Establishment of H3K9me3-dependent heterochromatin during embryogenesis in Drosophila miranda

  1. Kevin H-C Wei
  2. Carolus Chan
  3. Doris Bachtrog  Is a corresponding author
  1. University of California, Berkeley, United States

Abstract

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 stage3 over transposable elements (TE) 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 develops 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.

Data availability

All ChIP-seq and ATAC-seq data generated have been deposited on Genebank under BioProject PRJNA601450. Intermediate files, including ChIP enrichment files and peak calls, are uploaded on Dryad. R and perl scripts for spike in normalization, generating enrichment around peaks, and enrichment heatmaps are available on KW's github page (https://github.com/weikevinhc/heterochromatin.git).

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Kevin H-C Wei

    Department of Integrative Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Carolus Chan

    Department of Integrative Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Doris Bachtrog

    Department of Integrative Biology, University of California, Berkeley, Berkeley, United States
    For correspondence
    dbachtrog@berkeley.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9724-9467

Funding

National Institutes of Health (R01AG057029)

  • Doris Bachtrog

National Institutes of Health (R01GM101255)

  • Doris Bachtrog

National Institutes of Health (R01GM076007)

  • Doris Bachtrog

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Irene E Chiolo, University of Southern California, United States

Publication history

  1. Received: January 30, 2020
  2. Accepted: June 14, 2021
  3. Accepted Manuscript published: June 15, 2021 (version 1)
  4. Version of Record published: July 16, 2021 (version 2)

Copyright

© 2021, Wei et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Kevin H-C Wei
  2. Carolus Chan
  3. Doris Bachtrog
(2021)
Establishment of H3K9me3-dependent heterochromatin during embryogenesis in Drosophila miranda
eLife 10:e55612.
https://doi.org/10.7554/eLife.55612
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