The somatic piRNA pathway controls germline transposition over generations
Abstract Transposable elements (TEs) are parasitic DNA sequences that threaten genome integrity by replicative transposition in host gonads. The Piwi-interacting RNAs (piRNAs) pathway is assumed to maintain Drosophila genome homeostasis by downregulating transcriptional and post-transcriptional TE e...
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Veröffentlicht in: | Nucleic acids research 2018-10, Vol.46 (18), p.9524-9536 |
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creator | Barckmann, Bridlin El-Barouk, Marianne Pélisson, Alain Mugat, Bruno Li, Blaise Franckhauser, Céline Fiston Lavier, Anna-Sophie Mirouze, Marie Fablet, Marie Chambeyron, Séverine |
description | Abstract
Transposable elements (TEs) are parasitic DNA sequences that threaten genome integrity by replicative transposition in host gonads. The Piwi-interacting RNAs (piRNAs) pathway is assumed to maintain Drosophila genome homeostasis by downregulating transcriptional and post-transcriptional TE expression in the ovary. However, the bursts of transposition that are expected to follow transposome derepression after piRNA pathway impairment have not yet been reported. Here, we show, at a genome-wide level, that piRNA loss in the ovarian somatic cells boosts several families of the endogenous retroviral subclass of TEs, at various steps of their replication cycle, from somatic transcription to germinal genome invasion. For some of these TEs, the derepression caused by the loss of piRNAs is backed up by another small RNA pathway (siRNAs) operating in somatic tissues at the post transcriptional level. Derepressed transposition during 70 successive generations of piRNA loss exponentially increases the genomic copy number by up to 10-fold. |
doi_str_mv | 10.1093/nar/gky761 |
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Transposable elements (TEs) are parasitic DNA sequences that threaten genome integrity by replicative transposition in host gonads. The Piwi-interacting RNAs (piRNAs) pathway is assumed to maintain Drosophila genome homeostasis by downregulating transcriptional and post-transcriptional TE expression in the ovary. However, the bursts of transposition that are expected to follow transposome derepression after piRNA pathway impairment have not yet been reported. Here, we show, at a genome-wide level, that piRNA loss in the ovarian somatic cells boosts several families of the endogenous retroviral subclass of TEs, at various steps of their replication cycle, from somatic transcription to germinal genome invasion. For some of these TEs, the derepression caused by the loss of piRNAs is backed up by another small RNA pathway (siRNAs) operating in somatic tissues at the post transcriptional level. Derepressed transposition during 70 successive generations of piRNA loss exponentially increases the genomic copy number by up to 10-fold.</description><identifier>ISSN: 0305-1048</identifier><identifier>EISSN: 1362-4962</identifier><identifier>DOI: 10.1093/nar/gky761</identifier><identifier>PMID: 30312469</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Biochemistry, Molecular Biology ; Botanics ; Genome Integrity, Repair and ; Genomics ; Life Sciences ; Vegetal Biology</subject><ispartof>Nucleic acids research, 2018-10, Vol.46 (18), p.9524-9536</ispartof><rights>The Author(s) 2018. Published by Oxford University Press on behalf of Nucleic Acids Research. 2018</rights><rights>Attribution</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c508t-ac0736441264ebece0b8a640f84dab04b69293143b71ab010a8ad59e20489da03</citedby><cites>FETCH-LOGICAL-c508t-ac0736441264ebece0b8a640f84dab04b69293143b71ab010a8ad59e20489da03</cites><orcidid>0000-0002-7306-6532 ; 0000-0003-3080-1899 ; 0000-0003-2775-6556 ; 0000-0002-7819-4541</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6182186/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6182186/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,1598,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30312469$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01904679$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Barckmann, Bridlin</creatorcontrib><creatorcontrib>El-Barouk, Marianne</creatorcontrib><creatorcontrib>Pélisson, Alain</creatorcontrib><creatorcontrib>Mugat, Bruno</creatorcontrib><creatorcontrib>Li, Blaise</creatorcontrib><creatorcontrib>Franckhauser, Céline</creatorcontrib><creatorcontrib>Fiston Lavier, Anna-Sophie</creatorcontrib><creatorcontrib>Mirouze, Marie</creatorcontrib><creatorcontrib>Fablet, Marie</creatorcontrib><creatorcontrib>Chambeyron, Séverine</creatorcontrib><title>The somatic piRNA pathway controls germline transposition over generations</title><title>Nucleic acids research</title><addtitle>Nucleic Acids Res</addtitle><description>Abstract
Transposable elements (TEs) are parasitic DNA sequences that threaten genome integrity by replicative transposition in host gonads. The Piwi-interacting RNAs (piRNAs) pathway is assumed to maintain Drosophila genome homeostasis by downregulating transcriptional and post-transcriptional TE expression in the ovary. However, the bursts of transposition that are expected to follow transposome derepression after piRNA pathway impairment have not yet been reported. Here, we show, at a genome-wide level, that piRNA loss in the ovarian somatic cells boosts several families of the endogenous retroviral subclass of TEs, at various steps of their replication cycle, from somatic transcription to germinal genome invasion. For some of these TEs, the derepression caused by the loss of piRNAs is backed up by another small RNA pathway (siRNAs) operating in somatic tissues at the post transcriptional level. Derepressed transposition during 70 successive generations of piRNA loss exponentially increases the genomic copy number by up to 10-fold.</description><subject>Biochemistry, Molecular Biology</subject><subject>Botanics</subject><subject>Genome Integrity, Repair and</subject><subject>Genomics</subject><subject>Life Sciences</subject><subject>Vegetal Biology</subject><issn>0305-1048</issn><issn>1362-4962</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><recordid>eNp9kU1rGzEQhkVISNy0l_yAsJdAW9hkRpLl1SVgQvOFaaGkZzG7lm21u6uNtHbxv4_MJiHtIScxmkfPaHgZO0E4R9DioqVwsfyznSjcYyMUiudSK77PRiBgnCPI4oh9iPE3AEocy0N2JEAgl0qP2P3DymbRN9S7Kuvcz-_TrKN-9Ze2WeXbPvg6Zksbmtq1NusDtbHz0fXOt5nf2JB6rQ20q-NHdrCgOtpPz-cx-3X97eHqNp_9uLm7ms7yagxFn1MFE6GkRK6kLW1loSxISVgUck4lyFJprgVKUU4w1QhU0HysLU976DmBOGaXg7dbl42dVzZ9k2rTBddQ2BpPzvzbad3KLP3GKCw4FioJvgyC1X_Pbqczs7sD1CDVRG8wsZ-fhwX_uLaxN42Lla1raq1fR8MRteYFCp3QrwNaBR9jsItXN4LZBWVSUGYIKsGnb5d4RV-SScDZAPh1957oCRyQnOM</recordid><startdate>20181012</startdate><enddate>20181012</enddate><creator>Barckmann, Bridlin</creator><creator>El-Barouk, Marianne</creator><creator>Pélisson, Alain</creator><creator>Mugat, Bruno</creator><creator>Li, Blaise</creator><creator>Franckhauser, Céline</creator><creator>Fiston Lavier, Anna-Sophie</creator><creator>Mirouze, Marie</creator><creator>Fablet, Marie</creator><creator>Chambeyron, Séverine</creator><general>Oxford University Press</general><scope>TOX</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-7306-6532</orcidid><orcidid>https://orcid.org/0000-0003-3080-1899</orcidid><orcidid>https://orcid.org/0000-0003-2775-6556</orcidid><orcidid>https://orcid.org/0000-0002-7819-4541</orcidid></search><sort><creationdate>20181012</creationdate><title>The somatic piRNA pathway controls germline transposition over generations</title><author>Barckmann, Bridlin ; El-Barouk, Marianne ; Pélisson, Alain ; Mugat, Bruno ; Li, Blaise ; Franckhauser, Céline ; Fiston Lavier, Anna-Sophie ; Mirouze, Marie ; Fablet, Marie ; Chambeyron, Séverine</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c508t-ac0736441264ebece0b8a640f84dab04b69293143b71ab010a8ad59e20489da03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Biochemistry, Molecular Biology</topic><topic>Botanics</topic><topic>Genome Integrity, Repair and</topic><topic>Genomics</topic><topic>Life Sciences</topic><topic>Vegetal Biology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Barckmann, Bridlin</creatorcontrib><creatorcontrib>El-Barouk, Marianne</creatorcontrib><creatorcontrib>Pélisson, Alain</creatorcontrib><creatorcontrib>Mugat, Bruno</creatorcontrib><creatorcontrib>Li, Blaise</creatorcontrib><creatorcontrib>Franckhauser, Céline</creatorcontrib><creatorcontrib>Fiston Lavier, Anna-Sophie</creatorcontrib><creatorcontrib>Mirouze, Marie</creatorcontrib><creatorcontrib>Fablet, Marie</creatorcontrib><creatorcontrib>Chambeyron, Séverine</creatorcontrib><collection>Oxford Journals Open Access Collection</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Nucleic acids research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Barckmann, Bridlin</au><au>El-Barouk, Marianne</au><au>Pélisson, Alain</au><au>Mugat, Bruno</au><au>Li, Blaise</au><au>Franckhauser, Céline</au><au>Fiston Lavier, Anna-Sophie</au><au>Mirouze, Marie</au><au>Fablet, Marie</au><au>Chambeyron, Séverine</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The somatic piRNA pathway controls germline transposition over generations</atitle><jtitle>Nucleic acids research</jtitle><addtitle>Nucleic Acids Res</addtitle><date>2018-10-12</date><risdate>2018</risdate><volume>46</volume><issue>18</issue><spage>9524</spage><epage>9536</epage><pages>9524-9536</pages><issn>0305-1048</issn><eissn>1362-4962</eissn><abstract>Abstract
Transposable elements (TEs) are parasitic DNA sequences that threaten genome integrity by replicative transposition in host gonads. The Piwi-interacting RNAs (piRNAs) pathway is assumed to maintain Drosophila genome homeostasis by downregulating transcriptional and post-transcriptional TE expression in the ovary. However, the bursts of transposition that are expected to follow transposome derepression after piRNA pathway impairment have not yet been reported. Here, we show, at a genome-wide level, that piRNA loss in the ovarian somatic cells boosts several families of the endogenous retroviral subclass of TEs, at various steps of their replication cycle, from somatic transcription to germinal genome invasion. For some of these TEs, the derepression caused by the loss of piRNAs is backed up by another small RNA pathway (siRNAs) operating in somatic tissues at the post transcriptional level. Derepressed transposition during 70 successive generations of piRNA loss exponentially increases the genomic copy number by up to 10-fold.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>30312469</pmid><doi>10.1093/nar/gky761</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-7306-6532</orcidid><orcidid>https://orcid.org/0000-0003-3080-1899</orcidid><orcidid>https://orcid.org/0000-0003-2775-6556</orcidid><orcidid>https://orcid.org/0000-0002-7819-4541</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Biochemistry, Molecular Biology Botanics Genome Integrity, Repair and Genomics Life Sciences Vegetal Biology |
title | The somatic piRNA pathway controls germline transposition over generations |
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