Gonad transcriptome analysis of pearl oyster Pinctada margaritifera: identification of potential sex differentiation and sex determining genes
Black pearl farming is based on culture of the blacklip pearl oyster Pinctada margaritifera (Mollusca, lophotrochozoa), a protandrous hermaphrodite species. At first maturation, all individuals are males. The female sex appears progressively from two years old, which represents a limitation for broo...
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creator | Teaniniuraitemoana, Vaihiti Huvet, Arnaud Levy, Peva Klopp, Christophe Lhuillier, Emeline Gaertner-Mazouni, Nabila Gueguen, Yannick Le Moullac, Gilles |
description | Black pearl farming is based on culture of the blacklip pearl oyster Pinctada margaritifera (Mollusca, lophotrochozoa), a protandrous hermaphrodite species. At first maturation, all individuals are males. The female sex appears progressively from two years old, which represents a limitation for broodstock conditioning for aquaculture production. In marine mollusks displaying hermaphroditic features, data on sexual determinism and differentiation, including the molecular sex determining cascade, are scarce. To increase genomic resources and identify the molecular mechanisms whereby gene expression may act in the sexual dimorphism of P. margaritifera, we performed gonad transcriptome analysis.
The gonad transcriptome of P. margaritifera was sequenced from several gonadic samples of males and females at different development stages, using a Next-Generation-Sequencing method and RNAseq technology. After Illumina sequencing, assembly and annotation, we obtained 70,147 contigs of which 62.2% shared homologies with existing protein sequences, and 9% showed functional annotation with Gene Ontology terms. Differential expression analysis identified 1,993 differentially expressed contigs between the different categories of gonads. Clustering methods of samples revealed that the sex explained most of the variation in gonad gene expression. K-means clustering of differentially expressed contigs showed 815 and 574 contigs were more expressed in male and female gonads, respectively. The analysis of these contigs revealed the presence of known specific genes coding for proteins involved in sex determinism and/or differentiation, such as dmrt and fem-1 like for males, or foxl2 and vitellogenin for females. The specific gene expression profiles of pmarg-fem1-like, pmarg-dmrt and pmarg-foxl2 in different reproductive stages (undetermined, sexual inversion and regression) suggest that these three genes are potentially involved in the sperm-oocyte switch in P. margaritifera.
The study provides a new transcriptomic tool to study reproduction in hermaphroditic marine mollusks. It identifies sex differentiation and potential sex determining genes in P. margaritifera, a protandrous hermaphrodite species. |
doi_str_mv | 10.1186/1471-2164-15-491 |
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The gonad transcriptome of P. margaritifera was sequenced from several gonadic samples of males and females at different development stages, using a Next-Generation-Sequencing method and RNAseq technology. After Illumina sequencing, assembly and annotation, we obtained 70,147 contigs of which 62.2% shared homologies with existing protein sequences, and 9% showed functional annotation with Gene Ontology terms. Differential expression analysis identified 1,993 differentially expressed contigs between the different categories of gonads. Clustering methods of samples revealed that the sex explained most of the variation in gonad gene expression. K-means clustering of differentially expressed contigs showed 815 and 574 contigs were more expressed in male and female gonads, respectively. The analysis of these contigs revealed the presence of known specific genes coding for proteins involved in sex determinism and/or differentiation, such as dmrt and fem-1 like for males, or foxl2 and vitellogenin for females. The specific gene expression profiles of pmarg-fem1-like, pmarg-dmrt and pmarg-foxl2 in different reproductive stages (undetermined, sexual inversion and regression) suggest that these three genes are potentially involved in the sperm-oocyte switch in P. margaritifera.
The study provides a new transcriptomic tool to study reproduction in hermaphroditic marine mollusks. It identifies sex differentiation and potential sex determining genes in P. margaritifera, a protandrous hermaphrodite species.</description><identifier>ISSN: 1471-2164</identifier><identifier>EISSN: 1471-2164</identifier><identifier>DOI: 10.1186/1471-2164-15-491</identifier><identifier>PMID: 24942841</identifier><language>eng</language><publisher>England: BioMed Central Ltd</publisher><subject>Amino Acid Sequence ; Analysis ; Animals ; Biodiversity and Ecology ; DNA sequencing ; Environmental Sciences ; Female ; Gene Expression Profiling ; Gene Ontology ; Genetic aspects ; Genetic research ; Gonads - metabolism ; INDEL Mutation ; Life Sciences ; Lophotrochozoa ; Male ; Margaritifera ; Microsatellite Repeats ; Molecular Sequence Annotation ; Molecular Sequence Data ; Mollusca ; Nucleotide sequencing ; Pinctada - genetics ; Pinctada margaritifera ; Polymorphism, Single Nucleotide ; RNA sequencing ; Sequence Analysis, DNA ; Sex Determination Analysis ; Sex Determination Processes ; Transcriptome</subject><ispartof>BMC genomics, 2014-06, Vol.15 (1), p.491-491, Article 491</ispartof><rights>COPYRIGHT 2014 BioMed Central Ltd.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>Teaniniuraitemoana et al.; licensee BioMed Central Ltd. 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-b690t-3ddad6e1408af57c85de0d07e8c1438a6a86947641a937011a7a38f838db7a2b3</citedby><cites>FETCH-LOGICAL-b690t-3ddad6e1408af57c85de0d07e8c1438a6a86947641a937011a7a38f838db7a2b3</cites><orcidid>0000-0001-6912-881X ; 0000-0002-8304-5460 ; 0000-0002-8749-9582 ; 0000-0001-7126-5477</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/PMC4082630/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4082630/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24942841$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01719157$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Teaniniuraitemoana, Vaihiti</creatorcontrib><creatorcontrib>Huvet, Arnaud</creatorcontrib><creatorcontrib>Levy, Peva</creatorcontrib><creatorcontrib>Klopp, Christophe</creatorcontrib><creatorcontrib>Lhuillier, Emeline</creatorcontrib><creatorcontrib>Gaertner-Mazouni, Nabila</creatorcontrib><creatorcontrib>Gueguen, Yannick</creatorcontrib><creatorcontrib>Le Moullac, Gilles</creatorcontrib><title>Gonad transcriptome analysis of pearl oyster Pinctada margaritifera: identification of potential sex differentiation and sex determining genes</title><title>BMC genomics</title><addtitle>BMC Genomics</addtitle><description>Black pearl farming is based on culture of the blacklip pearl oyster Pinctada margaritifera (Mollusca, lophotrochozoa), a protandrous hermaphrodite species. At first maturation, all individuals are males. The female sex appears progressively from two years old, which represents a limitation for broodstock conditioning for aquaculture production. In marine mollusks displaying hermaphroditic features, data on sexual determinism and differentiation, including the molecular sex determining cascade, are scarce. To increase genomic resources and identify the molecular mechanisms whereby gene expression may act in the sexual dimorphism of P. margaritifera, we performed gonad transcriptome analysis.
The gonad transcriptome of P. margaritifera was sequenced from several gonadic samples of males and females at different development stages, using a Next-Generation-Sequencing method and RNAseq technology. After Illumina sequencing, assembly and annotation, we obtained 70,147 contigs of which 62.2% shared homologies with existing protein sequences, and 9% showed functional annotation with Gene Ontology terms. Differential expression analysis identified 1,993 differentially expressed contigs between the different categories of gonads. Clustering methods of samples revealed that the sex explained most of the variation in gonad gene expression. K-means clustering of differentially expressed contigs showed 815 and 574 contigs were more expressed in male and female gonads, respectively. The analysis of these contigs revealed the presence of known specific genes coding for proteins involved in sex determinism and/or differentiation, such as dmrt and fem-1 like for males, or foxl2 and vitellogenin for females. The specific gene expression profiles of pmarg-fem1-like, pmarg-dmrt and pmarg-foxl2 in different reproductive stages (undetermined, sexual inversion and regression) suggest that these three genes are potentially involved in the sperm-oocyte switch in P. margaritifera.
The study provides a new transcriptomic tool to study reproduction in hermaphroditic marine mollusks. It identifies sex differentiation and potential sex determining genes in P. margaritifera, a protandrous hermaphrodite species.</description><subject>Amino Acid Sequence</subject><subject>Analysis</subject><subject>Animals</subject><subject>Biodiversity and Ecology</subject><subject>DNA sequencing</subject><subject>Environmental Sciences</subject><subject>Female</subject><subject>Gene Expression Profiling</subject><subject>Gene Ontology</subject><subject>Genetic aspects</subject><subject>Genetic research</subject><subject>Gonads - metabolism</subject><subject>INDEL Mutation</subject><subject>Life Sciences</subject><subject>Lophotrochozoa</subject><subject>Male</subject><subject>Margaritifera</subject><subject>Microsatellite Repeats</subject><subject>Molecular Sequence Annotation</subject><subject>Molecular Sequence Data</subject><subject>Mollusca</subject><subject>Nucleotide sequencing</subject><subject>Pinctada - genetics</subject><subject>Pinctada margaritifera</subject><subject>Polymorphism, Single Nucleotide</subject><subject>RNA sequencing</subject><subject>Sequence Analysis, DNA</subject><subject>Sex Determination Analysis</subject><subject>Sex Determination Processes</subject><subject>Transcriptome</subject><issn>1471-2164</issn><issn>1471-2164</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kk-P1CAYxhujcdfRuydD4sU9dIWWFuphk8lEdzeZROOfM3kLtItpYQRms_Ml_MzS6TrZMWs4QB5-zwMvL1n2muBzQnj9nlBG8oLUNCdVThvyJDs9SE8frE-yFyH8xJgwXlTPs5OCNrTglJxmvy-dBYWiBxukN5voRo3AwrALJiDXoY0GPyC3C1F79MVYGUEBGsH34E00nfbwARmlbVobCdE4u7e5OEkwoKDvkDJdAvfCHgCrZl2n1NFYY3vUa6vDy-xZB0PQr-7nRfbj08fvq6t8_fnyerVc523d4JiXSoGqNaGYQ1cxySulscJMc0loyaEGXjeU1ZRAUzJMCDAoecdLrloGRVsusos5d7NtR61kupqHQWy8SZXthAMjjnesuRG9uxXpxKIucQo4mwNu_rFdLddi0tJbk4ZU7JYkdjWzrXH_Oex4R7pRTL0TU-8EqURqbUp5d39l735tdYhiNEHqYQCr3TYkjDJOWZUeYJG9ndEeBi2M7VyKlRMullXZ1E1TNUWizh-h0lB6NNJZ3ZmkHxnOjgyJifou9rANQVx_-3rM4pmV3oXgdXcol2Ax_d3HCnzzsCcHw9_PWv4Bb6LrpQ</recordid><startdate>20140618</startdate><enddate>20140618</enddate><creator>Teaniniuraitemoana, Vaihiti</creator><creator>Huvet, Arnaud</creator><creator>Levy, Peva</creator><creator>Klopp, Christophe</creator><creator>Lhuillier, Emeline</creator><creator>Gaertner-Mazouni, Nabila</creator><creator>Gueguen, Yannick</creator><creator>Le Moullac, Gilles</creator><general>BioMed Central Ltd</general><general>BioMed Central</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>ISR</scope><scope>8FD</scope><scope>F1W</scope><scope>FR3</scope><scope>H95</scope><scope>H98</scope><scope>L.G</scope><scope>P64</scope><scope>RC3</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-6912-881X</orcidid><orcidid>https://orcid.org/0000-0002-8304-5460</orcidid><orcidid>https://orcid.org/0000-0002-8749-9582</orcidid><orcidid>https://orcid.org/0000-0001-7126-5477</orcidid></search><sort><creationdate>20140618</creationdate><title>Gonad transcriptome analysis of pearl oyster Pinctada margaritifera: identification of potential sex differentiation and sex determining genes</title><author>Teaniniuraitemoana, Vaihiti ; Huvet, Arnaud ; Levy, Peva ; Klopp, Christophe ; Lhuillier, Emeline ; Gaertner-Mazouni, Nabila ; Gueguen, Yannick ; Le Moullac, Gilles</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-b690t-3ddad6e1408af57c85de0d07e8c1438a6a86947641a937011a7a38f838db7a2b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Amino Acid Sequence</topic><topic>Analysis</topic><topic>Animals</topic><topic>Biodiversity and Ecology</topic><topic>DNA sequencing</topic><topic>Environmental Sciences</topic><topic>Female</topic><topic>Gene Expression Profiling</topic><topic>Gene Ontology</topic><topic>Genetic aspects</topic><topic>Genetic research</topic><topic>Gonads - metabolism</topic><topic>INDEL Mutation</topic><topic>Life Sciences</topic><topic>Lophotrochozoa</topic><topic>Male</topic><topic>Margaritifera</topic><topic>Microsatellite Repeats</topic><topic>Molecular Sequence Annotation</topic><topic>Molecular Sequence Data</topic><topic>Mollusca</topic><topic>Nucleotide sequencing</topic><topic>Pinctada - genetics</topic><topic>Pinctada margaritifera</topic><topic>Polymorphism, Single Nucleotide</topic><topic>RNA sequencing</topic><topic>Sequence Analysis, DNA</topic><topic>Sex Determination Analysis</topic><topic>Sex Determination Processes</topic><topic>Transcriptome</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Teaniniuraitemoana, Vaihiti</creatorcontrib><creatorcontrib>Huvet, Arnaud</creatorcontrib><creatorcontrib>Levy, Peva</creatorcontrib><creatorcontrib>Klopp, Christophe</creatorcontrib><creatorcontrib>Lhuillier, Emeline</creatorcontrib><creatorcontrib>Gaertner-Mazouni, Nabila</creatorcontrib><creatorcontrib>Gueguen, Yannick</creatorcontrib><creatorcontrib>Le Moullac, Gilles</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Science</collection><collection>Technology Research Database</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Aquaculture Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</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>BMC genomics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Teaniniuraitemoana, Vaihiti</au><au>Huvet, Arnaud</au><au>Levy, Peva</au><au>Klopp, Christophe</au><au>Lhuillier, Emeline</au><au>Gaertner-Mazouni, Nabila</au><au>Gueguen, Yannick</au><au>Le Moullac, Gilles</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Gonad transcriptome analysis of pearl oyster Pinctada margaritifera: identification of potential sex differentiation and sex determining genes</atitle><jtitle>BMC genomics</jtitle><addtitle>BMC Genomics</addtitle><date>2014-06-18</date><risdate>2014</risdate><volume>15</volume><issue>1</issue><spage>491</spage><epage>491</epage><pages>491-491</pages><artnum>491</artnum><issn>1471-2164</issn><eissn>1471-2164</eissn><abstract>Black pearl farming is based on culture of the blacklip pearl oyster Pinctada margaritifera (Mollusca, lophotrochozoa), a protandrous hermaphrodite species. At first maturation, all individuals are males. The female sex appears progressively from two years old, which represents a limitation for broodstock conditioning for aquaculture production. In marine mollusks displaying hermaphroditic features, data on sexual determinism and differentiation, including the molecular sex determining cascade, are scarce. To increase genomic resources and identify the molecular mechanisms whereby gene expression may act in the sexual dimorphism of P. margaritifera, we performed gonad transcriptome analysis.
The gonad transcriptome of P. margaritifera was sequenced from several gonadic samples of males and females at different development stages, using a Next-Generation-Sequencing method and RNAseq technology. After Illumina sequencing, assembly and annotation, we obtained 70,147 contigs of which 62.2% shared homologies with existing protein sequences, and 9% showed functional annotation with Gene Ontology terms. Differential expression analysis identified 1,993 differentially expressed contigs between the different categories of gonads. Clustering methods of samples revealed that the sex explained most of the variation in gonad gene expression. K-means clustering of differentially expressed contigs showed 815 and 574 contigs were more expressed in male and female gonads, respectively. The analysis of these contigs revealed the presence of known specific genes coding for proteins involved in sex determinism and/or differentiation, such as dmrt and fem-1 like for males, or foxl2 and vitellogenin for females. The specific gene expression profiles of pmarg-fem1-like, pmarg-dmrt and pmarg-foxl2 in different reproductive stages (undetermined, sexual inversion and regression) suggest that these three genes are potentially involved in the sperm-oocyte switch in P. margaritifera.
The study provides a new transcriptomic tool to study reproduction in hermaphroditic marine mollusks. It identifies sex differentiation and potential sex determining genes in P. margaritifera, a protandrous hermaphrodite species.</abstract><cop>England</cop><pub>BioMed Central Ltd</pub><pmid>24942841</pmid><doi>10.1186/1471-2164-15-491</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0001-6912-881X</orcidid><orcidid>https://orcid.org/0000-0002-8304-5460</orcidid><orcidid>https://orcid.org/0000-0002-8749-9582</orcidid><orcidid>https://orcid.org/0000-0001-7126-5477</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Amino Acid Sequence Analysis Animals Biodiversity and Ecology DNA sequencing Environmental Sciences Female Gene Expression Profiling Gene Ontology Genetic aspects Genetic research Gonads - metabolism INDEL Mutation Life Sciences Lophotrochozoa Male Margaritifera Microsatellite Repeats Molecular Sequence Annotation Molecular Sequence Data Mollusca Nucleotide sequencing Pinctada - genetics Pinctada margaritifera Polymorphism, Single Nucleotide RNA sequencing Sequence Analysis, DNA Sex Determination Analysis Sex Determination Processes Transcriptome |
title | Gonad transcriptome analysis of pearl oyster Pinctada margaritifera: identification of potential sex differentiation and sex determining genes |
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