Capture of a functionally active methyl-CpG binding domain by an arthropod retrotransposon family

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Abstract

The repressive capacity of cytosine DNA methylation is mediated by recruitment of silencing complexes by methyl-CpG binding domain (MBD) proteins. We discovered that a family of arthropod Copia retrotransposons have incorporated a host-derived MBD domain. We functionally demonstrate how retrotransposon encoded MBDs preferentially bind to CpG-dense methylated regions, which correspond to transposable element regions of the host genome, in the myriapod Strigamia maritima Consistently, MBD-encoding Copia retrotransposons (CopiaMBD) are inserted in regions with higher CpG-densities than other LTR elements. This suggests that retrotransposons use MBDs to integrate into heterochromatic regions in Strigamia, avoiding potentially harmful insertions into host genes. In contrast, CopiaMBD insertions in the spider Stegodyphus dumicola genome accumulate in methylated gene bodies, given that transposons are not actively targeted by DNA methylation in the spider genome. Together, these data demonstrate that retrotransposons can co-opt host-derived epigenome readers, harnessing the host epigenome landscape to advantageously tune the retrotransposition process.

Original languageEnglish
Pages (from-to)1277-1286
JournalGenome Research
Volume29
Issue number8
Early online date25 Jun 2019
DOIs
Publication statusPublished - Aug 2019

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Retroelements
Arthropods
Spiders
Genome
DNA Methylation
DNA Transposable Elements
Cytosine
Genes
Carrier Proteins
Methyl CpG Binding Domain

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title = "Capture of a functionally active methyl-CpG binding domain by an arthropod retrotransposon family",
abstract = "The repressive capacity of cytosine DNA methylation is mediated by recruitment of silencing complexes by methyl-CpG binding domain (MBD) proteins. We discovered that a family of arthropod Copia retrotransposons have incorporated a host-derived MBD domain. We functionally demonstrate how retrotransposon encoded MBDs preferentially bind to CpG-dense methylated regions, which correspond to transposable element regions of the host genome, in the myriapod Strigamia maritima Consistently, MBD-encoding Copia retrotransposons (CopiaMBD) are inserted in regions with higher CpG-densities than other LTR elements. This suggests that retrotransposons use MBDs to integrate into heterochromatic regions in Strigamia, avoiding potentially harmful insertions into host genes. In contrast, CopiaMBD insertions in the spider Stegodyphus dumicola genome accumulate in methylated gene bodies, given that transposons are not actively targeted by DNA methylation in the spider genome. Together, these data demonstrate that retrotransposons can co-opt host-derived epigenome readers, harnessing the host epigenome landscape to advantageously tune the retrotransposition process.",
author = "{de Mendoza}, Alex and Jahnvi Pflueger and Ryan Lister",
year = "2019",
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TY - JOUR

T1 - Capture of a functionally active methyl-CpG binding domain by an arthropod retrotransposon family

AU - de Mendoza, Alex

AU - Pflueger, Jahnvi

AU - Lister, Ryan

PY - 2019/8

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N2 - The repressive capacity of cytosine DNA methylation is mediated by recruitment of silencing complexes by methyl-CpG binding domain (MBD) proteins. We discovered that a family of arthropod Copia retrotransposons have incorporated a host-derived MBD domain. We functionally demonstrate how retrotransposon encoded MBDs preferentially bind to CpG-dense methylated regions, which correspond to transposable element regions of the host genome, in the myriapod Strigamia maritima Consistently, MBD-encoding Copia retrotransposons (CopiaMBD) are inserted in regions with higher CpG-densities than other LTR elements. This suggests that retrotransposons use MBDs to integrate into heterochromatic regions in Strigamia, avoiding potentially harmful insertions into host genes. In contrast, CopiaMBD insertions in the spider Stegodyphus dumicola genome accumulate in methylated gene bodies, given that transposons are not actively targeted by DNA methylation in the spider genome. Together, these data demonstrate that retrotransposons can co-opt host-derived epigenome readers, harnessing the host epigenome landscape to advantageously tune the retrotransposition process.

AB - The repressive capacity of cytosine DNA methylation is mediated by recruitment of silencing complexes by methyl-CpG binding domain (MBD) proteins. We discovered that a family of arthropod Copia retrotransposons have incorporated a host-derived MBD domain. We functionally demonstrate how retrotransposon encoded MBDs preferentially bind to CpG-dense methylated regions, which correspond to transposable element regions of the host genome, in the myriapod Strigamia maritima Consistently, MBD-encoding Copia retrotransposons (CopiaMBD) are inserted in regions with higher CpG-densities than other LTR elements. This suggests that retrotransposons use MBDs to integrate into heterochromatic regions in Strigamia, avoiding potentially harmful insertions into host genes. In contrast, CopiaMBD insertions in the spider Stegodyphus dumicola genome accumulate in methylated gene bodies, given that transposons are not actively targeted by DNA methylation in the spider genome. Together, these data demonstrate that retrotransposons can co-opt host-derived epigenome readers, harnessing the host epigenome landscape to advantageously tune the retrotransposition process.

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