Ocnus is essential for male germ cell development in Drosophila melanogaster

The ocnus (ocn) gene encodes a protein abundant in the testes, implying its role in testis development. When Drosophila melanogaster is infected with the endosymbiont wMel Wolbachia, which affects the spermatogenesis of its hosts, ocn is downregulated in the third‐instar larval testes, suggesting a...

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Veröffentlicht in:Insect molecular biology 2018-10, Vol.27 (5), p.545-555
Hauptverfasser: Zheng, Y., Bi, J., Hou, M.‐Y., Shen, W., Zhang, W., Ai, H., Yu, X.‐Q., Wang, Y.‐F.
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container_end_page 555
container_issue 5
container_start_page 545
container_title Insect molecular biology
container_volume 27
creator Zheng, Y.
Bi, J.
Hou, M.‐Y.
Shen, W.
Zhang, W.
Ai, H.
Yu, X.‐Q.
Wang, Y.‐F.
description The ocnus (ocn) gene encodes a protein abundant in the testes, implying its role in testis development. When Drosophila melanogaster is infected with the endosymbiont wMel Wolbachia, which affects the spermatogenesis of its hosts, ocn is downregulated in the third‐instar larval testes, suggesting a role of ocn in spermatogenesis. In this study, we knocked down ocn in the testes and found that the hatch rates of embryos derived from ocn‐knockdown males were significantly decreased, and 84.38% of the testes were much smaller in comparison to controls. Analysis of the smaller testes showed no germ cells but they had an extended hub. Using RNA‐sequencing (RNA‐Seq), we identified 69 genes with at least a twofold change (q‐value 
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When Drosophila melanogaster is infected with the endosymbiont wMel Wolbachia, which affects the spermatogenesis of its hosts, ocn is downregulated in the third‐instar larval testes, suggesting a role of ocn in spermatogenesis. In this study, we knocked down ocn in the testes and found that the hatch rates of embryos derived from ocn‐knockdown males were significantly decreased, and 84.38% of the testes were much smaller in comparison to controls. Analysis of the smaller testes showed no germ cells but they had an extended hub. Using RNA‐sequencing (RNA‐Seq), we identified 69 genes with at least a twofold change (q‐value &lt; 5%) in their expression after ocn knockdown; of these, eight testes‐specific and three reproduction‐related genes were verified to be significantly downregulated using quantitative reverse transcription‐PCR. Three genes (orientation disruptor, p24‐2 and CG13541) were also significantly downregulated in the presence of Wolbachia. Furthermore, 98 genes were not expressed when ocn was knocked down in testes. These results suggest that ocn plays a crucial role in male germ cell development in Drosophila, possibly by regulating the expression of multiple spermatogenesis‐related genes. Our data provide important information to help understand the molecular regulatory mechanisms underlying spermatogenesis.</description><identifier>ISSN: 0962-1075</identifier><identifier>EISSN: 1365-2583</identifier><identifier>DOI: 10.1111/imb.12393</identifier><identifier>PMID: 29732657</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Drosophila melanogaster ; Embryos ; Gene expression ; Gene sequencing ; Genes ; germ cell ; Germ cells ; Insects ; Males ; ocnus ; Proteins ; Regulatory mechanisms (biology) ; Reverse transcription ; Ribonucleic acid ; RNA ; RNA‐seq ; Spermatogenesis ; Testes ; testis ; Wolbachia</subject><ispartof>Insect molecular biology, 2018-10, Vol.27 (5), p.545-555</ispartof><rights>2018 The Royal Entomological Society</rights><rights>2018 The Royal Entomological Society.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3533-f641fe04eac17a43a28fb4177ca6bf56238b8b5ffd265d7bd28598b0655b1ae63</citedby><cites>FETCH-LOGICAL-c3533-f641fe04eac17a43a28fb4177ca6bf56238b8b5ffd265d7bd28598b0655b1ae63</cites><orcidid>0000-0002-1823-373X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fimb.12393$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fimb.12393$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,27924,27925,45574,45575</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29732657$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zheng, Y.</creatorcontrib><creatorcontrib>Bi, J.</creatorcontrib><creatorcontrib>Hou, M.‐Y.</creatorcontrib><creatorcontrib>Shen, W.</creatorcontrib><creatorcontrib>Zhang, W.</creatorcontrib><creatorcontrib>Ai, H.</creatorcontrib><creatorcontrib>Yu, X.‐Q.</creatorcontrib><creatorcontrib>Wang, Y.‐F.</creatorcontrib><title>Ocnus is essential for male germ cell development in Drosophila melanogaster</title><title>Insect molecular biology</title><addtitle>Insect Mol Biol</addtitle><description>The ocnus (ocn) gene encodes a protein abundant in the testes, implying its role in testis development. When Drosophila melanogaster is infected with the endosymbiont wMel Wolbachia, which affects the spermatogenesis of its hosts, ocn is downregulated in the third‐instar larval testes, suggesting a role of ocn in spermatogenesis. In this study, we knocked down ocn in the testes and found that the hatch rates of embryos derived from ocn‐knockdown males were significantly decreased, and 84.38% of the testes were much smaller in comparison to controls. Analysis of the smaller testes showed no germ cells but they had an extended hub. Using RNA‐sequencing (RNA‐Seq), we identified 69 genes with at least a twofold change (q‐value &lt; 5%) in their expression after ocn knockdown; of these, eight testes‐specific and three reproduction‐related genes were verified to be significantly downregulated using quantitative reverse transcription‐PCR. Three genes (orientation disruptor, p24‐2 and CG13541) were also significantly downregulated in the presence of Wolbachia. Furthermore, 98 genes were not expressed when ocn was knocked down in testes. These results suggest that ocn plays a crucial role in male germ cell development in Drosophila, possibly by regulating the expression of multiple spermatogenesis‐related genes. Our data provide important information to help understand the molecular regulatory mechanisms underlying spermatogenesis.</description><subject>Drosophila melanogaster</subject><subject>Embryos</subject><subject>Gene expression</subject><subject>Gene sequencing</subject><subject>Genes</subject><subject>germ cell</subject><subject>Germ cells</subject><subject>Insects</subject><subject>Males</subject><subject>ocnus</subject><subject>Proteins</subject><subject>Regulatory mechanisms (biology)</subject><subject>Reverse transcription</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA‐seq</subject><subject>Spermatogenesis</subject><subject>Testes</subject><subject>testis</subject><subject>Wolbachia</subject><issn>0962-1075</issn><issn>1365-2583</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><recordid>eNp10DtPwzAUBWALgWgpDPwBZIkFhlA_ascZobwqFXWB2bKTa0jlJMVuQPx7XAoMSHi5y6ej44PQMSUXNL1x3dgLynjBd9CQcikyJhTfRUNSSJZRkosBOohxSQhRhSz20YAVOWdS5EM0X5RtH3EdMcQI7bo2Hrsu4MZ4wM8QGlyC97iCN_DdqkkC1y2-Dl3sVi-1N7gBb9ru2cQ1hEO054yPcPR9R-jp9uZxep_NF3ez6eU8K7ngPHNyQh2QCZiS5mbCDVPOTmiel0ZaJyTjyiornKtSxyq3FVOiUJZIISw1IPkInW1zV6F77SGudVPHTU_TQtdHzQgXOZFKbujpH7rs-tCmdppRohTjlImkzreqTB-LAZxehbox4UNTojcT6zSx_po42ZPvxN42UP3Kn00TGG_Be-3h4_8kPXu42kZ-Ap0xhJM</recordid><startdate>201810</startdate><enddate>201810</enddate><creator>Zheng, Y.</creator><creator>Bi, J.</creator><creator>Hou, M.‐Y.</creator><creator>Shen, W.</creator><creator>Zhang, W.</creator><creator>Ai, H.</creator><creator>Yu, X.‐Q.</creator><creator>Wang, Y.‐F.</creator><general>Blackwell Publishing Ltd</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-1823-373X</orcidid></search><sort><creationdate>201810</creationdate><title>Ocnus is essential for male germ cell development in Drosophila melanogaster</title><author>Zheng, Y. ; Bi, J. ; Hou, M.‐Y. ; Shen, W. ; Zhang, W. ; Ai, H. ; Yu, X.‐Q. ; Wang, Y.‐F.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3533-f641fe04eac17a43a28fb4177ca6bf56238b8b5ffd265d7bd28598b0655b1ae63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Drosophila melanogaster</topic><topic>Embryos</topic><topic>Gene expression</topic><topic>Gene sequencing</topic><topic>Genes</topic><topic>germ cell</topic><topic>Germ cells</topic><topic>Insects</topic><topic>Males</topic><topic>ocnus</topic><topic>Proteins</topic><topic>Regulatory mechanisms (biology)</topic><topic>Reverse transcription</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>RNA‐seq</topic><topic>Spermatogenesis</topic><topic>Testes</topic><topic>testis</topic><topic>Wolbachia</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zheng, Y.</creatorcontrib><creatorcontrib>Bi, J.</creatorcontrib><creatorcontrib>Hou, M.‐Y.</creatorcontrib><creatorcontrib>Shen, W.</creatorcontrib><creatorcontrib>Zhang, W.</creatorcontrib><creatorcontrib>Ai, H.</creatorcontrib><creatorcontrib>Yu, X.‐Q.</creatorcontrib><creatorcontrib>Wang, Y.‐F.</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Insect molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zheng, Y.</au><au>Bi, J.</au><au>Hou, M.‐Y.</au><au>Shen, W.</au><au>Zhang, W.</au><au>Ai, H.</au><au>Yu, X.‐Q.</au><au>Wang, Y.‐F.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Ocnus is essential for male germ cell development in Drosophila melanogaster</atitle><jtitle>Insect molecular biology</jtitle><addtitle>Insect Mol Biol</addtitle><date>2018-10</date><risdate>2018</risdate><volume>27</volume><issue>5</issue><spage>545</spage><epage>555</epage><pages>545-555</pages><issn>0962-1075</issn><eissn>1365-2583</eissn><abstract>The ocnus (ocn) gene encodes a protein abundant in the testes, implying its role in testis development. When Drosophila melanogaster is infected with the endosymbiont wMel Wolbachia, which affects the spermatogenesis of its hosts, ocn is downregulated in the third‐instar larval testes, suggesting a role of ocn in spermatogenesis. In this study, we knocked down ocn in the testes and found that the hatch rates of embryos derived from ocn‐knockdown males were significantly decreased, and 84.38% of the testes were much smaller in comparison to controls. Analysis of the smaller testes showed no germ cells but they had an extended hub. Using RNA‐sequencing (RNA‐Seq), we identified 69 genes with at least a twofold change (q‐value &lt; 5%) in their expression after ocn knockdown; of these, eight testes‐specific and three reproduction‐related genes were verified to be significantly downregulated using quantitative reverse transcription‐PCR. Three genes (orientation disruptor, p24‐2 and CG13541) were also significantly downregulated in the presence of Wolbachia. Furthermore, 98 genes were not expressed when ocn was knocked down in testes. These results suggest that ocn plays a crucial role in male germ cell development in Drosophila, possibly by regulating the expression of multiple spermatogenesis‐related genes. Our data provide important information to help understand the molecular regulatory mechanisms underlying spermatogenesis.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>29732657</pmid><doi>10.1111/imb.12393</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0002-1823-373X</orcidid></addata></record>
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source Wiley Online Library Journals Frontfile Complete
subjects Drosophila melanogaster
Embryos
Gene expression
Gene sequencing
Genes
germ cell
Germ cells
Insects
Males
ocnus
Proteins
Regulatory mechanisms (biology)
Reverse transcription
Ribonucleic acid
RNA
RNA‐seq
Spermatogenesis
Testes
testis
Wolbachia
title Ocnus is essential for male germ cell development in Drosophila melanogaster
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