarre²,

Gueguen

et al. 2018

Preprint

Self Cite

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“…The anti-trimethyl-histone H3 (Lys27) (Millipore, #07-449) antibody was used for ChIP seq experiment. We followed the protocol previously published in Akulenko et al 47 with some modifications. Briefly, ~1000-2000 eggs were bleached, homogenized, and fixed according to optimized ChIP-seq protocol (Supplementary Protocol 2).…”

Section: Chip-seqmentioning

confidence: 99%

Anophelesmosquitoes revealed new principles of 3D genome organization in insects

Lukyanchikova

Nuriddinov

Belokopytova

et al. 2020

Preprint

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Chromosomes are hierarchically folded within cell nuclei into territories, domains and subdomains, but the functional importance and evolutionary dynamics of these hierarchies are poorly defined. Here, we comprehensively profiled genome organizations of five Anopheles mosquito species and showed how different levels of chromatin architecture influence contacts between genomic loci. Patterns observed on Hi-C maps are associated with known cytological structures, epigenetic profiles, and gene expression levels. At the level of individual loci, we identified specific, extremely longranged looping interactions, conserved for ~100 million years. We showed that the mechanisms underlying these looping contacts differ from previously described Polycomb-dependent interactions and clustering of active chromatin.

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“…Originally, the R strain w K devoid of active I-element copies was used for transgenesis. We revealed that the same transgenes, located at different euchromatic genomic loci, form piRNA clusters with various abilities of small RNA production, termed as "weak" and "strong" transgenic piRNA clusters ( Figure 1B) [19,22]. Most importantly, "strong" piRNA clusters are highly enriched in Rhi and produce piRNAs from all transgenic parts, in contrast to "weak" ones, whose piRNAs mostly map to the I-element fragment.Presumably, piRNAs originating from the ancestral I-elements and complementary to the transgenic I-element fragment drive this transformation.…”

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confidence: 95%

Epigenetic Requirements for Triggering Heterochromatinization and Piwi-Interacting RNA Production from Transgenes in the Drosophila Germline

Komarov

Akulenko

Brasset

et al. 2020

Cells

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Transgenes containing a fragment of the I retrotransposon represent a powerful model of piRNA cluster de novo formation in the Drosophila germline. We revealed that the same transgenes located at different genomic loci form piRNA clusters with various capacity of small RNA production. Transgenic piRNA clusters are not established in piRNA pathway mutants. However, in the wild-type context, the endogenous ancestral I-related piRNAs heterochromatinize and convert the I-containing transgenes into piRNA-producing loci. Here, we address how the quantitative level of piRNAs influences the heterochromatinization and piRNA production. We show that a minimal amount of maternal piRNAs from ancestral I-elements is sufficient to form the transgenic piRNA clusters. Supplemental piRNAs stemming from active I-element copies do not stimulate additional chromatin changes or piRNA production from transgenes. Therefore, chromatin changes and piRNA production are initiated by a minimum threshold level of complementary piRNAs, suggesting a selective advantage of prompt cell response to the lowest level of piRNAs. It is noteworthy that the weak piRNA clusters do not transform into strong ones after being targeted by abundant I-specific piRNAs, indicating the importance of the genomic context for piRNA cluster establishment. Analysis of ovarian transcription profiles suggests that regions facilitating convergent transcription favor the formation of transgenic piRNA clusters.

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Transcriptional and chromatin changes accompanying de novo formation of transgenic piRNA clusters

Cited by 27 publications

References 37 publications

Environmentally-induced epigenetic conversion of a piRNA cluster

Environmentally-induced epigenetic conversion of a piRNA cluster

Anophelesmosquitoes revealed new principles of 3D genome organization in insects

Epigenetic Requirements for Triggering Heterochromatinization and Piwi-Interacting RNA Production from Transgenes in the Drosophila Germline

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