Long-term experimental evolution reveals purifying selection on piRNA-mediated control of transposable element expression
Abstract Background Transposable elements (TEs) are an almost universal constituent of eukaryotic genomes. In animals, Piwi-interacting small RNAs (piRNAs) and repressive chromatin often play crucial roles in preventing TE transcription and thus restricting TE activity. Nevertheless, TE content vari...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2020-11-01
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| Series: | BMC Biology |
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| Online Access: | http://link.springer.com/article/10.1186/s12915-020-00897-y |
| _version_ | 1818151521604337664 |
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| author | Ulfar Bergthorsson Caroline J. Sheeba Anke Konrad Tony Belicard Toni Beltran Vaishali Katju Peter Sarkies |
| author_facet | Ulfar Bergthorsson Caroline J. Sheeba Anke Konrad Tony Belicard Toni Beltran Vaishali Katju Peter Sarkies |
| author_sort | Ulfar Bergthorsson |
| collection | DOAJ |
| description | Abstract Background Transposable elements (TEs) are an almost universal constituent of eukaryotic genomes. In animals, Piwi-interacting small RNAs (piRNAs) and repressive chromatin often play crucial roles in preventing TE transcription and thus restricting TE activity. Nevertheless, TE content varies widely across eukaryotes and the dynamics of TE activity and TE silencing across evolutionary time is poorly understood. Results Here, we used experimentally evolved populations of C. elegans to study the dynamics of TE expression over 409 generations. The experimental populations were evolved at population sizes of 1, 10 and 100 individuals to manipulate the efficiency of natural selection versus genetic drift. We demonstrate increased TE expression relative to the ancestral population, with the largest increases occurring in the smallest populations. We show that the transcriptional activation of TEs within active regions of the genome is associated with failure of piRNA-mediated silencing, whilst desilenced TEs in repressed chromatin domains retain small RNAs. Additionally, we find that the sequence context of the surrounding region influences the propensity of TEs to lose silencing through failure of small RNA-mediated silencing. Conclusions Our results show that natural selection in C. elegans is responsible for maintaining low levels of TE expression, and provide new insights into the epigenomic features responsible. |
| first_indexed | 2024-12-11T13:40:09Z |
| format | Article |
| id | doaj.art-323ddc11421c48e49e5b2465523f1783 |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-12-11T13:40:09Z |
| publishDate | 2020-11-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-323ddc11421c48e49e5b2465523f17832022-12-22T01:04:49ZengBMCBMC Biology1741-70072020-11-0118111710.1186/s12915-020-00897-yLong-term experimental evolution reveals purifying selection on piRNA-mediated control of transposable element expressionUlfar Bergthorsson0Caroline J. Sheeba1Anke Konrad2Tony Belicard3Toni Beltran4Vaishali Katju5Peter Sarkies6Department of Veterinary Integrative Biosciences, Texas A&M UniversityMRC London Institute of Medical SciencesDepartment of Veterinary Integrative Biosciences, Texas A&M UniversityMRC London Institute of Medical SciencesMRC London Institute of Medical SciencesDepartment of Veterinary Integrative Biosciences, Texas A&M UniversityMRC London Institute of Medical SciencesAbstract Background Transposable elements (TEs) are an almost universal constituent of eukaryotic genomes. In animals, Piwi-interacting small RNAs (piRNAs) and repressive chromatin often play crucial roles in preventing TE transcription and thus restricting TE activity. Nevertheless, TE content varies widely across eukaryotes and the dynamics of TE activity and TE silencing across evolutionary time is poorly understood. Results Here, we used experimentally evolved populations of C. elegans to study the dynamics of TE expression over 409 generations. The experimental populations were evolved at population sizes of 1, 10 and 100 individuals to manipulate the efficiency of natural selection versus genetic drift. We demonstrate increased TE expression relative to the ancestral population, with the largest increases occurring in the smallest populations. We show that the transcriptional activation of TEs within active regions of the genome is associated with failure of piRNA-mediated silencing, whilst desilenced TEs in repressed chromatin domains retain small RNAs. Additionally, we find that the sequence context of the surrounding region influences the propensity of TEs to lose silencing through failure of small RNA-mediated silencing. Conclusions Our results show that natural selection in C. elegans is responsible for maintaining low levels of TE expression, and provide new insights into the epigenomic features responsible.http://link.springer.com/article/10.1186/s12915-020-00897-yC. elegansExperimental evolutionTransposable elementsEpigeneticsSmall RNAspiRNAs |
| spellingShingle | Ulfar Bergthorsson Caroline J. Sheeba Anke Konrad Tony Belicard Toni Beltran Vaishali Katju Peter Sarkies Long-term experimental evolution reveals purifying selection on piRNA-mediated control of transposable element expression BMC Biology C. elegans Experimental evolution Transposable elements Epigenetics Small RNAs piRNAs |
| title | Long-term experimental evolution reveals purifying selection on piRNA-mediated control of transposable element expression |
| title_full | Long-term experimental evolution reveals purifying selection on piRNA-mediated control of transposable element expression |
| title_fullStr | Long-term experimental evolution reveals purifying selection on piRNA-mediated control of transposable element expression |
| title_full_unstemmed | Long-term experimental evolution reveals purifying selection on piRNA-mediated control of transposable element expression |
| title_short | Long-term experimental evolution reveals purifying selection on piRNA-mediated control of transposable element expression |
| title_sort | long term experimental evolution reveals purifying selection on pirna mediated control of transposable element expression |
| topic | C. elegans Experimental evolution Transposable elements Epigenetics Small RNAs piRNAs |
| url | http://link.springer.com/article/10.1186/s12915-020-00897-y |
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