Establishment of H3K9me3-dependent heterochromatin during embryogenesis in Drosophila miranda

Heterochromatin is a key architectural feature of eukaryotic genomes crucial for silencing of repetitive elements. During Drosophila embryonic cellularization, heterochromatin rapidly appears over repetitive sequences, but the molecular details of how heterochromatin is established are poorly unders...

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Main Authors: Kevin H-C Wei, Carolus Chan, Doris Bachtrog
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-06-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/55612
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author Kevin H-C Wei
Carolus Chan
Doris Bachtrog
author_facet Kevin H-C Wei
Carolus Chan
Doris Bachtrog
author_sort Kevin H-C Wei
collection DOAJ
description Heterochromatin is a key architectural feature of eukaryotic genomes crucial for silencing of repetitive elements. During Drosophila embryonic cellularization, heterochromatin rapidly appears over repetitive sequences, but the molecular details of how heterochromatin is established are poorly understood. Here, we map the genome-wide distribution of H3K9me3-dependent heterochromatin in individual embryos of Drosophila miranda at precisely staged developmental time points. We find that canonical H3K9me3 enrichment is established prior to cellularization and matures into stable and broad heterochromatin domains through development. Intriguingly, initial nucleation sites of H3K9me3 enrichment appear as early as embryonic stage 3 over transposable elements (TEs) and progressively broaden, consistent with spreading to neighboring nucleosomes. The earliest nucleation sites are limited to specific regions of a small number of recently active retrotransposon families and often appear over promoter and 5’ regions of LTR retrotransposons, while late nucleation sites develop broadly across the entirety of most TEs. Interestingly, early nucleating TEs are strongly associated with abundant maternal piRNAs and show early zygotic transcription. These results support a model of piRNA-associated co-transcriptional silencing while also suggesting additional mechanisms for site-restricted H3K9me3 nucleation at TEs in pre-cellular Drosophila embryos.
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spelling doaj.art-0b15e99a02c94e5980d7675f2a86cc4e2022-12-22T02:02:00ZengeLife Sciences Publications LtdeLife2050-084X2021-06-011010.7554/eLife.55612Establishment of H3K9me3-dependent heterochromatin during embryogenesis in Drosophila mirandaKevin H-C Wei0https://orcid.org/0000-0002-1694-9582Carolus Chan1Doris Bachtrog2https://orcid.org/0000-0001-9724-9467Department of Integrative Biology, University of California, Berkeley, Berkeley, United StatesDepartment of Integrative Biology, University of California, Berkeley, Berkeley, United StatesDepartment of Integrative Biology, University of California, Berkeley, Berkeley, United StatesHeterochromatin is a key architectural feature of eukaryotic genomes crucial for silencing of repetitive elements. During Drosophila embryonic cellularization, heterochromatin rapidly appears over repetitive sequences, but the molecular details of how heterochromatin is established are poorly understood. Here, we map the genome-wide distribution of H3K9me3-dependent heterochromatin in individual embryos of Drosophila miranda at precisely staged developmental time points. We find that canonical H3K9me3 enrichment is established prior to cellularization and matures into stable and broad heterochromatin domains through development. Intriguingly, initial nucleation sites of H3K9me3 enrichment appear as early as embryonic stage 3 over transposable elements (TEs) and progressively broaden, consistent with spreading to neighboring nucleosomes. The earliest nucleation sites are limited to specific regions of a small number of recently active retrotransposon families and often appear over promoter and 5’ regions of LTR retrotransposons, while late nucleation sites develop broadly across the entirety of most TEs. Interestingly, early nucleating TEs are strongly associated with abundant maternal piRNAs and show early zygotic transcription. These results support a model of piRNA-associated co-transcriptional silencing while also suggesting additional mechanisms for site-restricted H3K9me3 nucleation at TEs in pre-cellular Drosophila embryos.https://elifesciences.org/articles/55612heterochromatinDrosophiladevelopmentpiRNAtransposable elementssatellite DNA
spellingShingle Kevin H-C Wei
Carolus Chan
Doris Bachtrog
Establishment of H3K9me3-dependent heterochromatin during embryogenesis in Drosophila miranda
eLife
heterochromatin
Drosophila
development
piRNA
transposable elements
satellite DNA
title Establishment of H3K9me3-dependent heterochromatin during embryogenesis in Drosophila miranda
title_full Establishment of H3K9me3-dependent heterochromatin during embryogenesis in Drosophila miranda
title_fullStr Establishment of H3K9me3-dependent heterochromatin during embryogenesis in Drosophila miranda
title_full_unstemmed Establishment of H3K9me3-dependent heterochromatin during embryogenesis in Drosophila miranda
title_short Establishment of H3K9me3-dependent heterochromatin during embryogenesis in Drosophila miranda
title_sort establishment of h3k9me3 dependent heterochromatin during embryogenesis in drosophila miranda
topic heterochromatin
Drosophila
development
piRNA
transposable elements
satellite DNA
url https://elifesciences.org/articles/55612
work_keys_str_mv AT kevinhcwei establishmentofh3k9me3dependentheterochromatinduringembryogenesisindrosophilamiranda
AT caroluschan establishmentofh3k9me3dependentheterochromatinduringembryogenesisindrosophilamiranda
AT dorisbachtrog establishmentofh3k9me3dependentheterochromatinduringembryogenesisindrosophilamiranda