Synthetic circuits reveal how mechanisms of gene regulatory networks constrain evolution

Abstract Phenotypic variation is the raw material of adaptive Darwinian evolution. The phenotypic variation found in organismal development is biased towards certain phenotypes, but the molecular mechanisms behind such biases are still poorly understood. Gene regulatory networks have been proposed a...

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Main Authors: Yolanda Schaerli, Alba Jiménez, José M Duarte, Ljiljana Mihajlovic, Julien Renggli, Mark Isalan, James Sharpe, Andreas Wagner
Format: Article
Language:English
Published: Springer Nature 2018-09-01
Series:Molecular Systems Biology
Subjects:
Online Access:https://doi.org/10.15252/msb.20178102
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author Yolanda Schaerli
Alba Jiménez
José M Duarte
Ljiljana Mihajlovic
Julien Renggli
Mark Isalan
James Sharpe
Andreas Wagner
author_facet Yolanda Schaerli
Alba Jiménez
José M Duarte
Ljiljana Mihajlovic
Julien Renggli
Mark Isalan
James Sharpe
Andreas Wagner
author_sort Yolanda Schaerli
collection DOAJ
description Abstract Phenotypic variation is the raw material of adaptive Darwinian evolution. The phenotypic variation found in organismal development is biased towards certain phenotypes, but the molecular mechanisms behind such biases are still poorly understood. Gene regulatory networks have been proposed as one cause of constrained phenotypic variation. However, most pertinent evidence is theoretical rather than experimental. Here, we study evolutionary biases in two synthetic gene regulatory circuits expressed in Escherichia coli that produce a gene expression stripe—a pivotal pattern in embryonic development. The two parental circuits produce the same phenotype, but create it through different regulatory mechanisms. We show that mutations cause distinct novel phenotypes in the two networks and use a combination of experimental measurements, mathematical modelling and DNA sequencing to understand why mutations bring forth only some but not other novel gene expression phenotypes. Our results reveal that the regulatory mechanisms of networks restrict the possible phenotypic variation upon mutation. Consequently, seemingly equivalent networks can indeed be distinct in how they constrain the outcome of further evolution.
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spelling doaj-art-c164d92a7ca6416bbea3fd62ef8230e62025-08-20T03:43:31ZengSpringer NatureMolecular Systems Biology1744-42922018-09-0114911810.15252/msb.20178102Synthetic circuits reveal how mechanisms of gene regulatory networks constrain evolutionYolanda Schaerli0Alba Jiménez1José M Duarte2Ljiljana Mihajlovic3Julien Renggli4Mark Isalan5James Sharpe6Andreas Wagner7Department of Fundamental Microbiology, University of LausanneSystems Biology Program, Centre for Genomic Regulation (CRG), Universitat Pompeu FabraDepartment of Evolutionary Biology and Environmental Studies, University of ZurichDepartment of Fundamental Microbiology, University of LausanneIndependent ResearcherDepartment of Life Sciences, Imperial College LondonSystems Biology Program, Centre for Genomic Regulation (CRG), Universitat Pompeu FabraDepartment of Evolutionary Biology and Environmental Studies, University of ZurichAbstract Phenotypic variation is the raw material of adaptive Darwinian evolution. The phenotypic variation found in organismal development is biased towards certain phenotypes, but the molecular mechanisms behind such biases are still poorly understood. Gene regulatory networks have been proposed as one cause of constrained phenotypic variation. However, most pertinent evidence is theoretical rather than experimental. Here, we study evolutionary biases in two synthetic gene regulatory circuits expressed in Escherichia coli that produce a gene expression stripe—a pivotal pattern in embryonic development. The two parental circuits produce the same phenotype, but create it through different regulatory mechanisms. We show that mutations cause distinct novel phenotypes in the two networks and use a combination of experimental measurements, mathematical modelling and DNA sequencing to understand why mutations bring forth only some but not other novel gene expression phenotypes. Our results reveal that the regulatory mechanisms of networks restrict the possible phenotypic variation upon mutation. Consequently, seemingly equivalent networks can indeed be distinct in how they constrain the outcome of further evolution.https://doi.org/10.15252/msb.20178102constrained evolutionepistasisgene regulatory networksregulatory mechanismssynthetic circuits
spellingShingle Yolanda Schaerli
Alba Jiménez
José M Duarte
Ljiljana Mihajlovic
Julien Renggli
Mark Isalan
James Sharpe
Andreas Wagner
Synthetic circuits reveal how mechanisms of gene regulatory networks constrain evolution
Molecular Systems Biology
constrained evolution
epistasis
gene regulatory networks
regulatory mechanisms
synthetic circuits
title Synthetic circuits reveal how mechanisms of gene regulatory networks constrain evolution
title_full Synthetic circuits reveal how mechanisms of gene regulatory networks constrain evolution
title_fullStr Synthetic circuits reveal how mechanisms of gene regulatory networks constrain evolution
title_full_unstemmed Synthetic circuits reveal how mechanisms of gene regulatory networks constrain evolution
title_short Synthetic circuits reveal how mechanisms of gene regulatory networks constrain evolution
title_sort synthetic circuits reveal how mechanisms of gene regulatory networks constrain evolution
topic constrained evolution
epistasis
gene regulatory networks
regulatory mechanisms
synthetic circuits
url https://doi.org/10.15252/msb.20178102
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