Expansion of genes encoding piRNA-associated argonaute proteins in the pea aphid: diversification of expression profiles in different plastic morphs
Piwi-interacting RNAs (piRNAs) are known to regulate transposon activity in germ cells of several animal models that propagate sexually. However, the role of piRNAs during asexual reproduction remains almost unknown. Aphids that can alternate sexual and asexual reproduction cycles in response to sea...
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description | Piwi-interacting RNAs (piRNAs) are known to regulate transposon activity in germ cells of several animal models that propagate sexually. However, the role of piRNAs during asexual reproduction remains almost unknown. Aphids that can alternate sexual and asexual reproduction cycles in response to seasonal changes of photoperiod provide a unique opportunity to study piRNAs and the piRNA pathway in both reproductive modes. Taking advantage of the recently sequenced genome of the pea aphid Acyrthosiphon pisum, we found an unusually large lineage-specific expansion of genes encoding the Piwi sub-clade of Argonaute proteins. In situ hybridisation showed differential expressions between the duplicated piwi copies: while Api-piwi2 and Api-piwi6 are "specialised" in germ cells their most closely related copy, respectively Api-piwi5 and Api-piwi3, are expressed in the somatic cells. The differential expression was also identified in duplicated ago3: Api-ago3a in germ cells and Api-ago3b in somatic cells. Moreover, analyses of expression profiles of the expanded piwi and ago3 genes by semi-quantitative RT-PCR showed that expressions varied according to the reproductive types. These specific expression patterns suggest that expanded aphid piwi and ago3 genes have distinct roles in asexual and sexual reproduction. |
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However, the role of piRNAs during asexual reproduction remains almost unknown. Aphids that can alternate sexual and asexual reproduction cycles in response to seasonal changes of photoperiod provide a unique opportunity to study piRNAs and the piRNA pathway in both reproductive modes. Taking advantage of the recently sequenced genome of the pea aphid Acyrthosiphon pisum, we found an unusually large lineage-specific expansion of genes encoding the Piwi sub-clade of Argonaute proteins. In situ hybridisation showed differential expressions between the duplicated piwi copies: while Api-piwi2 and Api-piwi6 are "specialised" in germ cells their most closely related copy, respectively Api-piwi5 and Api-piwi3, are expressed in the somatic cells. The differential expression was also identified in duplicated ago3: Api-ago3a in germ cells and Api-ago3b in somatic cells. Moreover, analyses of expression profiles of the expanded piwi and ago3 genes by semi-quantitative RT-PCR showed that expressions varied according to the reproductive types. These specific expression patterns suggest that expanded aphid piwi and ago3 genes have distinct roles in asexual and sexual reproduction.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0028051</identifier><identifier>PMID: 22162754</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Acids ; Acyrthosiphon pisum ; Analysis ; Animal models ; Animals ; Annual variations ; Aphidoidea ; Aphids ; Aphids - metabolism ; Argonaute Proteins - metabolism ; Asexual reproduction ; Biology ; Cell Lineage ; Cloning, Molecular ; Codon, Terminator ; Developmental biology ; Drosophila ; Ecosystem biology ; Ecosystems ; Evolution, Molecular ; Gene expression ; Gene Expression Profiling ; Gene Expression Regulation, Developmental ; Genes ; Genetic research ; Genome, Plant ; Genomes ; Genomics ; Germ cells ; Growth factors ; Hemiptera ; In Situ Hybridization ; Industrial research ; Insects ; Models, Biological ; Models, Genetic ; Oligonucleotides, Antisense - genetics ; Phylogeny ; Plastics ; Polymerase chain reaction ; Population ; Proteins ; Reproduction ; Reproduction (biology) ; Reproduction (copying) ; RNA, Small Interfering - metabolism ; Seasonal variations ; Seasons ; Sexual reproduction ; Somatic cells ; Transposons</subject><ispartof>PloS one, 2011-12, Vol.6 (12), p.e28051-e28051</ispartof><rights>COPYRIGHT 2011 Public Library of Science</rights><rights>2011 Lu et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://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>Lu et al. 2011</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c757t-6f600104b6c78400836076ede6c094ee8b35ffcea54f1af26c8dc6592242db133</citedby><cites>FETCH-LOGICAL-c757t-6f600104b6c78400836076ede6c094ee8b35ffcea54f1af26c8dc6592242db133</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3230593/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3230593/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22162754$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Smagghe, Guy</contributor><creatorcontrib>Lu, Hsiao-Ling</creatorcontrib><creatorcontrib>Tanguy, Sylvie</creatorcontrib><creatorcontrib>Rispe, Claude</creatorcontrib><creatorcontrib>Gauthier, Jean-Pierre</creatorcontrib><creatorcontrib>Walsh, Tom</creatorcontrib><creatorcontrib>Gordon, Karl</creatorcontrib><creatorcontrib>Edwards, Owain</creatorcontrib><creatorcontrib>Tagu, Denis</creatorcontrib><creatorcontrib>Chang, Chun-che</creatorcontrib><creatorcontrib>Jaubert-Possamai, Stéphanie</creatorcontrib><title>Expansion of genes encoding piRNA-associated argonaute proteins in the pea aphid: diversification of expression profiles in different plastic morphs</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Piwi-interacting RNAs (piRNAs) are known to regulate transposon activity in germ cells of several animal models that propagate sexually. 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These specific expression patterns suggest that expanded aphid piwi and ago3 genes have distinct roles in asexual and sexual reproduction.</description><subject>Acids</subject><subject>Acyrthosiphon pisum</subject><subject>Analysis</subject><subject>Animal models</subject><subject>Animals</subject><subject>Annual variations</subject><subject>Aphidoidea</subject><subject>Aphids</subject><subject>Aphids - metabolism</subject><subject>Argonaute Proteins - metabolism</subject><subject>Asexual reproduction</subject><subject>Biology</subject><subject>Cell Lineage</subject><subject>Cloning, Molecular</subject><subject>Codon, Terminator</subject><subject>Developmental biology</subject><subject>Drosophila</subject><subject>Ecosystem biology</subject><subject>Ecosystems</subject><subject>Evolution, Molecular</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Genes</subject><subject>Genetic research</subject><subject>Genome, Plant</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Germ cells</subject><subject>Growth factors</subject><subject>Hemiptera</subject><subject>In Situ Hybridization</subject><subject>Industrial research</subject><subject>Insects</subject><subject>Models, Biological</subject><subject>Models, Genetic</subject><subject>Oligonucleotides, Antisense - genetics</subject><subject>Phylogeny</subject><subject>Plastics</subject><subject>Polymerase chain reaction</subject><subject>Population</subject><subject>Proteins</subject><subject>Reproduction</subject><subject>Reproduction (biology)</subject><subject>Reproduction (copying)</subject><subject>RNA, Small Interfering - metabolism</subject><subject>Seasonal variations</subject><subject>Seasons</subject><subject>Sexual reproduction</subject><subject>Somatic cells</subject><subject>Transposons</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk99u0zAUxiMEYqPwBggiIYG4aLGdxEm4QKqmAZUmJo0_t9apfZy6Su3MTqbxHjwwbptNLdoFipQ4ye_7zvE5PknykpIZzUr6Ye0Gb6Gddc7ijBBWkYI-Sk5pnbEpZyR7fLA-SZ6FsCakyCrOnyYnjFHOyiI_Tf6c33Zgg3E2dTpt0GJI0UqnjG3Szlx9m08hBCcN9KhS8I2zMPSYdt71aGxIjU37VXxHSKFbGfUxVeYGfTDaSOhHX7ztPIZdlCjUpsWdUBmt0aPt066F0BuZbpzvVuF58kRDG_DF-JwkPz-f_zj7Or24_LI4m19MZVmU_ZRrTggl-ZLLssoJqTJOSo4KuSR1jlgts0JriVDkmoJmXFZK8qJmLGdqSbNskrze-3atC2IsaBA0ozTnFclYJBZ7QjlYi86bDfjfwoERuw_ONwJ8TLxFkem6Bl0RhQi5yhnkjLKqqIt6WTPOMXp9GqMNyw0qGfftoT0yPf5jzUo07kbEPEhRb9N9Nxp4dz1g6MXGBIltCxbdEERNY8NLHm-T5M0_5MObG6kGYv7GahfDyq2nmOclrzilrIjU7AEqXgo3RsbDt23nseD9kSAyPd72DQwhiMX3q_9nL38ds28P2BVC26-Ca4ftIQvHYL4HpXcheNT3NaZEbGfnrhpiOztinJ0oe3XYn3vR3bBkfwESAhZk</recordid><startdate>20111205</startdate><enddate>20111205</enddate><creator>Lu, Hsiao-Ling</creator><creator>Tanguy, Sylvie</creator><creator>Rispe, Claude</creator><creator>Gauthier, Jean-Pierre</creator><creator>Walsh, Tom</creator><creator>Gordon, Karl</creator><creator>Edwards, Owain</creator><creator>Tagu, Denis</creator><creator>Chang, Chun-che</creator><creator>Jaubert-Possamai, Stéphanie</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>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</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>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20111205</creationdate><title>Expansion of genes encoding piRNA-associated argonaute proteins in the pea aphid: diversification of expression profiles in different plastic morphs</title><author>Lu, Hsiao-Ling ; Tanguy, Sylvie ; Rispe, Claude ; Gauthier, Jean-Pierre ; Walsh, Tom ; Gordon, Karl ; Edwards, Owain ; Tagu, Denis ; Chang, Chun-che ; Jaubert-Possamai, Stéphanie</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c757t-6f600104b6c78400836076ede6c094ee8b35ffcea54f1af26c8dc6592242db133</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Acids</topic><topic>Acyrthosiphon pisum</topic><topic>Analysis</topic><topic>Animal models</topic><topic>Animals</topic><topic>Annual variations</topic><topic>Aphidoidea</topic><topic>Aphids</topic><topic>Aphids - metabolism</topic><topic>Argonaute Proteins - metabolism</topic><topic>Asexual reproduction</topic><topic>Biology</topic><topic>Cell Lineage</topic><topic>Cloning, Molecular</topic><topic>Codon, Terminator</topic><topic>Developmental biology</topic><topic>Drosophila</topic><topic>Ecosystem biology</topic><topic>Ecosystems</topic><topic>Evolution, Molecular</topic><topic>Gene expression</topic><topic>Gene Expression Profiling</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Genes</topic><topic>Genetic research</topic><topic>Genome, Plant</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Germ cells</topic><topic>Growth factors</topic><topic>Hemiptera</topic><topic>In Situ Hybridization</topic><topic>Industrial research</topic><topic>Insects</topic><topic>Models, Biological</topic><topic>Models, Genetic</topic><topic>Oligonucleotides, Antisense - genetics</topic><topic>Phylogeny</topic><topic>Plastics</topic><topic>Polymerase chain reaction</topic><topic>Population</topic><topic>Proteins</topic><topic>Reproduction</topic><topic>Reproduction (biology)</topic><topic>Reproduction (copying)</topic><topic>RNA, Small Interfering - 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However, the role of piRNAs during asexual reproduction remains almost unknown. Aphids that can alternate sexual and asexual reproduction cycles in response to seasonal changes of photoperiod provide a unique opportunity to study piRNAs and the piRNA pathway in both reproductive modes. Taking advantage of the recently sequenced genome of the pea aphid Acyrthosiphon pisum, we found an unusually large lineage-specific expansion of genes encoding the Piwi sub-clade of Argonaute proteins. In situ hybridisation showed differential expressions between the duplicated piwi copies: while Api-piwi2 and Api-piwi6 are "specialised" in germ cells their most closely related copy, respectively Api-piwi5 and Api-piwi3, are expressed in the somatic cells. The differential expression was also identified in duplicated ago3: Api-ago3a in germ cells and Api-ago3b in somatic cells. Moreover, analyses of expression profiles of the expanded piwi and ago3 genes by semi-quantitative RT-PCR showed that expressions varied according to the reproductive types. These specific expression patterns suggest that expanded aphid piwi and ago3 genes have distinct roles in asexual and sexual reproduction.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>22162754</pmid><doi>10.1371/journal.pone.0028051</doi><tpages>e28051</tpages><oa>free_for_read</oa></addata></record> |
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source | PubMed Central Free; MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; Free Full-Text Journals in Chemistry |
subjects | Acids Acyrthosiphon pisum Analysis Animal models Animals Annual variations Aphidoidea Aphids Aphids - metabolism Argonaute Proteins - metabolism Asexual reproduction Biology Cell Lineage Cloning, Molecular Codon, Terminator Developmental biology Drosophila Ecosystem biology Ecosystems Evolution, Molecular Gene expression Gene Expression Profiling Gene Expression Regulation, Developmental Genes Genetic research Genome, Plant Genomes Genomics Germ cells Growth factors Hemiptera In Situ Hybridization Industrial research Insects Models, Biological Models, Genetic Oligonucleotides, Antisense - genetics Phylogeny Plastics Polymerase chain reaction Population Proteins Reproduction Reproduction (biology) Reproduction (copying) RNA, Small Interfering - metabolism Seasonal variations Seasons Sexual reproduction Somatic cells Transposons |
title | Expansion of genes encoding piRNA-associated argonaute proteins in the pea aphid: diversification of expression profiles in different plastic morphs |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-03T07%3A05%3A01IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Expansion%20of%20genes%20encoding%20piRNA-associated%20argonaute%20proteins%20in%20the%20pea%20aphid:%20diversification%20of%20expression%20profiles%20in%20different%20plastic%20morphs&rft.jtitle=PloS%20one&rft.au=Lu,%20Hsiao-Ling&rft.date=2011-12-05&rft.volume=6&rft.issue=12&rft.spage=e28051&rft.epage=e28051&rft.pages=e28051-e28051&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0028051&rft_dat=%3Cgale_plos_%3EA476861125%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1311468032&rft_id=info:pmid/22162754&rft_galeid=A476861125&rft_doaj_id=oai_doaj_org_article_3f99af80deea4d42a421285959b9266e&rfr_iscdi=true |