{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,9]],"date-time":"2026-10-09T06:17:21Z","timestamp":1791526641174,"version":"4.3.4"},"reference-count":55,"publisher":"Oxford University Press (OUP)","issue":"11","license":[{"start":{"date-parts":[[2023,9,19]],"date-time":"2023-09-19T00:00:00Z","timestamp":1695081600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2023,11,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>In species with internal fertilization, sperm, and seminal fluid are transferred from male to female during mating. While both sperm and seminal fluid contain various types of molecules, including RNA, the role of most of these molecules in the coordination of fertilization or in other possible functions is poorly understood. In Drosophila, exosomes from the accessory gland, which produces seminal fluid, are transferred to females, but their potential cargoes have not been described. Moreover, while the RNA composition of sperm has been described in several mammalian species, little work on this problem has occurred in Drosophila. Here we use single nucleotide polymorphism differences between males and females from a set of highly inbred lines of D. melanogaster, and transcriptome data from the female reproductive tract, sperm, testis, and accessory gland, to investigate the potential origin, male vs female, RNA molecules isolated from 3 female reproductive tract organs, the seminal receptacle and spermatheca, which store sperm, and the parovaria, which does not. We find that mated females carry male-derived transcripts from many genes, including those that are markers of the accessory gland and known seminal fluid proteins. Our observations also support the idea that intact sperm transcripts can be isolated from the female sperm storage organs.<\/jats:p>","DOI":"10.1093\/g3journal\/jkad202","type":"journal-article","created":{"date-parts":[[2023,9,19]],"date-time":"2023-09-19T22:21:17Z","timestamp":1695162077000},"source":"Crossref","is-referenced-by-count":10,"title":["Male-derived transcripts isolated from the mated female reproductive tract in <i>Drosophila melanogaster<\/i>"],"prefix":"10.1093","volume":"13","author":[{"given":"Julie M","family":"Cridland","sequence":"first","affiliation":[{"name":"Department of Evolution and Ecology, University of California, Davis , Davis, CA 95616 , USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David J","family":"Begun","sequence":"additional","affiliation":[{"name":"Department of Evolution and Ecology, University of California, Davis , Davis, CA 95616 , USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2023,9,19]]},"reference":[{"issue":"3","key":"2024022107532332200_jkad202-B1","doi-asserted-by":"publisher","first-page":"986","DOI":"10.1093\/molbev\/msaa264","article-title":"Differences in postmating transcriptional responses between conspecific and heterospecific matings in Drosophila","volume":"38","author":"Ahmed-Braimah","year":"2021","journal-title":"Mol Biol Evol."},{"issue":"2","key":"2024022107532332200_jkad202-B2","doi-asserted-by":"publisher","first-page":"e0004451","DOI":"10.1371\/journal.pntd.0004451","article-title":"Mating-induced transcriptome changes in the reproductive tract of female Aedes aegypti","volume":"10","author":"Alfonso-Parra","year":"2016","journal-title":"PLoS Negl. Trop. Dis"},{"issue":"1","key":"2024022107532332200_jkad202-B3","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1146\/annurev-ento-120709-144823","article-title":"Insect seminal fluid proteins: identification and function","volume":"56","author":"Avila","year":"2011","journal-title":"Annu Rev Entomol."},{"key":"2024022107532332200_jkad202-B4","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1016\/bs.acc.2019.08.004","article-title":"Exosomes of male reproduction","volume":"95","author":"Baskaran","year":"2020","journal-title":"Adv Clin Chem."},{"issue":"19","key":"2024022107532332200_jkad202-B5","doi-asserted-by":"publisher","first-page":"7878","DOI":"10.1073\/pnas.1100388108","article-title":"Postmating transcriptional changes in reproductive tracts of con- and heterospecifically mated Drosophila mojavensis females","volume":"108","author":"Bono","year":"2011","journal-title":"Proc Natl Acad Sci U S A."},{"issue":"1","key":"2024022107532332200_jkad202-B6","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1093\/genetics\/139.1.189","article-title":"Variation in sperm displacement and its association with accessory gland protein loci in Drosophila melanogaster","volume":"139","author":"Clark","year":"1995","journal-title":"Genetics"},{"issue":"3","key":"2024022107532332200_jkad202-B7","doi-asserted-by":"publisher","first-page":"1487","DOI":"10.1093\/genetics\/149.3.1487","article-title":"Female genotypes affect sperm displacement in Drosophila","volume":"149","author":"Clark","year":"1998","journal-title":"Genetics"},{"issue":"5399","key":"2024022107532332200_jkad202-B8","doi-asserted-by":"publisher","first-page":"217","DOI":"10.1126\/science.283.5399.217","article-title":"Female x male interactions in Drosophila sperm competition","volume":"283","author":"Clark","year":"1999","journal-title":"Science"},{"issue":"5","key":"2024022107532332200_jkad202-B9","doi-asserted-by":"publisher","first-page":"671","DOI":"10.1083\/jcb.201401072","article-title":"BMP-regulated exosomes from Drosophila male reproductive glands reprogram female behavior","volume":"206","author":"Corrigan","year":"2014","journal-title":"J. Cell Biol"},{"issue":"1","key":"2024022107532332200_jkad202-B10","doi-asserted-by":"publisher","first-page":"79","DOI":"10.1534\/genetics.120.303515","article-title":"Polymorphism and divergence of novel gene expression patterns in Drosophila melanogaster","volume":"216","author":"Cridland","year":"2020","journal-title":"Genetics"},{"issue":"1","key":"2024022107532332200_jkad202-B11","doi-asserted-by":"publisher","first-page":"iyab207","DOI":"10.1093\/genetics\/iyab207","article-title":"Population biology of accessory gland-expressed de novo genes in Drosophila melanogaster","volume":"220","author":"Cridland","year":"2022","journal-title":"Genetics"},{"issue":"2","key":"2024022107532332200_jkad202-B12","doi-asserted-by":"publisher","first-page":"giab008","DOI":"10.1093\/gigascience\/giab008","article-title":"Twelve years of SAMtools and BCFtools","volume":"10","author":"Danecek","year":"2021","journal-title":"Gigascience"},{"key":"2024022107532332200_jkad202-B13","first-page":"1","volume-title":"Current Topics in Developmental Biology","author":"Fitch","year":"1997"},{"issue":"2","key":"2024022107532332200_jkad202-B14","doi-asserted-by":"publisher","first-page":"1245","DOI":"10.1534\/genetics.106.064915","article-title":"Associations between sperm competition and natural variation in male reproductive genes on the third chromosome of Drosophila melanogaster","volume":"176","author":"Fiumera","year":"2007","journal-title":"Genetics"},{"key":"2024022107532332200_jkad202-B15","first-page":"293","volume-title":"Advances in Genetics","author":"Fowler","year":"1973"},{"issue":"19","key":"2024022107532332200_jkad202-B16","doi-asserted-by":"publisher","first-page":"4098","DOI":"10.1111\/j.1365-294X.2011.05253.x","article-title":"Female influence on pre- and post-copulatory sexual selection and its genetic basis in Drosophila melanogaster","volume":"20","author":"Giardina","year":"2011","journal-title":"Mol Ecol."},{"issue":"4","key":"2024022107532332200_jkad202-B17","doi-asserted-by":"publisher","first-page":"iyac035","DOI":"10.1093\/genetics\/iyac035","article-title":"FlyBase: a guided tour of highlighted features","volume":"220","author":"Gramates","year":"2022","journal-title":"Genetics"},{"issue":"3","key":"2024022107532332200_jkad202-B18","doi-asserted-by":"publisher","first-page":"758","DOI":"10.2307\/2410484","article-title":"Sperm displacement without sperm transfer in Drosophila melanogaster","volume":"48","author":"Harshman","year":"1994","journal-title":"Evolution"},{"issue":"22","key":"2024022107532332200_jkad202-B19","doi-asserted-by":"publisher","first-page":"10114","DOI":"10.1073\/pnas.92.22.10114","article-title":"A Drosophila seminal fluid protein, Acp26Aa, stimulates egg laying in females for 1 day after mating","volume":"92","author":"Herndon","year":"1995","journal-title":"Proc Natl Acad Sci U S A."},{"issue":"9","key":"2024022107532332200_jkad202-B20","doi-asserted-by":"publisher","first-page":"5083","DOI":"10.1073\/pnas.96.9.5083","article-title":"Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes a reproductive load","volume":"96","author":"Holland","year":"1999","journal-title":"Proc Natl Acad Sci U S A."},{"key":"2024022107532332200_jkad202-B21","first-page":"137","author":"Hopkins","year":"2018"},{"issue":"8","key":"2024022107532332200_jkad202-B22","doi-asserted-by":"publisher","first-page":"451","DOI":"10.1016\/j.tree.2014.05.006","article-title":"Why do sperm carry RNA? Relatedness, conflict, and control","volume":"29","author":"Hosken","year":"2014","journal-title":"Trends Ecol. Evol"},{"issue":"1","key":"2024022107532332200_jkad202-B23","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1093\/nar\/gkn923","article-title":"Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists","volume":"37","author":"Huang","year":"2009","journal-title":"Nucleic Acids Res"},{"issue":"1","key":"2024022107532332200_jkad202-B24","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1038\/nprot.2008.211","article-title":"Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources","volume":"4","author":"Huang","year":"2009","journal-title":"Nat Protoc."},{"issue":"15","key":"2024022107532332200_jkad202-B25","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2001897118","article-title":"Identification of a micropeptide and multiple secondary cell genes that modulate Drosophila male reproductive success","volume":"118","author":"Immarigeon","year":"2021","journal-title":"Proc Natl Acad Sci U S A."},{"issue":"6","key":"2024022107532332200_jkad202-B26","doi-asserted-by":"publisher","first-page":"604","DOI":"10.1093\/humupd\/dmt031","article-title":"The presence, role and clinical use of spermatozoal RNAs","volume":"19","author":"Jodar","year":"2013","journal-title":"Hum Reprod Update."},{"issue":"4","key":"2024022107532332200_jkad202-B27","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1038\/nmeth.3317","article-title":"HISAT: a fast spliced aligner with low memory requirements","volume":"12","author":"Kim","year":"2015","journal-title":"Nat Methods."},{"issue":"15","key":"2024022107532332200_jkad202-B28","doi-asserted-by":"publisher","first-page":"8692","DOI":"10.1073\/pnas.151123998","article-title":"Sexually antagonistic coevolution of a postmating-prezygotic reproductive character in desert Drosophila","volume":"98","author":"Knowles","year":"2001","journal-title":"Proc Natl Acad Sci U S A."},{"issue":"4","key":"2024022107532332200_jkad202-B29","doi-asserted-by":"publisher","first-page":"1229","DOI":"10.1534\/genetics.115.174664","article-title":"The Drosophila genome nexus: a population genomic resource of 623 Drosophila melanogaster genomes, including 197 from a single ancestral range population","volume":"199","author":"Lack","year":"2015","journal-title":"Genetics"},{"issue":"47","key":"2024022107532332200_jkad202-B30","doi-asserted-by":"publisher","first-page":"19292","DOI":"10.1073\/pnas.1214517109","article-title":"Bone morphogenetic protein- and mating-dependent secretory cell growth and migration in the Drosophila accessory gland","volume":"109","author":"Leiblich","year":"2012","journal-title":"Proc Natl Acad Sci U S A."},{"issue":"8","key":"2024022107532332200_jkad202-B31","doi-asserted-by":"publisher","first-page":"jkad122","DOI":"10.1093\/g3journal\/jkad122","article-title":"Identifying candidate de novo genes expressed in the somatic female reproductive tract of Drosophila melanogaster","volume":"13","author":"Lombardo","year":"2023","journal-title":"G3 (Bethesda)"},{"issue":"7384","key":"2024022107532332200_jkad202-B32","doi-asserted-by":"publisher","first-page":"173","DOI":"10.1038\/nature10811","article-title":"The Drosophila melanogaster genetic reference panel","volume":"482","author":"Mackay","year":"2012","journal-title":"Nature"},{"issue":"2","key":"2024022107532332200_jkad202-B33","doi-asserted-by":"publisher","first-page":"iyab213","DOI":"10.1093\/genetics\/iyab213","article-title":"Single-nucleus transcriptomes reveal evolutionary and functional properties of cell types in the Drosophila accessory gland","volume":"220","author":"Majane","year":"2022","journal-title":"Genetics"},{"issue":"5976","key":"2024022107532332200_jkad202-B34","doi-asserted-by":"publisher","first-page":"354","DOI":"10.1126\/science.1187096","article-title":"Resolving mechanisms of competitive fertilization success in Drosophila melanogaster","volume":"328","author":"Manier","year":"2010","journal-title":"Science"},{"issue":"11","key":"2024022107532332200_jkad202-B35","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2119899119","article-title":"The life history of Drosophila sperm involves molecular continuity between male and female reproductive tracts","volume":"119","author":"McCullough","year":"2022","journal-title":"Proc Natl Acad Sci U S A."},{"issue":"3","key":"2024022107532332200_jkad202-B36","doi-asserted-by":"publisher","first-page":"jkab020","DOI":"10.1093\/g3journal\/jkab020","article-title":"Drosophila Female reproductive tract gene expression reveals coordinated mating responses and rapidly evolving tissue-specific genes","volume":"11","author":"McDonough-Goldstein","year":"2021","journal-title":"G3 (Bethesda)"},{"issue":"4","key":"2024022107532332200_jkad202-B37","doi-asserted-by":"publisher","first-page":"156","DOI":"10.1016\/j.molmed.2005.02.006","article-title":"The controversy, potential and roles of spermatozoal RNA","volume":"11","author":"Miller","year":"2005","journal-title":"Trends Mol Med."},{"issue":"6","key":"2024022107532332200_jkad202-B38","doi-asserted-by":"publisher","first-page":"1352","DOI":"10.1016\/j.cell.2014.11.005","article-title":"Paternal diet defines offspring chromatin state and intergenerational obesity","volume":"159","author":"\u00d6st","year":"2014","journal-title":"Cell"},{"issue":"9335","key":"2024022107532332200_jkad202-B39","doi-asserted-by":"publisher","first-page":"772","DOI":"10.1016\/S0140-6736(02)09899-9","article-title":"Spermatozoal RNA profiles of normal fertile men","volume":"360","author":"Ostermeier","year":"2002","journal-title":"Lancet"},{"key":"2024022107532332200_jkad202-B40","first-page":"123","volume-title":"Sexual Selection and Reproductive Competition in Insects","author":"Parker","year":"1979"},{"issue":"1","key":"2024022107532332200_jkad202-B41","doi-asserted-by":"publisher","first-page":"20","DOI":"10.1186\/s12862-022-01975-1","article-title":"Seminal fluid gene expression and reproductive fitness in Drosophila melanogaster","volume":"22","author":"Patlar","year":"2022","journal-title":"BMC Ecol Evol"},{"key":"2024022107532332200_jkad202-B42","volume-title":"Evolution in the Genus Drosophila","author":"Patterson","year":"1952"},{"issue":"3","key":"2024022107532332200_jkad202-B43","doi-asserted-by":"publisher","first-page":"290","DOI":"10.1038\/nbt.3122","article-title":"Stringtie enables improved reconstruction of a transcriptome from RNA-Seq reads","volume":"33","author":"Pertea","year":"2015","journal-title":"Nat Biotechnol."},{"issue":"6","key":"2024022107532332200_jkad202-B44","doi-asserted-by":"publisher","first-page":"1804","DOI":"10.1111\/j.1558-5646.1999.tb04564.x","article-title":"Evolution of multiple kinds of female sperm-storage organs in Drosophila","volume":"53","author":"Pitnick","year":"1999","journal-title":"Evolution"},{"issue":"49","key":"2024022107532332200_jkad202-B45","doi-asserted-by":"publisher","first-page":"18674","DOI":"10.1073\/pnas.0606228103","article-title":"Predicted seminal astacin-like protease is required for processing of reproductive proteins in Drosophila melanogaster","volume":"103","author":"Ravi Ram","year":"2006","journal-title":"Proc Natl Acad Sci U S A."},{"issue":"12","key":"2024022107532332200_jkad202-B46","doi-asserted-by":"publisher","first-page":"e238","DOI":"10.1371\/journal.pgen.0030238","article-title":"Sustained post-mating response in Drosophila melanogaster requires multiple seminal fluid proteins","volume":"3","author":"Ravi Ram","year":"2007","journal-title":"PLoS Genet"},{"issue":"3","key":"2024022107532332200_jkad202-B47","doi-asserted-by":"publisher","first-page":"427","DOI":"10.1093\/icb\/icm046","article-title":"Seminal influences: Drosophila acps and the molecular interplay between males and females during reproduction","volume":"47","author":"Ravi Ram","year":"2007","journal-title":"Integr Comp Biol."},{"issue":"6579)","key":"2024022107532332200_jkad202-B48","doi-asserted-by":"publisher","first-page":"232","DOI":"10.1038\/381232a0","article-title":"Sexually antagonistic male adaptation triggered by experimental arrest of female evolution","volume":"381","author":"Rice","year":"1996","journal-title":"Nature"},{"key":"2024022107532332200_jkad202-B49","doi-asserted-by":"publisher","first-page":"e1001192","DOI":"10.1371\/journal.pbio.1001192","article-title":"Sperm-storage defects and live birth in Drosophila females lacking spermathecal secretory cells","volume":"9","author":"Schnakenberg","year":"2011","journal-title":"PLoS Biol"},{"issue":"7","key":"2024022107532332200_jkad202-B50","doi-asserted-by":"publisher","first-page":"4104","DOI":"10.1093\/nar\/gkt132","article-title":"Stability, delivery and functions of human sperm RNAs at fertilization","volume":"41","author":"Sendler","year":"2013","journal-title":"Nucleic Acids Res"},{"issue":"Suppl_1","key":"2024022107532332200_jkad202-B51","doi-asserted-by":"publisher","first-page":"347","DOI":"10.1093\/biolreprod\/87.s1.347","article-title":"Female reproductive glands play essential roles in reproduction that may have been conserved during evolution","volume":"87","author":"Sun","year":"2012","journal-title":"Biol Reprod."},{"key":"2024022107532332200_jkad202-B52","doi-asserted-by":"publisher","first-page":"e00415","DOI":"10.7554\/eLife.00415","article-title":"Ovulation in Drosophila is controlled by secretory cells of the female reproductive tract","volume":"2","author":"Sun","year":"2013","journal-title":"Elife"},{"issue":"1813","key":"2024022107532332200_jkad202-B53","doi-asserted-by":"publisher","first-page":"20200072","DOI":"10.1098\/rstb.2020.0072","article-title":"The Drosophila seminal proteome and its role in postcopulatory sexual selection","volume":"375","author":"Wigby","year":"2020","journal-title":"Philos Trans R Soc Lond B Biol Sci"},{"issue":"11","key":"2024022107532332200_jkad202-B54","doi-asserted-by":"publisher","first-page":"e1001191","DOI":"10.1371\/journal.pbio.1001191","article-title":"Precious essences: female secretions promote sperm storage in Drosophila","volume":"9","author":"Wolfner","year":"2011","journal-title":"PLoS Biol"},{"issue":"2","key":"2024022107532332200_jkad202-B55","doi-asserted-by":"publisher","first-page":"921","DOI":"10.1534\/genetics.108.092106","article-title":"A role for Acp29AB, a predicted seminal fluid lectin, in female sperm storage in Drosophila melanogaster","volume":"180","author":"Wong","year":"2008","journal-title":"Genetics"}],"container-title":["G3: Genes, Genomes, Genetics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/g3journal\/advance-article-pdf\/doi\/10.1093\/g3journal\/jkad202\/51706393\/jkad202.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/g3journal\/article-pdf\/13\/11\/jkad202\/56715295\/jkad202.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/g3journal\/article-pdf\/13\/11\/jkad202\/56715295\/jkad202.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,2,21]],"date-time":"2024-02-21T07:53:28Z","timestamp":1708502008000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/g3journal\/article\/doi\/10.1093\/g3journal\/jkad202\/7277365"}},"subtitle":[],"editor":[{"given":"E","family":"Betran","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2023,9,19]]},"references-count":55,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2023,9,19]]},"published-print":{"date-parts":[[2023,11,1]]}},"URL":"https:\/\/doi.org\/10.1093\/g3journal\/jkad202","relation":{},"ISSN":["2160-1836"],"issn-type":[{"value":"2160-1836","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2023,11]]},"published":{"date-parts":[[2023,9,19]]},"article-number":"jkad202"}}