Global expression pattern of genes containing positively selected sites in European anchovy (Engraulis encrasicolus L.) may shed light on teleost reproduction
European anchovy is a multiple-spawning and highly fecundate pelagic fish with high economic and ecological significance. Although fecundity is influenced by nutrition, temperature and weight of spawners, high reproductive capacity is related to molecular processes in the ovary. The ovary is an esse...
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description | European anchovy is a multiple-spawning and highly fecundate pelagic fish with high economic and ecological significance. Although fecundity is influenced by nutrition, temperature and weight of spawners, high reproductive capacity is related to molecular processes in the ovary. The ovary is an essential and complex reproductive organ composed of various somatic and germ cells, which interact to facilitate the development of the ovary and functional oocytes. Revealing the ovarian transcriptome profile of highly fecundate fishes provides insights into oocyte production in teleosts. Here we use a comprehensive tissue-specific RNA sequencing which yielded 102.3 billion clean bases to analyze the transcriptional profiles of the ovary compared with other organs (liver, kidney, ovary, testis, fin, cauda and gill) and juvenile tissues of European anchovy. We conducted a comparative transcriptome and positive selection analysis of seven teleost species with varying fecundity rates to identify genes potentially involved in oogenesis and oocyte development. Of the 2,272 single copies of orthologous genes found, up to 535 genes were under positive selection in European anchovy and these genes are associated with a wide spectrum of cellular and molecular functions, with enrichments such as RNA methylation and modification, ribosome biogenesis, DNA repair, cell cycle processing and peptide/amide biosynthesis. Of the 535 positively selected genes, 55 were upregulated, and 45 were downregulated in the ovary, most of which were related to RNA and DNA transferase, developmental transcription factors, protein kinases and replication factors. Overall, our analysis of the transcriptome level in the ovarian tissue of a teleost will provide further insights into molecular processes and deepen our genetic understanding of egg production in highly fecund fish. |
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Although fecundity is influenced by nutrition, temperature and weight of spawners, high reproductive capacity is related to molecular processes in the ovary. The ovary is an essential and complex reproductive organ composed of various somatic and germ cells, which interact to facilitate the development of the ovary and functional oocytes. Revealing the ovarian transcriptome profile of highly fecundate fishes provides insights into oocyte production in teleosts. Here we use a comprehensive tissue-specific RNA sequencing which yielded 102.3 billion clean bases to analyze the transcriptional profiles of the ovary compared with other organs (liver, kidney, ovary, testis, fin, cauda and gill) and juvenile tissues of European anchovy. We conducted a comparative transcriptome and positive selection analysis of seven teleost species with varying fecundity rates to identify genes potentially involved in oogenesis and oocyte development. Of the 2,272 single copies of orthologous genes found, up to 535 genes were under positive selection in European anchovy and these genes are associated with a wide spectrum of cellular and molecular functions, with enrichments such as RNA methylation and modification, ribosome biogenesis, DNA repair, cell cycle processing and peptide/amide biosynthesis. Of the 535 positively selected genes, 55 were upregulated, and 45 were downregulated in the ovary, most of which were related to RNA and DNA transferase, developmental transcription factors, protein kinases and replication factors. Overall, our analysis of the transcriptome level in the ovarian tissue of a teleost will provide further insights into molecular processes and deepen our genetic understanding of egg production in highly fecund fish.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0289940</identifier><identifier>PMID: 37566603</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Anchovies ; Animal reproduction ; Biology ; Biology and Life Sciences ; Biosynthesis ; Cell cycle ; Cell division ; Deoxyribonucleic acid ; Distribution ; DNA ; DNA methylation ; DNA repair ; Ecological effects ; Egg production ; Eggs ; Engraulis encrasicolus ; Environmental sustainability ; Ethics ; Evaluation ; Fecundity ; Fish ; Fish reproduction ; Fishing ; Food chains ; Gametocytes ; Gene expression ; Gene sequencing ; Genes ; Genetic aspects ; Genetic engineering ; Germ cells ; Juveniles ; Kinases ; Liver ; Medicine and Health Sciences ; Oocytes ; Oogenesis ; Ovaries ; Positive selection ; Reproductive organs ; Research and Analysis Methods ; Ribonucleic acid ; RNA ; RNA modification ; Spawning ; Success ; Tissues ; Transcription factors ; Transcriptomes</subject><ispartof>PloS one, 2023-08, Vol.18 (8), p.e0289940-e0289940</ispartof><rights>Copyright: © 2023 Eldem 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 Eldem 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>2023 Eldem et al 2023 Eldem et al</rights><rights>2023 Eldem 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. 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Although fecundity is influenced by nutrition, temperature and weight of spawners, high reproductive capacity is related to molecular processes in the ovary. The ovary is an essential and complex reproductive organ composed of various somatic and germ cells, which interact to facilitate the development of the ovary and functional oocytes. Revealing the ovarian transcriptome profile of highly fecundate fishes provides insights into oocyte production in teleosts. Here we use a comprehensive tissue-specific RNA sequencing which yielded 102.3 billion clean bases to analyze the transcriptional profiles of the ovary compared with other organs (liver, kidney, ovary, testis, fin, cauda and gill) and juvenile tissues of European anchovy. We conducted a comparative transcriptome and positive selection analysis of seven teleost species with varying fecundity rates to identify genes potentially involved in oogenesis and oocyte development. 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expression pattern of genes containing positively selected sites in European anchovy (Engraulis encrasicolus L.) may shed light on teleost reproduction</title><author>Eldem, Vahap ; Zararsız, Gökmen ; Erkan, Melike</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c489t-6d1df8c7e26757300c989cdac28f575c457e678b0e6b3741f04edae43a5b6d93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Anchovies</topic><topic>Animal reproduction</topic><topic>Biology</topic><topic>Biology and Life Sciences</topic><topic>Biosynthesis</topic><topic>Cell cycle</topic><topic>Cell division</topic><topic>Deoxyribonucleic acid</topic><topic>Distribution</topic><topic>DNA</topic><topic>DNA methylation</topic><topic>DNA repair</topic><topic>Ecological effects</topic><topic>Egg production</topic><topic>Eggs</topic><topic>Engraulis encrasicolus</topic><topic>Environmental 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expression pattern of genes containing positively selected sites in European anchovy (Engraulis encrasicolus L.) may shed light on teleost reproduction</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2023-08-11</date><risdate>2023</risdate><volume>18</volume><issue>8</issue><spage>e0289940</spage><epage>e0289940</epage><pages>e0289940-e0289940</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>European anchovy is a multiple-spawning and highly fecundate pelagic fish with high economic and ecological significance. Although fecundity is influenced by nutrition, temperature and weight of spawners, high reproductive capacity is related to molecular processes in the ovary. The ovary is an essential and complex reproductive organ composed of various somatic and germ cells, which interact to facilitate the development of the ovary and functional oocytes. Revealing the ovarian transcriptome profile of highly fecundate fishes provides insights into oocyte production in teleosts. Here we use a comprehensive tissue-specific RNA sequencing which yielded 102.3 billion clean bases to analyze the transcriptional profiles of the ovary compared with other organs (liver, kidney, ovary, testis, fin, cauda and gill) and juvenile tissues of European anchovy. We conducted a comparative transcriptome and positive selection analysis of seven teleost species with varying fecundity rates to identify genes potentially involved in oogenesis and oocyte development. Of the 2,272 single copies of orthologous genes found, up to 535 genes were under positive selection in European anchovy and these genes are associated with a wide spectrum of cellular and molecular functions, with enrichments such as RNA methylation and modification, ribosome biogenesis, DNA repair, cell cycle processing and peptide/amide biosynthesis. Of the 535 positively selected genes, 55 were upregulated, and 45 were downregulated in the ovary, most of which were related to RNA and DNA transferase, developmental transcription factors, protein kinases and replication factors. 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subjects | Anchovies Animal reproduction Biology Biology and Life Sciences Biosynthesis Cell cycle Cell division Deoxyribonucleic acid Distribution DNA DNA methylation DNA repair Ecological effects Egg production Eggs Engraulis encrasicolus Environmental sustainability Ethics Evaluation Fecundity Fish Fish reproduction Fishing Food chains Gametocytes Gene expression Gene sequencing Genes Genetic aspects Genetic engineering Germ cells Juveniles Kinases Liver Medicine and Health Sciences Oocytes Oogenesis Ovaries Positive selection Reproductive organs Research and Analysis Methods Ribonucleic acid RNA RNA modification Spawning Success Tissues Transcription factors Transcriptomes |
title | Global expression pattern of genes containing positively selected sites in European anchovy (Engraulis encrasicolus L.) may shed light on teleost reproduction |
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