Small-RNA-mediated transgenerational silencing of histone genes impairs fertility in piRNA mutants
PIWI-interacting RNAs (piRNAs) promote fertility in many animals. However, whether this is due to their conserved role in repressing repetitive elements (REs) remains unclear. Here, we show that the progressive loss of fertility in Caenorhabditis elegans lacking piRNAs is not caused by derepression...
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| Veröffentlicht in: | Nature cell biology 2020-02, Vol.22 (2), p.235-245 |
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| creator | Barucci, Giorgia Cornes, Eric Singh, Meetali Li, Blaise Ugolini, Martino Samolygo, Aleksei Didier, Celine Dingli, Florent Loew, Damarys Quarato, Piergiuseppe Cecere, Germano |
| description | PIWI-interacting RNAs (piRNAs) promote fertility in many animals. However, whether this is due to their conserved role in repressing repetitive elements (REs) remains unclear. Here, we show that the progressive loss of fertility in
Caenorhabditis elegans
lacking piRNAs is not caused by derepression of REs or other piRNA targets but, rather, is mediated by epigenetic silencing of all of the replicative histone genes. In the absence of piRNAs, downstream components of the piRNA pathway relocalize from germ granules and piRNA targets to histone mRNAs to synthesize antisense small RNAs (sRNAs) and induce transgenerational silencing. Removal of the downstream components of the piRNA pathway restores histone mRNA expression and fertility in piRNA mutants, and the inheritance of histone sRNAs in wild-type worms adversely affects their fertility for multiple generations. We conclude that sRNA-mediated silencing of histone genes impairs the fertility of piRNA mutants and may serve to maintain piRNAs across evolution.
Barucci et al. show that the progressive loss of fertility in
Caenorhabditis elegans
lacking piRNAs is mediated by the epigenetic silencing of all of the replicative histone genes. |
| doi_str_mv | 10.1038/s41556-020-0462-7 |
| format | Article |
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Caenorhabditis elegans
lacking piRNAs is not caused by derepression of REs or other piRNA targets but, rather, is mediated by epigenetic silencing of all of the replicative histone genes. In the absence of piRNAs, downstream components of the piRNA pathway relocalize from germ granules and piRNA targets to histone mRNAs to synthesize antisense small RNAs (sRNAs) and induce transgenerational silencing. Removal of the downstream components of the piRNA pathway restores histone mRNA expression and fertility in piRNA mutants, and the inheritance of histone sRNAs in wild-type worms adversely affects their fertility for multiple generations. We conclude that sRNA-mediated silencing of histone genes impairs the fertility of piRNA mutants and may serve to maintain piRNAs across evolution.
Barucci et al. show that the progressive loss of fertility in
Caenorhabditis elegans
lacking piRNAs is mediated by the epigenetic silencing of all of the replicative histone genes.</description><identifier>ISSN: 1465-7392</identifier><identifier>EISSN: 1476-4679</identifier><identifier>DOI: 10.1038/s41556-020-0462-7</identifier><identifier>PMID: 32015436</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>38/39 ; 38/91 ; 631/208/176/2016 ; 631/337/384/2054 ; 631/337/505 ; 631/532/2442 ; 64 ; 64/11 ; 82/58 ; Animals ; Animals, Genetically Modified ; Antisense RNA ; Argonaute Proteins - deficiency ; Argonaute Proteins - genetics ; Argonaute Proteins - metabolism ; Biodiversity ; Biological Evolution ; Biomedical and Life Sciences ; Caenorhabditis elegans ; Caenorhabditis elegans - genetics ; Caenorhabditis elegans - metabolism ; Caenorhabditis elegans Proteins - genetics ; Caenorhabditis elegans Proteins - metabolism ; Cancer Research ; Cell Biology ; CRISPR-Cas Systems ; Derepression ; Developmental Biology ; Epigenetic inheritance ; Epigenetics ; Fertility ; Fertility - genetics ; Gene Editing ; Gene expression ; Gene Silencing ; Genes ; Genetic engineering ; Heredity ; Histones ; Histones - genetics ; Histones - metabolism ; Inheritance Patterns ; Life Sciences ; Mutation ; Nematodes ; Populations and Evolution ; Repetitive Sequences, Nucleic Acid ; RNA ; RNA, Antisense - genetics ; RNA, Antisense - metabolism ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; RNA, Small Interfering - genetics ; RNA, Small Interfering - metabolism ; RNA-mediated interference ; Scientific equipment and supplies industry ; Stem Cells ; Worms</subject><ispartof>Nature cell biology, 2020-02, Vol.22 (2), p.235-245</ispartof><rights>The Author(s), under exclusive licence to Springer Nature Limited 2020</rights><rights>COPYRIGHT 2020 Nature Publishing Group</rights><rights>2020© The Author(s), under exclusive licence to Springer Nature Limited 2020</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c605t-f78687a6dfdd7334871204301d421e6645aa3acf95d015be1638c9771b0bc7ac3</citedby><cites>FETCH-LOGICAL-c605t-f78687a6dfdd7334871204301d421e6645aa3acf95d015be1638c9771b0bc7ac3</cites><orcidid>0000-0001-5912-3417 ; 0000-0002-5783-073X ; 0000-0002-7715-2446 ; 0000-0002-9111-8842 ; 0000-0003-3839-3383 ; 0000-0003-3080-1899</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/s41556-020-0462-7$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41556-020-0462-7$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,780,784,885,27924,27925,41488,42557,51319</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32015436$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-02617478$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Barucci, Giorgia</creatorcontrib><creatorcontrib>Cornes, Eric</creatorcontrib><creatorcontrib>Singh, Meetali</creatorcontrib><creatorcontrib>Li, Blaise</creatorcontrib><creatorcontrib>Ugolini, Martino</creatorcontrib><creatorcontrib>Samolygo, Aleksei</creatorcontrib><creatorcontrib>Didier, Celine</creatorcontrib><creatorcontrib>Dingli, Florent</creatorcontrib><creatorcontrib>Loew, Damarys</creatorcontrib><creatorcontrib>Quarato, Piergiuseppe</creatorcontrib><creatorcontrib>Cecere, Germano</creatorcontrib><title>Small-RNA-mediated transgenerational silencing of histone genes impairs fertility in piRNA mutants</title><title>Nature cell biology</title><addtitle>Nat Cell Biol</addtitle><addtitle>Nat Cell Biol</addtitle><description>PIWI-interacting RNAs (piRNAs) promote fertility in many animals. However, whether this is due to their conserved role in repressing repetitive elements (REs) remains unclear. Here, we show that the progressive loss of fertility in
Caenorhabditis elegans
lacking piRNAs is not caused by derepression of REs or other piRNA targets but, rather, is mediated by epigenetic silencing of all of the replicative histone genes. In the absence of piRNAs, downstream components of the piRNA pathway relocalize from germ granules and piRNA targets to histone mRNAs to synthesize antisense small RNAs (sRNAs) and induce transgenerational silencing. Removal of the downstream components of the piRNA pathway restores histone mRNA expression and fertility in piRNA mutants, and the inheritance of histone sRNAs in wild-type worms adversely affects their fertility for multiple generations. We conclude that sRNA-mediated silencing of histone genes impairs the fertility of piRNA mutants and may serve to maintain piRNAs across evolution.
Barucci et al. show that the progressive loss of fertility in
Caenorhabditis elegans
lacking piRNAs is mediated by the epigenetic silencing of all of the replicative histone genes.</description><subject>38/39</subject><subject>38/91</subject><subject>631/208/176/2016</subject><subject>631/337/384/2054</subject><subject>631/337/505</subject><subject>631/532/2442</subject><subject>64</subject><subject>64/11</subject><subject>82/58</subject><subject>Animals</subject><subject>Animals, Genetically Modified</subject><subject>Antisense RNA</subject><subject>Argonaute Proteins - deficiency</subject><subject>Argonaute Proteins - genetics</subject><subject>Argonaute Proteins - metabolism</subject><subject>Biodiversity</subject><subject>Biological Evolution</subject><subject>Biomedical and Life Sciences</subject><subject>Caenorhabditis elegans</subject><subject>Caenorhabditis elegans - genetics</subject><subject>Caenorhabditis elegans - metabolism</subject><subject>Caenorhabditis elegans Proteins - genetics</subject><subject>Caenorhabditis elegans Proteins - metabolism</subject><subject>Cancer Research</subject><subject>Cell Biology</subject><subject>CRISPR-Cas Systems</subject><subject>Derepression</subject><subject>Developmental Biology</subject><subject>Epigenetic inheritance</subject><subject>Epigenetics</subject><subject>Fertility</subject><subject>Fertility - 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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>Nature cell biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Barucci, Giorgia</au><au>Cornes, Eric</au><au>Singh, Meetali</au><au>Li, Blaise</au><au>Ugolini, Martino</au><au>Samolygo, Aleksei</au><au>Didier, Celine</au><au>Dingli, Florent</au><au>Loew, Damarys</au><au>Quarato, Piergiuseppe</au><au>Cecere, Germano</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Small-RNA-mediated transgenerational silencing of histone genes impairs fertility in piRNA mutants</atitle><jtitle>Nature cell biology</jtitle><stitle>Nat Cell Biol</stitle><addtitle>Nat Cell Biol</addtitle><date>2020-02-01</date><risdate>2020</risdate><volume>22</volume><issue>2</issue><spage>235</spage><epage>245</epage><pages>235-245</pages><issn>1465-7392</issn><eissn>1476-4679</eissn><abstract>PIWI-interacting RNAs (piRNAs) promote fertility in many animals. However, whether this is due to their conserved role in repressing repetitive elements (REs) remains unclear. Here, we show that the progressive loss of fertility in
Caenorhabditis elegans
lacking piRNAs is not caused by derepression of REs or other piRNA targets but, rather, is mediated by epigenetic silencing of all of the replicative histone genes. In the absence of piRNAs, downstream components of the piRNA pathway relocalize from germ granules and piRNA targets to histone mRNAs to synthesize antisense small RNAs (sRNAs) and induce transgenerational silencing. Removal of the downstream components of the piRNA pathway restores histone mRNA expression and fertility in piRNA mutants, and the inheritance of histone sRNAs in wild-type worms adversely affects their fertility for multiple generations. We conclude that sRNA-mediated silencing of histone genes impairs the fertility of piRNA mutants and may serve to maintain piRNAs across evolution.
Barucci et al. show that the progressive loss of fertility in
Caenorhabditis elegans
lacking piRNAs is mediated by the epigenetic silencing of all of the replicative histone genes.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>32015436</pmid><doi>10.1038/s41556-020-0462-7</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0001-5912-3417</orcidid><orcidid>https://orcid.org/0000-0002-5783-073X</orcidid><orcidid>https://orcid.org/0000-0002-7715-2446</orcidid><orcidid>https://orcid.org/0000-0002-9111-8842</orcidid><orcidid>https://orcid.org/0000-0003-3839-3383</orcidid><orcidid>https://orcid.org/0000-0003-3080-1899</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1465-7392 |
| ispartof | Nature cell biology, 2020-02, Vol.22 (2), p.235-245 |
| issn | 1465-7392 1476-4679 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_7272227 |
| source | MEDLINE; SpringerNature Journals; Nature Journals Online |
| subjects | 38/39 38/91 631/208/176/2016 631/337/384/2054 631/337/505 631/532/2442 64 64/11 82/58 Animals Animals, Genetically Modified Antisense RNA Argonaute Proteins - deficiency Argonaute Proteins - genetics Argonaute Proteins - metabolism Biodiversity Biological Evolution Biomedical and Life Sciences Caenorhabditis elegans Caenorhabditis elegans - genetics Caenorhabditis elegans - metabolism Caenorhabditis elegans Proteins - genetics Caenorhabditis elegans Proteins - metabolism Cancer Research Cell Biology CRISPR-Cas Systems Derepression Developmental Biology Epigenetic inheritance Epigenetics Fertility Fertility - genetics Gene Editing Gene expression Gene Silencing Genes Genetic engineering Heredity Histones Histones - genetics Histones - metabolism Inheritance Patterns Life Sciences Mutation Nematodes Populations and Evolution Repetitive Sequences, Nucleic Acid RNA RNA, Antisense - genetics RNA, Antisense - metabolism RNA, Messenger - genetics RNA, Messenger - metabolism RNA, Small Interfering - genetics RNA, Small Interfering - metabolism RNA-mediated interference Scientific equipment and supplies industry Stem Cells Worms |
| title | Small-RNA-mediated transgenerational silencing of histone genes impairs fertility in piRNA mutants |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-04T04%3A34%3A49IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Small-RNA-mediated%20transgenerational%20silencing%20of%20histone%20genes%20impairs%20fertility%20in%20piRNA%20mutants&rft.jtitle=Nature%20cell%20biology&rft.au=Barucci,%20Giorgia&rft.date=2020-02-01&rft.volume=22&rft.issue=2&rft.spage=235&rft.epage=245&rft.pages=235-245&rft.issn=1465-7392&rft.eissn=1476-4679&rft_id=info:doi/10.1038/s41556-020-0462-7&rft_dat=%3Cgale_pubme%3EA613408746%3C/gale_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2352043010&rft_id=info:pmid/32015436&rft_galeid=A613408746&rfr_iscdi=true |