Landscape of histone modifications in a sponge reveals the origin of animal cis-regulatory complexity
- University of Queensland, Australia
- 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
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Landscape of histone modifications in a sponge reveals the origin of animal cis-regulatory complexityPublicly available at the NCBI Gene Expression Omnibus (accession no: GSE79645).
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A high-resolution Amphimedon queenslandica transriptomic timecoursePublicly available at NCBI Gene Expression Omnibus (accession no: GSE54364).
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Amphimedon queenslandica deep developmental transcriptomesPublicly available at NCBI Sequence Read Archive (accession no: SRP044247).
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Characterization of differential transcript abundance through time during Nematostella vectensis developmentPublicly available at NCBI Sequence Read Archive (accession no: SRP018739).
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Evolutionary conservation of the eumetazoan gene regulatory landscapePublicly available at NCBI Gene Expression Omnibus (accession no: GSE46488).
Article and author information
Author details
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
- Robb Krumlauf, Stowers Institute for Medical Research, United States
Version history
- Received: October 8, 2016
- Accepted: March 27, 2017
- Accepted Manuscript published: April 11, 2017 (version 1)
- 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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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
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