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.

Data availability

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

Article and author information

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.

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.

Metrics

  • 5,175
    views
  • 966
    downloads
  • 54
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Further reading

    1. Developmental Biology
    Yunfei Mu, Shijia Hu ... Hongjun Shi
    Research Article

    Notch signaling has been identified as a key regulatory pathway in patterning the endocardium through activation of endothelial-to-mesenchymal transition (EMT) in the atrioventricular canal (AVC) and proximal outflow tract (OFT) region. However, the precise mechanism underlying Notch activation remains elusive. By transiently blocking the heartbeat of E9.5 mouse embryos, we found that Notch activation in the arterial endothelium was dependent on its ligand Dll4, whereas the reduced expression of Dll4 in the endocardium led to a ligand-depleted field, enabling Notch to be specifically activated in AVC and OFT by regional increased shear stress. The strong shear stress altered the membrane lipid microdomain structure of endocardial cells, which activated mTORC2 and PKC and promoted Notch1 cleavage even in the absence of strong ligand stimulation. These findings highlight the role of mechanical forces as a primary cue for endocardial patterning and provide insights into the mechanisms underlying congenital heart diseases of endocardial origin.

    1. Developmental Biology
    2. Evolutionary Biology
    Hope M Healey, Hayden B Penn ... William A Cresko
    Research Article

    Seahorses, pipefishes, and seadragons are fishes from the family Syngnathidae that have evolved extraordinary traits including male pregnancy, elongated snouts, loss of teeth, and dermal bony armor. The developmental genetic and cellular changes that led to the evolution of these traits are largely unknown. Recent syngnathid genome assemblies revealed suggestive gene content differences and provided the opportunity for detailed genetic analyses. We created a single-cell RNA sequencing atlas of Gulf pipefish embryos to understand the developmental basis of four traits: derived head shape, toothlessness, dermal armor, and male pregnancy. We completed marker gene analyses, built genetic networks, and examined the spatial expression of select genes. We identified osteochondrogenic mesenchymal cells in the elongating face that express regulatory genes bmp4, sfrp1a, and prdm16. We found no evidence for tooth primordia cells, and we observed re-deployment of osteoblast genetic networks in developing dermal armor. Finally, we found that epidermal cells expressed nutrient processing and environmental sensing genes, potentially relevant for the brooding environment. The examined pipefish evolutionary innovations are composed of recognizable cell types, suggesting that derived features originate from changes within existing gene networks. Future work addressing syngnathid gene networks across multiple stages and species is essential for understanding how the novelties of these fish evolved.