Repression of interrupted and intact rDNA by the SUMO pathway in Drosophila melanogaster

  1. Yicheng Luo
  2. Elena Fefelova
  3. Maria Ninova
  4. Yung-Chia Ariel Chen
  5. Alexei Aravin  Is a corresponding author
  1. California Institute of Technology, United States

Abstract

Ribosomal RNAs (rRNAs) are essential components of the ribosome and are among the most abundant macromolecules in the cell. To ensure high rRNA level, eukaryotic genomes contain dozens to hundreds of rDNA genes, however, only a fraction of the rRNA genes seems to be active, while others are transcriptionally silent. We found that individual rDNA genes have high level of cell-to-cell heterogeneity in their expression in Drosophila melanogaster. Insertion of heterologous sequences into rDNA leads to repression associated with reduced expression in individual cells and decreased number of cells expressing rDNA with insertions. We found that SUMO (Small Ubiquitin-like Modifier) and SUMO ligase Ubc9 are required for efficient repression of interrupted rDNA units and variable expression of intact rDNA. Disruption of the SUMO pathway abolishes discrimination of interrupted and intact rDNAs and removes cell-to-cell heterogeneity leading to uniformly high expression of individual rDNA in single cells. Our results suggest that the SUMO pathway is responsible for both repression of interrupted units and control of intact rDNA expression.

Data availability

Sequencing data have been deposited in GEO under accession codes GSE141068 and GSE115277. Other data generated or analysed during this study are included in the manuscript and supporting files.

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

Article and author information

Author details

  1. Yicheng Luo

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3704-2389
  2. Elena Fefelova

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9185-1243
  3. Maria Ninova

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Yung-Chia Ariel Chen

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Alexei Aravin

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    For correspondence
    aaa@caltech.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6956-8257

Funding

National Institute of General Medical Sciences (GM097363)

  • Alexei Aravin

Howard Hughes Medical Institute (Faculty Scholar Award)

  • Alexei Aravin

Ministry of Education and Science of Russian Federation (14.W03.31.0007)

  • Alexei Aravin

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

Reviewing Editor

  1. Robert H Singer, Albert Einstein College of Medicine, United States

Version history

  1. Received: October 3, 2019
  2. Accepted: November 6, 2020
  3. Accepted Manuscript published: November 9, 2020 (version 1)
  4. Version of Record published: November 19, 2020 (version 2)

Copyright

© 2020, Luo 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. Yicheng Luo
  2. Elena Fefelova
  3. Maria Ninova
  4. Yung-Chia Ariel Chen
  5. Alexei Aravin
(2020)
Repression of interrupted and intact rDNA by the SUMO pathway in Drosophila melanogaster
eLife 9:e52416.
https://doi.org/10.7554/eLife.52416

Share this article

https://doi.org/10.7554/eLife.52416

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