Landscape of histone modifications in a sponge reveals the origin of animal cis-regulatory complexity

  1. Federico Gaiti
  2. Katia Jindrich
  3. Selene L Fernandez-Valverde
  4. Kathrein E Roper
  5. Bernard M Degnan  Is a corresponding author
  6. Miloš Tanurdžić  Is a corresponding author
  1. University of Queensland, Australia
  2. Consejo Nacional de Ciencia y Tecnología, Mexico

Abstract

Combinatorial patterns of histone modifications regulate developmental and cell type-specific gene expression and underpin animal complexity, but it is unclear when this regulatory system evolved. By analysing histone modifications in a morphologically-simple, early branching animal, the sponge Amphimedon queenslandica, we show that the regulatory landscape used by complex bilaterians was already in place at the dawn of animal multicellularity. This includes distal enhancers, repressive chromatin and transcriptional units marked by H3K4me3 that vary with levels of developmental regulation. Strikingly, Amphimedon enhancers are enriched in metazoan-specific microsyntenic units, suggesting that their genomic location is extremely ancient and likely to place constraints on the evolution of surrounding genes. These results suggest that the regulatory foundation for spatiotemporal gene expression evolved prior to the divergence of sponges and eumetazoans, and was necessary for the evolution of animal multicellularity.

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Author details

  1. Federico Gaiti

    School of Biological Sciences, University of Queensland, Brisbane, Australia
    Competing interests
    The authors declare that no competing interests exist.
  2. Katia Jindrich

    School of Biological Sciences, University of Queensland, Brisbane, Australia
    Competing interests
    The authors declare that no competing interests exist.
  3. Selene L Fernandez-Valverde

    Laboratorio Nacional de Genómica para la Biodiversidad, Consejo Nacional de Ciencia y Tecnología, Irapuato, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  4. Kathrein E Roper

    School of Biological Sciences, University of Queensland, Brisbane, Australia
    Competing interests
    The authors declare that no competing interests exist.
  5. Bernard M Degnan

    School of Biological Sciences, University of Queensland, Brisbane, Australia
    For correspondence
    b.degnan@uq.edu.au
    Competing interests
    The authors declare that no competing interests exist.
  6. Miloš Tanurdžić

    School of Biological Sciences, University of Queensland, Brisbane, Australia
    For correspondence
    m.tanurdzic@uq.edu.au
    Competing interests
    The authors declare that no competing interests exist.

Funding

Australian Research Council (FL110100044)

  • Bernard M Degnan

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

Reviewing Editor

  1. Robb Krumlauf, Stowers Institute for Medical Research, United States

Version history

  1. Received: October 8, 2016
  2. Accepted: March 27, 2017
  3. Accepted Manuscript published: April 11, 2017 (version 1)
  4. Version of Record published: May 12, 2017 (version 2)

Copyright

© 2017, Gaiti 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. Federico Gaiti
  2. Katia Jindrich
  3. Selene L Fernandez-Valverde
  4. Kathrein E Roper
  5. Bernard M Degnan
  6. Miloš Tanurdžić
(2017)
Landscape of histone modifications in a sponge reveals the origin of animal cis-regulatory complexity
eLife 6:e22194.
https://doi.org/10.7554/eLife.22194

Share this article

https://doi.org/10.7554/eLife.22194

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