Promoter nucleosome organization shapes the evolution of gene expression.

Understanding why genes evolve at different rates is fundamental to evolutionary thinking. In species of the budding yeast, the rate at which genes diverge in expression correlates with the organization of their promoter nucleosomes: genes lacking a nucleosome-free region (denoted OPN for "Occu...

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Main Authors: Dalia Rosin, Gil Hornung, Itay Tirosh, Ariel Gispan, Naama Barkai
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC3305400?pdf=render
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spelling doaj-382b2af842e7492cb8d3d9743f2b84fb2020-11-25T02:29:18ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042012-01-0183e100257910.1371/journal.pgen.1002579Promoter nucleosome organization shapes the evolution of gene expression.Dalia RosinGil HornungItay TiroshAriel GispanNaama BarkaiUnderstanding why genes evolve at different rates is fundamental to evolutionary thinking. In species of the budding yeast, the rate at which genes diverge in expression correlates with the organization of their promoter nucleosomes: genes lacking a nucleosome-free region (denoted OPN for "Occupied Proximal Nucleosomes") vary widely between the species, while the expression of those containing NFR (denoted DPN for "Depleted Proximal Nucleosomes") remains largely conserved. To examine if early evolutionary dynamics contributes to this difference in divergence, we artificially selected for high expression of GFP-fused proteins. Surprisingly, selection was equally successful for OPN and DPN genes, with -80% of genes in each group stably increasing in expression by a similar amount. Notably, the two groups adapted by distinct mechanisms: DPN-selected strains duplicated large genomic regions, while OPN-selected strains favored trans mutations not involving duplications. When selection was removed, DPN (but not OPN) genes reverted rapidly to wild-type expression levels, consistent with their lower diversity between species. Our results suggest that promoter organization constrains the early evolutionary dynamics and in this way biases the path of long-term evolution.http://europepmc.org/articles/PMC3305400?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Dalia Rosin
Gil Hornung
Itay Tirosh
Ariel Gispan
Naama Barkai
spellingShingle Dalia Rosin
Gil Hornung
Itay Tirosh
Ariel Gispan
Naama Barkai
Promoter nucleosome organization shapes the evolution of gene expression.
PLoS Genetics
author_facet Dalia Rosin
Gil Hornung
Itay Tirosh
Ariel Gispan
Naama Barkai
author_sort Dalia Rosin
title Promoter nucleosome organization shapes the evolution of gene expression.
title_short Promoter nucleosome organization shapes the evolution of gene expression.
title_full Promoter nucleosome organization shapes the evolution of gene expression.
title_fullStr Promoter nucleosome organization shapes the evolution of gene expression.
title_full_unstemmed Promoter nucleosome organization shapes the evolution of gene expression.
title_sort promoter nucleosome organization shapes the evolution of gene expression.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2012-01-01
description Understanding why genes evolve at different rates is fundamental to evolutionary thinking. In species of the budding yeast, the rate at which genes diverge in expression correlates with the organization of their promoter nucleosomes: genes lacking a nucleosome-free region (denoted OPN for "Occupied Proximal Nucleosomes") vary widely between the species, while the expression of those containing NFR (denoted DPN for "Depleted Proximal Nucleosomes") remains largely conserved. To examine if early evolutionary dynamics contributes to this difference in divergence, we artificially selected for high expression of GFP-fused proteins. Surprisingly, selection was equally successful for OPN and DPN genes, with -80% of genes in each group stably increasing in expression by a similar amount. Notably, the two groups adapted by distinct mechanisms: DPN-selected strains duplicated large genomic regions, while OPN-selected strains favored trans mutations not involving duplications. When selection was removed, DPN (but not OPN) genes reverted rapidly to wild-type expression levels, consistent with their lower diversity between species. Our results suggest that promoter organization constrains the early evolutionary dynamics and in this way biases the path of long-term evolution.
url http://europepmc.org/articles/PMC3305400?pdf=render
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