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

Abstract
Data availability
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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

(2017) Landscape of histone modifications in a sponge reveals the origin of animal cis-regulatory complexity
Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE79645).

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE79645

The following previously published data sets were used

(2014) A high-resolution Amphimedon queenslandica transriptomic timecourse
Publicly available at NCBI Gene Expression Omnibus (accession no: GSE54364).

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE54364
(2015) Amphimedon queenslandica deep developmental transcriptomes
Publicly available at NCBI Sequence Read Archive (accession no: SRP044247).

https://trace.ncbi.nlm.nih.gov/Traces/sra/sra.cgi?study=SRP044247
1. Helm RR
2. Siebert S
3. Tulin S
4. Smith J
5. Dunn CW
(2013) Characterization of differential transcript abundance through time during Nematostella vectensis development
Publicly available at NCBI Sequence Read Archive (accession no: SRP018739).

http://sra.dnanexus.com/studies/SRP018739/experiments
1. Schwaiger M
2. Schönauer A
3. Rendeiro AF
4. Pribitzer C
5. Schauer A
6. Gilles A
7. Schinko J
8. Renfer E
9. Fredman D
10. Technau U
(2013) Evolutionary conservation of the eumetazoan gene regulatory landscape
Publicly available at NCBI Gene Expression Omnibus (accession no: GSE46488).

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE46488

Article and author information

Author details

Federico Gaiti

School of Biological Sciences, University of Queensland, Brisbane, Australia

Competing interests
The authors declare that no competing interests exist.
Katia Jindrich

School of Biological Sciences, University of Queensland, Brisbane, Australia

Competing interests
The authors declare that no competing interests exist.
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.
Kathrein E Roper

School of Biological Sciences, University of Queensland, Brisbane, Australia

Competing interests
The authors declare that no competing interests exist.
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.
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

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.