1. Computational and Systems Biology
  2. Neuroscience
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The formation of the light-sensing compartment of cone photoreceptors coincides with a transcriptional switch

  1. Janine M Daum
  2. Özkan Keles
  3. Sjoerd J B Holwerda
  4. Hubertus Kohler
  5. Filippo M Rijli
  6. Michael Stadler  Is a corresponding author
  7. Botond Roska  Is a corresponding author
  1. Friedrich Miescher Institute for Biomedical Research, Switzerland
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Cite this article as: eLife 2017;6:e31437 doi: 10.7554/eLife.31437

Abstract

High-resolution daylight vision is mediated by cone photoreceptors. The molecular program responsible for the formation of their light sensor, the outer segment, is not well understood. We correlated daily changes in ultrastructure and gene expression in postmitotic mouse cones, between birth and eye opening, using serial block-face electron microscopy (EM) and RNA sequencing. Outer segments appeared rapidly at postnatal day six and their appearance coincided with a switch in gene expression. The switch affected over 14% of all expressed genes. Genes that switched off were rich in transcription factors and neurogenic genes. Those that switched on contained genes relevant for cone function. Chromatin rearrangements in enhancer regions occurred before the switch was completed, but not after. We provide a resource comprised of correlated EM, RNAseq, and ATACseq data, showing that the growth of a key compartment of a postmitotic cell involves an extensive switch in gene expression and chromatin accessibility.

Article and author information

Author details

  1. Janine M Daum

    Friedrich Miescher Institute for Biomedical Research, Basel, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  2. Özkan Keles

    Friedrich Miescher Institute for Biomedical Research, Basel, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  3. Sjoerd J B Holwerda

    Friedrich Miescher Institute for Biomedical Research, Basel, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  4. Hubertus Kohler

    Friedrich Miescher Institute for Biomedical Research, Basel, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  5. Filippo M Rijli

    Friedrich Miescher Institute for Biomedical Research, Basel, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0515-0182
  6. Michael Stadler

    Friedrich Miescher Institute for Biomedical Research, Basel, Switzerland
    For correspondence
    michael.stadler@fmi.ch
    Competing interests
    The authors declare that no competing interests exist.
  7. Botond Roska

    Friedrich Miescher Institute for Biomedical Research, Basel, Switzerland
    For correspondence
    botond.roska@fmi.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9559-1450

Funding

Swiss National Science Foundation (3100330B_163457)

  • Botond Roska

European Research Council (669157)

  • Botond Roska

Swiss Natiional Science Foundation (CRSII3_141801)

  • Botond Roska

European Research Council (RETMUS)

  • Botond Roska

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

Ethics

Animal experimentation: Animal procedures were done in accordance with standard ethical guidelines (European Communities Guidelines on the Care and Use of Laboratory Animals, 86/609/EEC) and were approved by the Veterinary Department of the Canton of Basel-Stadt.

Reviewing Editor

  1. Eve Marder, Brandeis University, United States

Publication history

  1. Received: August 22, 2017
  2. Accepted: November 3, 2017
  3. Accepted Manuscript published: November 6, 2017 (version 1)
  4. Version of Record published: November 14, 2017 (version 2)

Copyright

© 2017, Daum 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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