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

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 Amph...

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Main Authors: Federico Gaiti, Katia Jindrich, Selene L Fernandez-Valverde, Kathrein E Roper, Bernard M Degnan, Miloš Tanurdžić
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2017-04-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/22194
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author Federico Gaiti
Katia Jindrich
Selene L Fernandez-Valverde
Kathrein E Roper
Bernard M Degnan
Miloš Tanurdžić
author_facet Federico Gaiti
Katia Jindrich
Selene L Fernandez-Valverde
Kathrein E Roper
Bernard M Degnan
Miloš Tanurdžić
author_sort Federico Gaiti
collection DOAJ
description 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 Amphimedonqueenslandica, 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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spelling doaj.art-bc1ab89c8cb545fe9e5e99034fafc4842022-12-22T03:24:27ZengeLife Sciences Publications LtdeLife2050-084X2017-04-01610.7554/eLife.22194Landscape of histone modifications in a sponge reveals the origin of animal cis-regulatory complexityFederico Gaiti0https://orcid.org/0000-0001-5111-8816Katia Jindrich1Selene L Fernandez-Valverde2Kathrein E Roper3Bernard M Degnan4Miloš Tanurdžić5https://orcid.org/0000-0002-7564-0868School of Biological Sciences, University of Queensland, Brisbane, AustraliaSchool of Biological Sciences, University of Queensland, Brisbane, AustraliaSchool of Biological Sciences, University of Queensland, Brisbane, AustraliaSchool of Biological Sciences, University of Queensland, Brisbane, AustraliaSchool of Biological Sciences, University of Queensland, Brisbane, AustraliaSchool of Biological Sciences, University of Queensland, Brisbane, AustraliaCombinatorial 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 Amphimedonqueenslandica, 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.https://elifesciences.org/articles/22194A. queenslandicaevolution of multicellularityhistone modificationscis-regulationenhancersgene expression
spellingShingle Federico Gaiti
Katia Jindrich
Selene L Fernandez-Valverde
Kathrein E Roper
Bernard M Degnan
Miloš Tanurdžić
Landscape of histone modifications in a sponge reveals the origin of animal cis-regulatory complexity
eLife
A. queenslandica
evolution of multicellularity
histone modifications
cis-regulation
enhancers
gene expression
title Landscape of histone modifications in a sponge reveals the origin of animal cis-regulatory complexity
title_full Landscape of histone modifications in a sponge reveals the origin of animal cis-regulatory complexity
title_fullStr Landscape of histone modifications in a sponge reveals the origin of animal cis-regulatory complexity
title_full_unstemmed Landscape of histone modifications in a sponge reveals the origin of animal cis-regulatory complexity
title_short Landscape of histone modifications in a sponge reveals the origin of animal cis-regulatory complexity
title_sort landscape of histone modifications in a sponge reveals the origin of animal cis regulatory complexity
topic A. queenslandica
evolution of multicellularity
histone modifications
cis-regulation
enhancers
gene expression
url https://elifesciences.org/articles/22194
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AT kathreineroper landscapeofhistonemodificationsinaspongerevealstheoriginofanimalcisregulatorycomplexity
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