Essential and recurrent roles for hairpin RNAs in silencing de novo sex chromosome conflict in Drosophila simulans
Meiotic drive loci distort the normally equal segregation of alleles, which benefits their own transmission even in the face of severe fitness costs to their host organism. However, relatively little is known about the molecular identity of meiotic drivers, their strategies of action, and mechanisms...
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description | Meiotic drive loci distort the normally equal segregation of alleles, which benefits their own transmission even in the face of severe fitness costs to their host organism. However, relatively little is known about the molecular identity of meiotic drivers, their strategies of action, and mechanisms that can suppress their activity. Here, we present data from the fruitfly Drosophila simulans that address these questions. We show that a family of de novo, protamine-derived X-linked selfish genes (the Dox gene family) is silenced by a pair of newly emerged hairpin RNA (hpRNA) small interfering RNA (siRNA)-class loci, Nmy and Tmy. In the w[XD1] genetic background, knockout of nmy derepresses Dox and MDox in testes and depletes male progeny, whereas knockout of tmy causes misexpression of PDox genes and renders males sterile. Importantly, genetic interactions between nmy and tmy mutant alleles reveal that Tmy also specifically maintains male progeny for normal sex ratio. We show the Dox loci are functionally polymorphic within D. simulans, such that both nmy-associated sex ratio bias and tmy-associated sterility can be rescued by wild-type X chromosomes bearing natural deletions in different Dox family genes. Finally, using tagged transgenes of Dox and PDox2, we provide the first experimental evidence Dox family genes encode proteins that are strongly derepressed in cognate hpRNA mutants. Altogether, these studies support a model in which protamine-derived drivers and hpRNA suppressors drive repeated cycles of sex chromosome conflict and resolution that shape genome evolution and the genetic control of male gametogenesis. |
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However, relatively little is known about the molecular identity of meiotic drivers, their strategies of action, and mechanisms that can suppress their activity. Here, we present data from the fruitfly Drosophila simulans that address these questions. We show that a family of de novo, protamine-derived X-linked selfish genes (the Dox gene family) is silenced by a pair of newly emerged hairpin RNA (hpRNA) small interfering RNA (siRNA)-class loci, Nmy and Tmy. In the w[XD1] genetic background, knockout of nmy derepresses Dox and MDox in testes and depletes male progeny, whereas knockout of tmy causes misexpression of PDox genes and renders males sterile. Importantly, genetic interactions between nmy and tmy mutant alleles reveal that Tmy also specifically maintains male progeny for normal sex ratio. We show the Dox loci are functionally polymorphic within D. simulans, such that both nmy-associated sex ratio bias and tmy-associated sterility can be rescued by wild-type X chromosomes bearing natural deletions in different Dox family genes. Finally, using tagged transgenes of Dox and PDox2, we provide the first experimental evidence Dox family genes encode proteins that are strongly derepressed in cognate hpRNA mutants. Altogether, these studies support a model in which protamine-derived drivers and hpRNA suppressors drive repeated cycles of sex chromosome conflict and resolution that shape genome evolution and the genetic control of male gametogenesis.</description><identifier>ISSN: 1545-7885</identifier><identifier>ISSN: 1544-9173</identifier><identifier>EISSN: 1545-7885</identifier><identifier>DOI: 10.1371/journal.pbio.3002136</identifier><identifier>PMID: 37289846</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Alleles ; Animals ; Biology and Life Sciences ; Cell division ; Chromosomes ; Drosophila ; Drosophila - genetics ; Drosophila simulans ; Drosophila simulans - genetics ; Equilibrium ; Fertility ; Fruit flies ; Gametogenesis ; Gene silencing ; Genes ; Genetic aspects ; Genetic control ; Genetic engineering ; Genetic research ; Genomes ; Genotype & phenotype ; Insects ; Life Sciences ; Male ; Males ; Meiosis ; Meiosis - genetics ; Meiotic drive ; Mutants ; Progeny ; Protamine ; Research and Analysis Methods ; Ribonucleic acid ; RNA ; RNA, Small Interfering - genetics ; Sex ; Sex chromosomes ; Sex Chromosomes - genetics ; Sex Ratio ; siRNA ; Sterility ; Suppressors ; Transgenes ; X Chromosome</subject><ispartof>PLoS biology, 2023-06, Vol.21 (6), p.e3002136</ispartof><rights>Copyright: © 2023 Vedanayagam et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2023 Public Library of Science</rights><rights>2023 Vedanayagam et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2023 Vedanayagam et al 2023 Vedanayagam et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c730t-64fcc389545702963ea785d4d54222a984aa35a8243670633a3146750c6ca0bf3</citedby><cites>FETCH-LOGICAL-c730t-64fcc389545702963ea785d4d54222a984aa35a8243670633a3146750c6ca0bf3</cites><orcidid>0000-0002-8432-5851 ; 0000-0002-7710-3716 ; 0000-0002-7166-9233 ; 0000-0002-7683-3207</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/PMC10292708/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10292708/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37289846$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-04267164$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Vedanayagam, Jeffrey</creatorcontrib><creatorcontrib>Herbette, Marion</creatorcontrib><creatorcontrib>Mudgett, Holly</creatorcontrib><creatorcontrib>Lin, Ching-Jung</creatorcontrib><creatorcontrib>Lai, Chun-Ming</creatorcontrib><creatorcontrib>McDonough-Goldstein, Caitlin</creatorcontrib><creatorcontrib>Dorus, Stephen</creatorcontrib><creatorcontrib>Loppin, Benjamin</creatorcontrib><creatorcontrib>Meiklejohn, Colin</creatorcontrib><creatorcontrib>Dubruille, Raphaëlle</creatorcontrib><creatorcontrib>Lai, Eric C</creatorcontrib><title>Essential and recurrent roles for hairpin RNAs in silencing de novo sex chromosome conflict in Drosophila simulans</title><title>PLoS biology</title><addtitle>PLoS Biol</addtitle><description>Meiotic drive loci distort the normally equal segregation of alleles, which benefits their own transmission even in the face of severe fitness costs to their host organism. 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We show the Dox loci are functionally polymorphic within D. simulans, such that both nmy-associated sex ratio bias and tmy-associated sterility can be rescued by wild-type X chromosomes bearing natural deletions in different Dox family genes. Finally, using tagged transgenes of Dox and PDox2, we provide the first experimental evidence Dox family genes encode proteins that are strongly derepressed in cognate hpRNA mutants. 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genetics</subject><subject>Meiotic drive</subject><subject>Mutants</subject><subject>Progeny</subject><subject>Protamine</subject><subject>Research and Analysis Methods</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA, Small Interfering - genetics</subject><subject>Sex</subject><subject>Sex chromosomes</subject><subject>Sex Chromosomes - genetics</subject><subject>Sex Ratio</subject><subject>siRNA</subject><subject>Sterility</subject><subject>Suppressors</subject><subject>Transgenes</subject><subject>X Chromosome</subject><issn>1545-7885</issn><issn>1544-9173</issn><issn>1545-7885</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqVk11v0zAUhiMEYmPwDxBY4oZdtDi2YztXqBqDVao2aXzcWq7jtK6cuLOTavx7Tmg2rdMuQLlwdPyc9_i89smytzme5lTknzahj6320-3ShSnFmOSUP8uO84IVEyFl8fzB_1H2KqUNMKQk8mV2RAWRpWT8OIvnKdm2c9oj3VYoWtPHCAEUg7cJ1SGitXZx61p0fTlLCNbkvG2Na1eosqgNu4CSvUVmHUMTUmgsMqGtvTPdAH-JENuundeQ1_Ret-l19qLWPtk343qS_fx6_uPsYrK4-jY_my0mRlDcTTirjaGyhB4EJiWnVgtZVKwqGCFEw_G1poWWhFEuMKdU05xxUWDDjcbLmp5k7_e6Wx-SGu1KikgqKZWYEiDme6IKeqO20TU6_lZBO_U3EOJK6dg5460yBaF4ycslgQMRw3TFSsZqQWlBKlxQ0Po8VuuXja0MeBi1PxA93GndWq3CTuXQHBFYgsLpXmH9KO9itlBDDDPCRc7ZLgf241gthpvepk41LhnrwV8b-qFJwrgUueSAfniEPm3FSK00dOvaOsAhzSCqZqLgQuSYDWWnT1DwVbZxcO22hrdxmHB6kABMZ2-7le5TUvPv1__BXv47e_XrkGV71sBbTNHW9-bmWA2jdGeIGkZJjaMEae8eXuh90t3s0D_lIxZ6</recordid><startdate>20230608</startdate><enddate>20230608</enddate><creator>Vedanayagam, Jeffrey</creator><creator>Herbette, Marion</creator><creator>Mudgett, Holly</creator><creator>Lin, Ching-Jung</creator><creator>Lai, Chun-Ming</creator><creator>McDonough-Goldstein, Caitlin</creator><creator>Dorus, Stephen</creator><creator>Loppin, Benjamin</creator><creator>Meiklejohn, Colin</creator><creator>Dubruille, Raphaëlle</creator><creator>Lai, Eric C</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PATMY</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><scope>DOA</scope><scope>CZG</scope><orcidid>https://orcid.org/0000-0002-8432-5851</orcidid><orcidid>https://orcid.org/0000-0002-7710-3716</orcidid><orcidid>https://orcid.org/0000-0002-7166-9233</orcidid><orcidid>https://orcid.org/0000-0002-7683-3207</orcidid></search><sort><creationdate>20230608</creationdate><title>Essential and recurrent roles for hairpin RNAs in silencing de novo sex chromosome conflict in Drosophila simulans</title><author>Vedanayagam, Jeffrey ; Herbette, Marion ; Mudgett, Holly ; Lin, Ching-Jung ; Lai, Chun-Ming ; McDonough-Goldstein, Caitlin ; Dorus, Stephen ; Loppin, Benjamin ; Meiklejohn, Colin ; Dubruille, Raphaëlle ; Lai, Eric C</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c730t-64fcc389545702963ea785d4d54222a984aa35a8243670633a3146750c6ca0bf3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Alleles</topic><topic>Animals</topic><topic>Biology and Life Sciences</topic><topic>Cell division</topic><topic>Chromosomes</topic><topic>Drosophila</topic><topic>Drosophila - genetics</topic><topic>Drosophila simulans</topic><topic>Drosophila simulans - genetics</topic><topic>Equilibrium</topic><topic>Fertility</topic><topic>Fruit flies</topic><topic>Gametogenesis</topic><topic>Gene silencing</topic><topic>Genes</topic><topic>Genetic aspects</topic><topic>Genetic control</topic><topic>Genetic engineering</topic><topic>Genetic research</topic><topic>Genomes</topic><topic>Genotype & phenotype</topic><topic>Insects</topic><topic>Life Sciences</topic><topic>Male</topic><topic>Males</topic><topic>Meiosis</topic><topic>Meiosis - genetics</topic><topic>Meiotic drive</topic><topic>Mutants</topic><topic>Progeny</topic><topic>Protamine</topic><topic>Research and Analysis Methods</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>RNA, Small Interfering - genetics</topic><topic>Sex</topic><topic>Sex chromosomes</topic><topic>Sex Chromosomes - genetics</topic><topic>Sex Ratio</topic><topic>siRNA</topic><topic>Sterility</topic><topic>Suppressors</topic><topic>Transgenes</topic><topic>X Chromosome</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Vedanayagam, Jeffrey</creatorcontrib><creatorcontrib>Herbette, Marion</creatorcontrib><creatorcontrib>Mudgett, Holly</creatorcontrib><creatorcontrib>Lin, Ching-Jung</creatorcontrib><creatorcontrib>Lai, Chun-Ming</creatorcontrib><creatorcontrib>McDonough-Goldstein, Caitlin</creatorcontrib><creatorcontrib>Dorus, Stephen</creatorcontrib><creatorcontrib>Loppin, Benjamin</creatorcontrib><creatorcontrib>Meiklejohn, Colin</creatorcontrib><creatorcontrib>Dubruille, Raphaëlle</creatorcontrib><creatorcontrib>Lai, Eric C</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Opposing Viewpoints Resource Center</collection><collection>Gale In Context: Canada</collection><collection>Science (Gale in Context)</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>ProQuest - 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However, relatively little is known about the molecular identity of meiotic drivers, their strategies of action, and mechanisms that can suppress their activity. Here, we present data from the fruitfly Drosophila simulans that address these questions. We show that a family of de novo, protamine-derived X-linked selfish genes (the Dox gene family) is silenced by a pair of newly emerged hairpin RNA (hpRNA) small interfering RNA (siRNA)-class loci, Nmy and Tmy. In the w[XD1] genetic background, knockout of nmy derepresses Dox and MDox in testes and depletes male progeny, whereas knockout of tmy causes misexpression of PDox genes and renders males sterile. Importantly, genetic interactions between nmy and tmy mutant alleles reveal that Tmy also specifically maintains male progeny for normal sex ratio. We show the Dox loci are functionally polymorphic within D. simulans, such that both nmy-associated sex ratio bias and tmy-associated sterility can be rescued by wild-type X chromosomes bearing natural deletions in different Dox family genes. Finally, using tagged transgenes of Dox and PDox2, we provide the first experimental evidence Dox family genes encode proteins that are strongly derepressed in cognate hpRNA mutants. Altogether, these studies support a model in which protamine-derived drivers and hpRNA suppressors drive repeated cycles of sex chromosome conflict and resolution that shape genome evolution and the genetic control of male gametogenesis.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>37289846</pmid><doi>10.1371/journal.pbio.3002136</doi><orcidid>https://orcid.org/0000-0002-8432-5851</orcidid><orcidid>https://orcid.org/0000-0002-7710-3716</orcidid><orcidid>https://orcid.org/0000-0002-7166-9233</orcidid><orcidid>https://orcid.org/0000-0002-7683-3207</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Alleles Animals Biology and Life Sciences Cell division Chromosomes Drosophila Drosophila - genetics Drosophila simulans Drosophila simulans - genetics Equilibrium Fertility Fruit flies Gametogenesis Gene silencing Genes Genetic aspects Genetic control Genetic engineering Genetic research Genomes Genotype & phenotype Insects Life Sciences Male Males Meiosis Meiosis - genetics Meiotic drive Mutants Progeny Protamine Research and Analysis Methods Ribonucleic acid RNA RNA, Small Interfering - genetics Sex Sex chromosomes Sex Chromosomes - genetics Sex Ratio siRNA Sterility Suppressors Transgenes X Chromosome |
title | Essential and recurrent roles for hairpin RNAs in silencing de novo sex chromosome conflict in Drosophila simulans |
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