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Environmental response in gene expression and DNA methylation reveals factors influencing the adaptive potential of Arabidopsis lyrata

Understanding what factors influence plastic and genetic variation is valuable for predicting how organisms respond to changes in the selective environment. Here, using gene expression and DNA methylation as molecular phenotypes, we study environmentally induced variation among Arabidopsis lyrata pl...

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Autores principales: Hämälä, Tuomas, Ning, Weixuan, Kuittinen, Helmi, Aryamanesh, Nader, Savolainen, Outi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9616567/
https://www.ncbi.nlm.nih.gov/pubmed/36306157
http://dx.doi.org/10.7554/eLife.83115
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author Hämälä, Tuomas
Ning, Weixuan
Kuittinen, Helmi
Aryamanesh, Nader
Savolainen, Outi
author_facet Hämälä, Tuomas
Ning, Weixuan
Kuittinen, Helmi
Aryamanesh, Nader
Savolainen, Outi
author_sort Hämälä, Tuomas
collection PubMed
description Understanding what factors influence plastic and genetic variation is valuable for predicting how organisms respond to changes in the selective environment. Here, using gene expression and DNA methylation as molecular phenotypes, we study environmentally induced variation among Arabidopsis lyrata plants grown at lowland and alpine field sites. Our results show that gene expression is highly plastic, as many more genes are differentially expressed between the field sites than between populations. These environmentally responsive genes evolve under strong selective constraint – the strength of purifying selection on the coding sequence is high, while the rate of adaptive evolution is low. We find, however, that positive selection on cis-regulatory variants has likely contributed to the maintenance of genetically variable environmental responses, but such variants segregate only between distantly related populations. In contrast to gene expression, DNA methylation at genic regions is largely insensitive to the environment, and plastic methylation changes are not associated with differential gene expression. Besides genes, we detect environmental effects at transposable elements (TEs): TEs at the high-altitude field site have higher expression and methylation levels, suggestive of a broad-scale TE activation. Compared to the lowland population, plants native to the alpine environment harbor an excess of recent TE insertions, and we observe that specific TE families are enriched within environmentally responsive genes. Our findings provide insight into selective forces shaping plastic and genetic variation. We also highlight how plastic responses at TEs can rapidly create novel heritable variation in stressful conditions.
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spelling pubmed-96165672022-10-29 Environmental response in gene expression and DNA methylation reveals factors influencing the adaptive potential of Arabidopsis lyrata Hämälä, Tuomas Ning, Weixuan Kuittinen, Helmi Aryamanesh, Nader Savolainen, Outi eLife Evolutionary Biology Understanding what factors influence plastic and genetic variation is valuable for predicting how organisms respond to changes in the selective environment. Here, using gene expression and DNA methylation as molecular phenotypes, we study environmentally induced variation among Arabidopsis lyrata plants grown at lowland and alpine field sites. Our results show that gene expression is highly plastic, as many more genes are differentially expressed between the field sites than between populations. These environmentally responsive genes evolve under strong selective constraint – the strength of purifying selection on the coding sequence is high, while the rate of adaptive evolution is low. We find, however, that positive selection on cis-regulatory variants has likely contributed to the maintenance of genetically variable environmental responses, but such variants segregate only between distantly related populations. In contrast to gene expression, DNA methylation at genic regions is largely insensitive to the environment, and plastic methylation changes are not associated with differential gene expression. Besides genes, we detect environmental effects at transposable elements (TEs): TEs at the high-altitude field site have higher expression and methylation levels, suggestive of a broad-scale TE activation. Compared to the lowland population, plants native to the alpine environment harbor an excess of recent TE insertions, and we observe that specific TE families are enriched within environmentally responsive genes. Our findings provide insight into selective forces shaping plastic and genetic variation. We also highlight how plastic responses at TEs can rapidly create novel heritable variation in stressful conditions. eLife Sciences Publications, Ltd 2022-10-28 /pmc/articles/PMC9616567/ /pubmed/36306157 http://dx.doi.org/10.7554/eLife.83115 Text en © 2022, Hämälä et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Evolutionary Biology
Hämälä, Tuomas
Ning, Weixuan
Kuittinen, Helmi
Aryamanesh, Nader
Savolainen, Outi
Environmental response in gene expression and DNA methylation reveals factors influencing the adaptive potential of Arabidopsis lyrata
title Environmental response in gene expression and DNA methylation reveals factors influencing the adaptive potential of Arabidopsis lyrata
title_full Environmental response in gene expression and DNA methylation reveals factors influencing the adaptive potential of Arabidopsis lyrata
title_fullStr Environmental response in gene expression and DNA methylation reveals factors influencing the adaptive potential of Arabidopsis lyrata
title_full_unstemmed Environmental response in gene expression and DNA methylation reveals factors influencing the adaptive potential of Arabidopsis lyrata
title_short Environmental response in gene expression and DNA methylation reveals factors influencing the adaptive potential of Arabidopsis lyrata
title_sort environmental response in gene expression and dna methylation reveals factors influencing the adaptive potential of arabidopsis lyrata
topic Evolutionary Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9616567/
https://www.ncbi.nlm.nih.gov/pubmed/36306157
http://dx.doi.org/10.7554/eLife.83115
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