Maternally inherited piRNAs direct transient heterochromatin formation at active transposons during early Drosophila embryogenesis

Abstract

The PIWI-interacting RNA (piRNA) pathway controls transposon expression in animal germ cells, thereby ensuring genome stability over generations. In Drosophila, piRNAs are intergenerationally inherited through the maternal lineage, and this has demonstrated importance in the specification of piRNA source loci and in silencing of I- and P-elements in the germ cells of daughters. Maternally inherited Piwi protein enters somatic nuclei in early embryos prior to zygotic genome activation and persists therein for roughly half of the time required to complete embryonic development. To investigate the role of the piRNA pathway in the embryonic soma, we created a conditionally unstable Piwi protein. This enabled maternally deposited Piwi to be cleared from newly laid embryos within 30 minutes and well ahead of the activation of zygotic transcription. Examination of RNA and protein profiles over time, and correlation with patterns of H3K9me3 deposition, suggests a role for maternally deposited Piwi in attenuating zygotic transposon expression in somatic cells of the developing embryo. In particular, robust deposition of piRNAs targeting roo, an element whose expression is mainly restricted to embryonic development, results in the deposition of transient heterochromatic marks at active roo insertions. We hypothesize that roo, an extremely successful mobile element, may have adopted a lifestyle of expression in the embryonic soma to evade silencing in germ cells.

Data availability

Raw data from high-throughput sequencing experiments are available at GEO under accession number GSE160778. Raw data from proteomics experiments are available on PRIDE with accession number PXD0022409. Source data files have been provided for Figures 1 and 2.

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

Article and author information

Author details

  1. Martin H Fabry

    Cancer Research UK Cambridge Institute, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8484-4715
  2. Federica A Falconio

    Cancer Research UK Cambridge Institute, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Fadwa Joud

    Cancer Research UK Cambridge Institute, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Emily K Lythgoe

    Cancer Research UK Cambridge Institute, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Benjamin Czech

    Cancer Research UK Cambridge Institute, University of Cambridge, Cambridge, United Kingdom
    For correspondence
    benjamin.czech@cruk.cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8471-0007
  6. Gregory J Hannon

    Cancer Research UK Cambridge Institute, University of Cambridge, Cambridge, United Kingdom
    For correspondence
    greg.hannon@cruk.cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4021-3898

Funding

Royal Society (Wolfson Research Professor (RP130039))

  • Gregory J Hannon

Cancer Research UK (Core funding (A21143))

  • Gregory J Hannon

Wellcome Trust (Investigator award (110161/ Z/15/Z))

  • Gregory J Hannon

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

Version history

  1. Received: March 19, 2021
  2. Preprint posted: May 25, 2021 (view preprint)
  3. Accepted: July 7, 2021
  4. Accepted Manuscript published: July 8, 2021 (version 1)
  5. Version of Record published: August 9, 2021 (version 2)

Copyright

© 2021, Fabry 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. Martin H Fabry
  2. Federica A Falconio
  3. Fadwa Joud
  4. Emily K Lythgoe
  5. Benjamin Czech
  6. Gregory J Hannon
(2021)
Maternally inherited piRNAs direct transient heterochromatin formation at active transposons during early Drosophila embryogenesis
eLife 10:e68573.
https://doi.org/10.7554/eLife.68573

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https://doi.org/10.7554/eLife.68573

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