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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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Autores principales: Wei, Kevin H-C, Chan, Carolus, Bachtrog, Doris
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8285105/
https://www.ncbi.nlm.nih.gov/pubmed/34128466
http://dx.doi.org/10.7554/eLife.55612
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author Wei, Kevin H-C
Chan, Carolus
Bachtrog, Doris
author_facet Wei, Kevin H-C
Chan, Carolus
Bachtrog, Doris
author_sort Wei, Kevin H-C
collection PubMed
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 pubmed-82851052021-07-19 Establishment of H3K9me3-dependent heterochromatin during embryogenesis in Drosophila miranda Wei, Kevin H-C Chan, Carolus Bachtrog, Doris eLife Genetics and Genomics 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. eLife Sciences Publications, Ltd 2021-06-15 /pmc/articles/PMC8285105/ /pubmed/34128466 http://dx.doi.org/10.7554/eLife.55612 Text en © 2021, Wei et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Genetics and Genomics
Wei, Kevin H-C
Chan, Carolus
Bachtrog, Doris
Establishment of H3K9me3-dependent heterochromatin during embryogenesis in Drosophila miranda
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 Genetics and Genomics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8285105/
https://www.ncbi.nlm.nih.gov/pubmed/34128466
http://dx.doi.org/10.7554/eLife.55612
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