Compartmentalized oskar degradation in the germ plasm safeguards germline development

  1. Catherine E Eichler
  2. Anna C Hakes
  3. Brooke Hull
  4. Elizabeth R Gavis  Is a corresponding author
  1. Princeton University, United States

Abstract

Partitioning of mRNAs into ribonucleoprotein (RNP) granules supports diverse regulatory programs within the crowded cytoplasm. At least two types of RNP granules populate the germ plasm, a cytoplasmic domain at the posterior of the Drosophila oocyte and embryo. Germ granules deliver mRNAs required for germline development to pole cells, the germ cell progenitors. A second type of RNP granule, here named founder granules, contains oskar mRNA, which encodes the germ plasm organizer. Whereas oskar mRNA is essential for germ plasm assembly during oogenesis, we show that it is toxic to pole cells. Founder granules mediate compartmentalized degradation of oskar during embryogenesis to minimize its inheritance by pole cells. Degradation of oskar in founder granules is temporally and mechanistically distinct from degradation of oskar and other mRNAs during the maternal-to-zygotic transition. Our results show how compartmentalization in RNP granules differentially controls fates of mRNAs localized within the same cytoplasmic domain.

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Article and author information

Author details

  1. Catherine E Eichler

    Department of Molecular Biology, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Anna C Hakes

    Department of Molecular Biology, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Brooke Hull

    Department of Molecular Biology, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Elizabeth R Gavis

    Department of Molecular Biology, Princeton University, Princeton, United States
    For correspondence
    gavis@princeton.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0251-0760

Funding

National Institutes of Health (R01 GM067758)

  • Elizabeth R Gavis

National Institutes of Health (R35 GM126967)

  • Elizabeth R Gavis

National Institutes of Health (T32 GM007388)

  • Elizabeth R Gavis

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

Reviewing Editor

  1. Michael Buszczak, University of Texas Southwestern Medical Center, United States

Version history

  1. Received: July 6, 2019
  2. Accepted: January 7, 2020
  3. Accepted Manuscript published: January 7, 2020 (version 1)
  4. Version of Record published: January 28, 2020 (version 2)

Copyright

© 2020, Eichler 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. Catherine E Eichler
  2. Anna C Hakes
  3. Brooke Hull
  4. Elizabeth R Gavis
(2020)
Compartmentalized oskar degradation in the germ plasm safeguards germline development
eLife 9:e49988.
https://doi.org/10.7554/eLife.49988

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