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

  • 5,124
    views
  • 950
    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
    Emily Delgouffe, Samuel Madureira Silva ... Ellen Goossens
    Research Article

    Although the impact of gender-affirming hormone therapy (GAHT) on spermatogenesis in trans women has already been studied, data on its precise effects on the testicular environment is poor. Therefore, this study aimed to characterize, through histological and transcriptomic analysis, the spermatogonial stem cell niche of 106 trans women who underwent standardized GAHT, comprising estrogens and cyproterone acetate. A partial dedifferentiation of Sertoli cells was observed, marked by the co-expression of androgen receptor and anti-Müllerian hormone which mirrors the situation in peripubertal boys. The Leydig cells also exhibited a distribution analogous to peripubertal tissue, accompanied by a reduced insulin-like factor 3 expression. Although most peritubular myoid cells expressed alpha-smooth muscle actin 2, the expression pattern was disturbed. Besides this, fibrosis was particularly evident in the tubular wall and the lumen was collapsing in most participants. A spermatogenic arrest was also observed in all participants. The transcriptomic profile of transgender tissue confirmed a loss of mature characteristics - a partial rejuvenation - of the spermatogonial stem cell niche and, in addition, detected inflammation processes occurring in the samples. The present study shows that GAHT changes the spermatogonial stem cell niche by partially rejuvenating the somatic cells and inducing fibrotic processes. These findings are important to further understand how estrogens and testosterone suppression affect the testis environment, and in the case of orchidectomized testes as medical waste material, their potential use in research.

    1. Developmental Biology
    2. Stem Cells and Regenerative Medicine
    Kara A Nelson, Kari F Lenhart ... Stephen DiNardo
    Research Article

    Niches are often found in specific positions in tissues relative to the stem cells they support. Consistency of niche position suggests that placement is important for niche function. However, the complexity of most niches has precluded a thorough understanding of how their proper placement is established. To address this, we investigated the formation of a genetically tractable niche, the Drosophila Posterior Signaling Center (PSC), the assembly of which had not been previously explored. This niche controls hematopoietic progenitors of the lymph gland (LG). PSC cells were previously shown to be specified laterally in the embryo, but ultimately reside dorsally, at the LG posterior. Here, using live-imaging, we show that PSC cells migrate as a tight collective and associate with multiple tissues during their trajectory to the LG posterior. We find that Slit emanating from two extrinsic sources, visceral mesoderm and cardioblasts, is required for the PSC to remain a collective, and for its attachment to cardioblasts during migration. Without proper Slit-Robo signaling, PSC cells disperse, form aberrant contacts, and ultimately fail to reach their stereotypical position near progenitors. Our work characterizes a novel example of niche formation and identifies an extrinsic signaling relay that controls precise niche positioning.