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...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-10-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/83115 |
| _version_ | 1811335943294025728 |
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| author | Tuomas Hämälä Weixuan Ning Helmi Kuittinen Nader Aryamanesh Outi Savolainen |
| author_facet | Tuomas Hämälä Weixuan Ning Helmi Kuittinen Nader Aryamanesh Outi Savolainen |
| author_sort | Tuomas Hämälä |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-13T17:31:20Z |
| format | Article |
| id | doaj.art-40c3d031ca1945cbab030bccb7504e46 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-13T17:31:20Z |
| publishDate | 2022-10-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-40c3d031ca1945cbab030bccb7504e462022-12-22T02:37:32ZengeLife Sciences Publications LtdeLife2050-084X2022-10-011110.7554/eLife.83115Environmental response in gene expression and DNA methylation reveals factors influencing the adaptive potential of Arabidopsis lyrataTuomas Hämälä0https://orcid.org/0000-0001-8306-3397Weixuan Ning1Helmi Kuittinen2Nader Aryamanesh3Outi Savolainen4Department of Ecology and Genetics, University of Oulu, Oulu, FinlandDepartment of Ecology and Genetics, University of Oulu, Oulu, FinlandDepartment of Ecology and Genetics, University of Oulu, Oulu, FinlandDepartment of Ecology and Genetics, University of Oulu, Oulu, FinlandDepartment of Ecology and Genetics, University of Oulu, Oulu, FinlandUnderstanding 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.https://elifesciences.org/articles/83115reciprocal transplantDNA methylationgene expressionArabidopsis lyrataselective constraintlocal adaptation |
| spellingShingle | Tuomas Hämälä Weixuan Ning Helmi Kuittinen Nader Aryamanesh Outi Savolainen Environmental response in gene expression and DNA methylation reveals factors influencing the adaptive potential of Arabidopsis lyrata eLife reciprocal transplant DNA methylation gene expression Arabidopsis lyrata selective constraint local adaptation |
| 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 | reciprocal transplant DNA methylation gene expression Arabidopsis lyrata selective constraint local adaptation |
| url | https://elifesciences.org/articles/83115 |
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