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De novo transcriptome assembly from the gonads of a scleractinian coral, Euphyllia ancora: molecular mechanisms underlying scleractinian gametogenesis
Sexual reproduction of scleractinians has captured the attention of researchers and the general public for decades. Although extensive ecological data has been acquired, underlying molecular and cellular mechanisms remain largely unknown. In this study, to better understand mechanisms underlying gam...
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Published in: | BMC genomics 2020-10, Vol.21 (1), p.732-732, Article 732 |
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description | Sexual reproduction of scleractinians has captured the attention of researchers and the general public for decades. Although extensive ecological data has been acquired, underlying molecular and cellular mechanisms remain largely unknown. In this study, to better understand mechanisms underlying gametogenesis, we isolated ovaries and testes at different developmental phases from a gonochoric coral, Euphyllia ancora, and adopted a transcriptomic approach to reveal sex- and phase-specific gene expression profiles. In particular, we explored genes associated with oocyte development and maturation, spermiogenesis, sperm motility / capacitation, and fertilization.
1.6 billion raw reads were obtained from 24 gonadal samples. De novo assembly of trimmed reads, and elimination of contigs derived from symbiotic dinoflagellates (Symbiodiniaceae) and other organisms yielded a reference E. ancora gonadal transcriptome of 35,802 contigs. Analysis of 4 developmental phases identified 2023 genes that were differentially expressed during oogenesis and 678 during spermatogenesis. In premature/mature ovaries, 631 genes were specifically upregulated, with 538 in mature testes. Upregulated genes included those involved in gametogenesis, gamete maturation, sperm motility / capacitation, and fertilization in other metazoans, including humans. Meanwhile, a large number of genes without homology to sequences in the SWISS-PROT database were also observed among upregulated genes in premature / mature ovaries and mature testes.
Our findings show that scleractinian gametogenesis shares many molecular characteristics with that of other metazoans, but it also possesses unique characteristics developed during cnidarian and/or scleractinian evolution. To the best of our knowledge, this study is the first to create a gonadal transcriptome assembly from any scleractinian. This study and associated datasets provide a foundation for future studies regarding gametogenesis and differences between male and female colonies from molecular and cellular perspectives. Furthermore, our transcriptome assembly will be a useful reference for future development of sex-specific and/or stage-specific germ cell markers that can be used in coral aquaculture and ecological studies. |
doi_str_mv | 10.1186/s12864-020-07113-9 |
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1.6 billion raw reads were obtained from 24 gonadal samples. De novo assembly of trimmed reads, and elimination of contigs derived from symbiotic dinoflagellates (Symbiodiniaceae) and other organisms yielded a reference E. ancora gonadal transcriptome of 35,802 contigs. Analysis of 4 developmental phases identified 2023 genes that were differentially expressed during oogenesis and 678 during spermatogenesis. In premature/mature ovaries, 631 genes were specifically upregulated, with 538 in mature testes. Upregulated genes included those involved in gametogenesis, gamete maturation, sperm motility / capacitation, and fertilization in other metazoans, including humans. Meanwhile, a large number of genes without homology to sequences in the SWISS-PROT database were also observed among upregulated genes in premature / mature ovaries and mature testes.
Our findings show that scleractinian gametogenesis shares many molecular characteristics with that of other metazoans, but it also possesses unique characteristics developed during cnidarian and/or scleractinian evolution. To the best of our knowledge, this study is the first to create a gonadal transcriptome assembly from any scleractinian. This study and associated datasets provide a foundation for future studies regarding gametogenesis and differences between male and female colonies from molecular and cellular perspectives. Furthermore, our transcriptome assembly will be a useful reference for future development of sex-specific and/or stage-specific germ cell markers that can be used in coral aquaculture and ecological studies.</description><identifier>ISSN: 1471-2164</identifier><identifier>EISSN: 1471-2164</identifier><identifier>DOI: 10.1186/s12864-020-07113-9</identifier><identifier>PMID: 33087060</identifier><language>eng</language><publisher>England: BioMed Central Ltd</publisher><subject>Animals ; Anthozoa - genetics ; Aquaculture ; Assembly ; Capacitation ; Coral reefs ; Data acquisition ; Dinoflagellates ; Ecological studies ; Euphyllia ancora ; Female ; Fertilization ; Gametocytes ; Gametogenesis ; Gametogenesis - genetics ; Gene expression ; Genes ; Genetic aspects ; Genomics ; Genotypes ; Gonads ; Homology ; Humans ; Identification and classification ; Male ; Maturation ; Molecular modelling ; Observations ; Oogenesis ; Ovaries ; Ovary ; Polyps ; Reproduction (biology) ; RNA-seq ; Scleractinian corals ; Sex ; Sexual development ; Sexual reproduction ; Sperm ; Sperm Motility ; Spermatogenesis ; Spermiogenesis ; Stony corals ; Testes ; Testis ; Transcriptome</subject><ispartof>BMC genomics, 2020-10, Vol.21 (1), p.732-732, Article 732</ispartof><rights>COPYRIGHT 2020 BioMed Central Ltd.</rights><rights>2020. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>The Author(s) 2020</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c663t-bc3d910a250a0fc941af39cf734004b346dff3453bc6f0ae734becdd2d815d163</citedby><cites>FETCH-LOGICAL-c663t-bc3d910a250a0fc941af39cf734004b346dff3453bc6f0ae734becdd2d815d163</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/PMC7579821/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2461997634?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,25731,27901,27902,36989,36990,44566,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33087060$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chiu, Yi-Ling</creatorcontrib><creatorcontrib>Shikina, Shinya</creatorcontrib><creatorcontrib>Yoshioka, Yuki</creatorcontrib><creatorcontrib>Shinzato, Chuya</creatorcontrib><creatorcontrib>Chang, Ching-Fong</creatorcontrib><title>De novo transcriptome assembly from the gonads of a scleractinian coral, Euphyllia ancora: molecular mechanisms underlying scleractinian gametogenesis</title><title>BMC genomics</title><addtitle>BMC Genomics</addtitle><description>Sexual reproduction of scleractinians has captured the attention of researchers and the general public for decades. Although extensive ecological data has been acquired, underlying molecular and cellular mechanisms remain largely unknown. In this study, to better understand mechanisms underlying gametogenesis, we isolated ovaries and testes at different developmental phases from a gonochoric coral, Euphyllia ancora, and adopted a transcriptomic approach to reveal sex- and phase-specific gene expression profiles. In particular, we explored genes associated with oocyte development and maturation, spermiogenesis, sperm motility / capacitation, and fertilization.
1.6 billion raw reads were obtained from 24 gonadal samples. De novo assembly of trimmed reads, and elimination of contigs derived from symbiotic dinoflagellates (Symbiodiniaceae) and other organisms yielded a reference E. ancora gonadal transcriptome of 35,802 contigs. Analysis of 4 developmental phases identified 2023 genes that were differentially expressed during oogenesis and 678 during spermatogenesis. In premature/mature ovaries, 631 genes were specifically upregulated, with 538 in mature testes. Upregulated genes included those involved in gametogenesis, gamete maturation, sperm motility / capacitation, and fertilization in other metazoans, including humans. Meanwhile, a large number of genes without homology to sequences in the SWISS-PROT database were also observed among upregulated genes in premature / mature ovaries and mature testes.
Our findings show that scleractinian gametogenesis shares many molecular characteristics with that of other metazoans, but it also possesses unique characteristics developed during cnidarian and/or scleractinian evolution. To the best of our knowledge, this study is the first to create a gonadal transcriptome assembly from any scleractinian. This study and associated datasets provide a foundation for future studies regarding gametogenesis and differences between male and female colonies from molecular and cellular perspectives. Furthermore, our transcriptome assembly will be a useful reference for future development of sex-specific and/or stage-specific germ cell markers that can be used in coral aquaculture and ecological studies.</description><subject>Animals</subject><subject>Anthozoa - genetics</subject><subject>Aquaculture</subject><subject>Assembly</subject><subject>Capacitation</subject><subject>Coral reefs</subject><subject>Data acquisition</subject><subject>Dinoflagellates</subject><subject>Ecological studies</subject><subject>Euphyllia ancora</subject><subject>Female</subject><subject>Fertilization</subject><subject>Gametocytes</subject><subject>Gametogenesis</subject><subject>Gametogenesis - genetics</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genomics</subject><subject>Genotypes</subject><subject>Gonads</subject><subject>Homology</subject><subject>Humans</subject><subject>Identification and classification</subject><subject>Male</subject><subject>Maturation</subject><subject>Molecular modelling</subject><subject>Observations</subject><subject>Oogenesis</subject><subject>Ovaries</subject><subject>Ovary</subject><subject>Polyps</subject><subject>Reproduction (biology)</subject><subject>RNA-seq</subject><subject>Scleractinian corals</subject><subject>Sex</subject><subject>Sexual development</subject><subject>Sexual reproduction</subject><subject>Sperm</subject><subject>Sperm Motility</subject><subject>Spermatogenesis</subject><subject>Spermiogenesis</subject><subject>Stony corals</subject><subject>Testes</subject><subject>Testis</subject><subject>Transcriptome</subject><issn>1471-2164</issn><issn>1471-2164</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNptkt9qFDEUxgdRbK2-gBcS8EbBqckkk5nxQii1aqEg-Oc6nElOZlNmkjWZKe6L-Lxmu7V2i-Qi4cvvfMk5fEXxnNFjxlr5NrGqlaKkFS1pwxgvuwfFIRMNKysmxcM754PiSUqXlLKmrerHxQHntG2opIfF7w9IfLgKZI7gk45uPYcJCaSEUz9uiI1hIvMKyRA8mESCJUCSHjGCnp134IkOEcY35GxZrzbj6ICA30rvyBRG1MsIkUyoV-BdmhJZvME4bpwf7tkMMOEcBvSYXHpaPLIwJnx2sx8VPz6efT_9XF58-XR-enJRain5XPaam45RqGoK1OpOMLC807bhglLRcyGNtVzUvNfSUsCs96iNqUzLasMkPyrOd74mwKVaRzdB3KgATl0LIQ4K4uzyR5WVtdDU6L6iUgjB-xq6mjJE2mjTW8he73de66Wf0Gj0eabjnun-jXcrNYQr1dRN11YsG7y6MYjh54JpVpNLGscRPIYlqSo3IlvB2zajL--hl2GJPo8qU5J1XSO5-EcNkBtw3ob8rt6aqhPJu7qqZMMzdfwfKi-Dk9PBo3VZ3yt4vVeQmRl_zQMsKanzb1_32WrH6hhSimhv58Go2qZY7VKscorVdYpVl4te3J3kbcnf2PI_CmHvhQ</recordid><startdate>20201021</startdate><enddate>20201021</enddate><creator>Chiu, Yi-Ling</creator><creator>Shikina, Shinya</creator><creator>Yoshioka, Yuki</creator><creator>Shinzato, Chuya</creator><creator>Chang, Ching-Fong</creator><general>BioMed Central Ltd</general><general>BioMed Central</general><general>BMC</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>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>7U7</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</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>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>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20201021</creationdate><title>De novo transcriptome assembly from the gonads of a scleractinian coral, Euphyllia ancora: molecular mechanisms underlying scleractinian gametogenesis</title><author>Chiu, Yi-Ling ; Shikina, Shinya ; Yoshioka, Yuki ; Shinzato, Chuya ; Chang, Ching-Fong</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c663t-bc3d910a250a0fc941af39cf734004b346dff3453bc6f0ae734becdd2d815d163</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Animals</topic><topic>Anthozoa - genetics</topic><topic>Aquaculture</topic><topic>Assembly</topic><topic>Capacitation</topic><topic>Coral reefs</topic><topic>Data acquisition</topic><topic>Dinoflagellates</topic><topic>Ecological studies</topic><topic>Euphyllia ancora</topic><topic>Female</topic><topic>Fertilization</topic><topic>Gametocytes</topic><topic>Gametogenesis</topic><topic>Gametogenesis - genetics</topic><topic>Gene expression</topic><topic>Genes</topic><topic>Genetic aspects</topic><topic>Genomics</topic><topic>Genotypes</topic><topic>Gonads</topic><topic>Homology</topic><topic>Humans</topic><topic>Identification and classification</topic><topic>Male</topic><topic>Maturation</topic><topic>Molecular modelling</topic><topic>Observations</topic><topic>Oogenesis</topic><topic>Ovaries</topic><topic>Ovary</topic><topic>Polyps</topic><topic>Reproduction (biology)</topic><topic>RNA-seq</topic><topic>Scleractinian corals</topic><topic>Sex</topic><topic>Sexual development</topic><topic>Sexual reproduction</topic><topic>Sperm</topic><topic>Sperm Motility</topic><topic>Spermatogenesis</topic><topic>Spermiogenesis</topic><topic>Stony corals</topic><topic>Testes</topic><topic>Testis</topic><topic>Transcriptome</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chiu, Yi-Ling</creatorcontrib><creatorcontrib>Shikina, Shinya</creatorcontrib><creatorcontrib>Yoshioka, Yuki</creatorcontrib><creatorcontrib>Shinzato, Chuya</creatorcontrib><creatorcontrib>Chang, Ching-Fong</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>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biological Sciences</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content (ProQuest)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals</collection><jtitle>BMC genomics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chiu, Yi-Ling</au><au>Shikina, Shinya</au><au>Yoshioka, Yuki</au><au>Shinzato, Chuya</au><au>Chang, Ching-Fong</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>De novo transcriptome assembly from the gonads of a scleractinian coral, Euphyllia ancora: molecular mechanisms underlying scleractinian gametogenesis</atitle><jtitle>BMC genomics</jtitle><addtitle>BMC Genomics</addtitle><date>2020-10-21</date><risdate>2020</risdate><volume>21</volume><issue>1</issue><spage>732</spage><epage>732</epage><pages>732-732</pages><artnum>732</artnum><issn>1471-2164</issn><eissn>1471-2164</eissn><abstract>Sexual reproduction of scleractinians has captured the attention of researchers and the general public for decades. Although extensive ecological data has been acquired, underlying molecular and cellular mechanisms remain largely unknown. In this study, to better understand mechanisms underlying gametogenesis, we isolated ovaries and testes at different developmental phases from a gonochoric coral, Euphyllia ancora, and adopted a transcriptomic approach to reveal sex- and phase-specific gene expression profiles. In particular, we explored genes associated with oocyte development and maturation, spermiogenesis, sperm motility / capacitation, and fertilization.
1.6 billion raw reads were obtained from 24 gonadal samples. De novo assembly of trimmed reads, and elimination of contigs derived from symbiotic dinoflagellates (Symbiodiniaceae) and other organisms yielded a reference E. ancora gonadal transcriptome of 35,802 contigs. Analysis of 4 developmental phases identified 2023 genes that were differentially expressed during oogenesis and 678 during spermatogenesis. In premature/mature ovaries, 631 genes were specifically upregulated, with 538 in mature testes. Upregulated genes included those involved in gametogenesis, gamete maturation, sperm motility / capacitation, and fertilization in other metazoans, including humans. Meanwhile, a large number of genes without homology to sequences in the SWISS-PROT database were also observed among upregulated genes in premature / mature ovaries and mature testes.
Our findings show that scleractinian gametogenesis shares many molecular characteristics with that of other metazoans, but it also possesses unique characteristics developed during cnidarian and/or scleractinian evolution. To the best of our knowledge, this study is the first to create a gonadal transcriptome assembly from any scleractinian. This study and associated datasets provide a foundation for future studies regarding gametogenesis and differences between male and female colonies from molecular and cellular perspectives. Furthermore, our transcriptome assembly will be a useful reference for future development of sex-specific and/or stage-specific germ cell markers that can be used in coral aquaculture and ecological studies.</abstract><cop>England</cop><pub>BioMed Central Ltd</pub><pmid>33087060</pmid><doi>10.1186/s12864-020-07113-9</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Anthozoa - genetics Aquaculture Assembly Capacitation Coral reefs Data acquisition Dinoflagellates Ecological studies Euphyllia ancora Female Fertilization Gametocytes Gametogenesis Gametogenesis - genetics Gene expression Genes Genetic aspects Genomics Genotypes Gonads Homology Humans Identification and classification Male Maturation Molecular modelling Observations Oogenesis Ovaries Ovary Polyps Reproduction (biology) RNA-seq Scleractinian corals Sex Sexual development Sexual reproduction Sperm Sperm Motility Spermatogenesis Spermiogenesis Stony corals Testes Testis Transcriptome |
title | De novo transcriptome assembly from the gonads of a scleractinian coral, Euphyllia ancora: molecular mechanisms underlying scleractinian gametogenesis |
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