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Natural selection in a population of Drosophila melanogaster explained by changes in gene expression caused by sequence variation in core promoter regions

BACKGROUND: Understanding the evolutionary forces that influence variation in gene regulatory regions in natural populations is an important challenge for evolutionary biology because natural selection for such variations could promote adaptive phenotypic evolution. Recently, whole-genome sequence a...

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Autores principales: Sato, Mitsuhiko P., Makino, Takashi, Kawata, Masakado
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4748610/
https://www.ncbi.nlm.nih.gov/pubmed/26860869
http://dx.doi.org/10.1186/s12862-016-0606-3
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author Sato, Mitsuhiko P.
Makino, Takashi
Kawata, Masakado
author_facet Sato, Mitsuhiko P.
Makino, Takashi
Kawata, Masakado
author_sort Sato, Mitsuhiko P.
collection PubMed
description BACKGROUND: Understanding the evolutionary forces that influence variation in gene regulatory regions in natural populations is an important challenge for evolutionary biology because natural selection for such variations could promote adaptive phenotypic evolution. Recently, whole-genome sequence analyses have identified regulatory regions subject to natural selection. However, these studies could not identify the relationship between sequence variation in the detected regions and change in gene expression levels. We analyzed sequence variations in core promoter regions, which are critical regions for gene regulation in higher eukaryotes, in a natural population of Drosophila melanogaster, and identified core promoter sequence variations associated with differences in gene expression levels subjected to natural selection. RESULTS: Among the core promoter regions whose sequence variation could change transcription factor binding sites and explain differences in expression levels, three core promoter regions were detected as candidates associated with purifying selection or selective sweep and seven as candidates associated with balancing selection, excluding the possibility of linkage between these regions and core promoter regions. CHKov1, which confers resistance to the sigma virus and related insecticides, was identified as core promoter regions that has been subject to selective sweep, although it could not be denied that selection for variation in core promoter regions was due to linked single nucleotide polymorphisms in the regulatory region outside core promoter regions. Nucleotide changes in core promoter regions of CHKov1 caused the loss of two basal transcription factor binding sites and acquisition of one transcription factor binding site, resulting in decreased gene expression levels. Of nine core promoter regions regions associated with balancing selection, brat, and CG9044 are associated with neuromuscular junction development, and Nmda1 are associated with learning, behavioral plasticity, and memory. Diversity of neural and behavioral traits may have been maintained by balancing selection. CONCLUSIONS: Our results revealed the evolutionary process occurring by natural selection for differences in gene expression levels caused by sequence variation in core promoter regions in a natural population. The sequences of core promoter regions were diverse even within the population, possibly providing a source for natural selection. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0606-3) contains supplementary material, which is available to authorized users.
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spelling pubmed-47486102016-02-11 Natural selection in a population of Drosophila melanogaster explained by changes in gene expression caused by sequence variation in core promoter regions Sato, Mitsuhiko P. Makino, Takashi Kawata, Masakado BMC Evol Biol Research Article BACKGROUND: Understanding the evolutionary forces that influence variation in gene regulatory regions in natural populations is an important challenge for evolutionary biology because natural selection for such variations could promote adaptive phenotypic evolution. Recently, whole-genome sequence analyses have identified regulatory regions subject to natural selection. However, these studies could not identify the relationship between sequence variation in the detected regions and change in gene expression levels. We analyzed sequence variations in core promoter regions, which are critical regions for gene regulation in higher eukaryotes, in a natural population of Drosophila melanogaster, and identified core promoter sequence variations associated with differences in gene expression levels subjected to natural selection. RESULTS: Among the core promoter regions whose sequence variation could change transcription factor binding sites and explain differences in expression levels, three core promoter regions were detected as candidates associated with purifying selection or selective sweep and seven as candidates associated with balancing selection, excluding the possibility of linkage between these regions and core promoter regions. CHKov1, which confers resistance to the sigma virus and related insecticides, was identified as core promoter regions that has been subject to selective sweep, although it could not be denied that selection for variation in core promoter regions was due to linked single nucleotide polymorphisms in the regulatory region outside core promoter regions. Nucleotide changes in core promoter regions of CHKov1 caused the loss of two basal transcription factor binding sites and acquisition of one transcription factor binding site, resulting in decreased gene expression levels. Of nine core promoter regions regions associated with balancing selection, brat, and CG9044 are associated with neuromuscular junction development, and Nmda1 are associated with learning, behavioral plasticity, and memory. Diversity of neural and behavioral traits may have been maintained by balancing selection. CONCLUSIONS: Our results revealed the evolutionary process occurring by natural selection for differences in gene expression levels caused by sequence variation in core promoter regions in a natural population. The sequences of core promoter regions were diverse even within the population, possibly providing a source for natural selection. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0606-3) contains supplementary material, which is available to authorized users. BioMed Central 2016-02-09 /pmc/articles/PMC4748610/ /pubmed/26860869 http://dx.doi.org/10.1186/s12862-016-0606-3 Text en © Sato et al. 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Sato, Mitsuhiko P.
Makino, Takashi
Kawata, Masakado
Natural selection in a population of Drosophila melanogaster explained by changes in gene expression caused by sequence variation in core promoter regions
title Natural selection in a population of Drosophila melanogaster explained by changes in gene expression caused by sequence variation in core promoter regions
title_full Natural selection in a population of Drosophila melanogaster explained by changes in gene expression caused by sequence variation in core promoter regions
title_fullStr Natural selection in a population of Drosophila melanogaster explained by changes in gene expression caused by sequence variation in core promoter regions
title_full_unstemmed Natural selection in a population of Drosophila melanogaster explained by changes in gene expression caused by sequence variation in core promoter regions
title_short Natural selection in a population of Drosophila melanogaster explained by changes in gene expression caused by sequence variation in core promoter regions
title_sort natural selection in a population of drosophila melanogaster explained by changes in gene expression caused by sequence variation in core promoter regions
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4748610/
https://www.ncbi.nlm.nih.gov/pubmed/26860869
http://dx.doi.org/10.1186/s12862-016-0606-3
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