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Recent and dynamic transposable elements contribute to genomic divergence under asexuality

BACKGROUND: Transposable elements (TEs) are mobile pieces of genetic information with high mutagenic potential for the host genome. Transposition is often neutral or deleterious but may also generate potentially adaptive genetic variation. This additional source of variation could be especially rele...

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Autores principales: Ferreira de Carvalho, Julie, de Jager, Victor, van Gurp, Thomas P., Wagemaker, Niels C. A. M., Verhoeven, Koen J. F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5100183/
https://www.ncbi.nlm.nih.gov/pubmed/27821059
http://dx.doi.org/10.1186/s12864-016-3234-9
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author Ferreira de Carvalho, Julie
de Jager, Victor
van Gurp, Thomas P.
Wagemaker, Niels C. A. M.
Verhoeven, Koen J. F.
author_facet Ferreira de Carvalho, Julie
de Jager, Victor
van Gurp, Thomas P.
Wagemaker, Niels C. A. M.
Verhoeven, Koen J. F.
author_sort Ferreira de Carvalho, Julie
collection PubMed
description BACKGROUND: Transposable elements (TEs) are mobile pieces of genetic information with high mutagenic potential for the host genome. Transposition is often neutral or deleterious but may also generate potentially adaptive genetic variation. This additional source of variation could be especially relevant in non-recombining species reproducing asexually. However, evidence is lacking to determine the relevance of TEs in plant asexual genome evolution and their associated effects. Here, we characterize the repetitive fraction of the genome of the common dandelion, Taraxacum officinale and compare it between five accessions from the same apomictic lineage. The main objective of this study is to evaluate the extent of within-lineage divergence attributed to TE content and activity. We examined the repetitive genomic contribution, diversity, transcription and methylation changes to characterize accession-specific TEs. RESULTS: Using low-coverage genomic sequencing, we report a highly heterogeneous TE compartment in the triploid apomict T. officinale representing up to 38.6 % of the homoploid genome. The repetitive compartment is dominated by LTR retrotransposon families accompanied by few non-LTR retrotransposons and DNA transposons. Up to half of the repeat clusters are biased towards very high read identity, indicating recent and potentially ongoing activity of these TE families. Interestingly, the five accessions are divided into two main clades based on their TE composition. Clade 2 is more dynamic than clade 1 with higher abundance of Gypsy Chromovirus sequences and transposons. Furthermore, a few low-abundant genomic TE clusters exhibit high level of transcription in two of the accessions analysed. Using reduced representation bisulfite sequencing, we detected 18.9 % of loci differentially methylated, of which 25.4 and 40.7 % are annotated as TEs or functional genes, respectively. Additionally, we show clear evidence for accession-specific TE families that are differentially transcribed and differentially methylated within the apomictic lineage, including one Copia Ale II LTR element and a PIF-Harbinger DNA transposon. CONCLUSION: We report here a very young and dynamic repetitive compartment that enhances divergence within one asexual lineage of T. officinale. We speculate that accession-specific TE families that are both transcriptionally and epigenetically variable are more prone to trigger changes in expression on nearby coding sequences. These findings emphasize the potential of TE-induced mutations on functional genes during asexual genome evolution. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-3234-9) contains supplementary material, which is available to authorized users.
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spelling pubmed-51001832016-11-08 Recent and dynamic transposable elements contribute to genomic divergence under asexuality Ferreira de Carvalho, Julie de Jager, Victor van Gurp, Thomas P. Wagemaker, Niels C. A. M. Verhoeven, Koen J. F. BMC Genomics Research Article BACKGROUND: Transposable elements (TEs) are mobile pieces of genetic information with high mutagenic potential for the host genome. Transposition is often neutral or deleterious but may also generate potentially adaptive genetic variation. This additional source of variation could be especially relevant in non-recombining species reproducing asexually. However, evidence is lacking to determine the relevance of TEs in plant asexual genome evolution and their associated effects. Here, we characterize the repetitive fraction of the genome of the common dandelion, Taraxacum officinale and compare it between five accessions from the same apomictic lineage. The main objective of this study is to evaluate the extent of within-lineage divergence attributed to TE content and activity. We examined the repetitive genomic contribution, diversity, transcription and methylation changes to characterize accession-specific TEs. RESULTS: Using low-coverage genomic sequencing, we report a highly heterogeneous TE compartment in the triploid apomict T. officinale representing up to 38.6 % of the homoploid genome. The repetitive compartment is dominated by LTR retrotransposon families accompanied by few non-LTR retrotransposons and DNA transposons. Up to half of the repeat clusters are biased towards very high read identity, indicating recent and potentially ongoing activity of these TE families. Interestingly, the five accessions are divided into two main clades based on their TE composition. Clade 2 is more dynamic than clade 1 with higher abundance of Gypsy Chromovirus sequences and transposons. Furthermore, a few low-abundant genomic TE clusters exhibit high level of transcription in two of the accessions analysed. Using reduced representation bisulfite sequencing, we detected 18.9 % of loci differentially methylated, of which 25.4 and 40.7 % are annotated as TEs or functional genes, respectively. Additionally, we show clear evidence for accession-specific TE families that are differentially transcribed and differentially methylated within the apomictic lineage, including one Copia Ale II LTR element and a PIF-Harbinger DNA transposon. CONCLUSION: We report here a very young and dynamic repetitive compartment that enhances divergence within one asexual lineage of T. officinale. We speculate that accession-specific TE families that are both transcriptionally and epigenetically variable are more prone to trigger changes in expression on nearby coding sequences. These findings emphasize the potential of TE-induced mutations on functional genes during asexual genome evolution. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-3234-9) contains supplementary material, which is available to authorized users. BioMed Central 2016-11-07 /pmc/articles/PMC5100183/ /pubmed/27821059 http://dx.doi.org/10.1186/s12864-016-3234-9 Text en © The Author(s). 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
Ferreira de Carvalho, Julie
de Jager, Victor
van Gurp, Thomas P.
Wagemaker, Niels C. A. M.
Verhoeven, Koen J. F.
Recent and dynamic transposable elements contribute to genomic divergence under asexuality
title Recent and dynamic transposable elements contribute to genomic divergence under asexuality
title_full Recent and dynamic transposable elements contribute to genomic divergence under asexuality
title_fullStr Recent and dynamic transposable elements contribute to genomic divergence under asexuality
title_full_unstemmed Recent and dynamic transposable elements contribute to genomic divergence under asexuality
title_short Recent and dynamic transposable elements contribute to genomic divergence under asexuality
title_sort recent and dynamic transposable elements contribute to genomic divergence under asexuality
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5100183/
https://www.ncbi.nlm.nih.gov/pubmed/27821059
http://dx.doi.org/10.1186/s12864-016-3234-9
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