{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,22]],"date-time":"2026-10-22T06:22:35Z","timestamp":1792650155757,"version":"4.5.0"},"reference-count":33,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,8,25]],"date-time":"2023-08-25T00:00:00Z","timestamp":1692921600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32172476 32102275"],"award-info":[{"award-number":["32172476 32102275"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012421","name":"Agricultural Science and Technology Innovation Program","doi-asserted-by":"publisher","award":["CAAS-ZDRW202203 CAAS-ZDRW202108"],"award-info":[{"award-number":["CAAS-ZDRW202203 CAAS-ZDRW202108"]}],"id":[{"id":"10.13039\/501100012421","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Physiol."],"abstract":"\n Introduction:<\/jats:bold>\n Trichogramma<\/jats:italic>\n wasps are egg parasitoids of agricultural lepidopteran pests. The sex of\n Trichogramma<\/jats:italic>\n is determined by its ploidy as well as certain sex ratio distorters, such as the endosymbiotic bacteria\n Wolbachia<\/jats:italic>\n spp. and the paternal sex ratio (PSR) chromosome. The sex determination systems of hymenopterans, such as\n Trichogramma<\/jats:italic>\n spp., involve cascades of the genes\n transformer<\/jats:italic>\n (\n tra<\/jats:italic>\n ),\n transformer<\/jats:italic>\n -\n 2<\/jats:italic>\n (\n tra2<\/jats:italic>\n ), and\n doublesex<\/jats:italic>\n (\n dsx<\/jats:italic>\n ) and are associated with sex-specific\n tra<\/jats:italic>\n and\n dsx<\/jats:italic>\n splicing. First, these genes and their sex-specific variants must be identified to elucidate the interactions between the sex ratio disorders and the sex determination mechanism of\n Trichogramma<\/jats:italic>\n .\n <\/jats:p>\n \n Methods:<\/jats:bold>\n Here, we characterized the sex determination genes\n tra<\/jats:italic>\n ,\n tra2<\/jats:italic>\n , and\n dsx<\/jats:italic>\n in\n Trichogramma dendrolimi<\/jats:italic>\n . Sex-specific\n tra<\/jats:italic>\n and\n dsx<\/jats:italic>\n variants were detected in cDNA samples obtained from both male and female\n Trichogramma<\/jats:italic>\n wasps. They were observed in the early embryos (1\u201310\u00a0h), late embryos (12\u201320\u00a0h), larvae (32\u00a0h and 48\u00a0h), pre-pupae (96\u00a0h), and pupae (144\u00a0h, 168\u00a0h, 192\u00a0h, and 216\u00a0h) of both male and female\n T. dendrolimi<\/jats:italic>\n offspring.\n <\/jats:p>\n \n Results:<\/jats:bold>\n We detected female-specific\n tra<\/jats:italic>\n variants throughout the entire early female offspring stage. The male-specific variant began to express at 9\u201310\u00a0h as the egg was not fertilized. However, we did not find any maternally derived, female-specific\n tra<\/jats:italic>\n variant in the early male embryo. This observation suggests that the female-specific\n tra<\/jats:italic>\n variant expressed in the female embryo at 1\u20139\u00a0h may not have originated from the maternal female wasp.\n <\/jats:p>\n \n Discussion:<\/jats:bold>\n The present study might be the first to identify the sex determination genes and sex-specific gene splicing in\n Trichogramma<\/jats:italic>\n wasps. The findings of this study lay the foundation for investigating the sex determination mechanisms of\n Trichogramma<\/jats:italic>\n and other wasps. They also facilitate sex identification in immature\n T. dendrolimi<\/jats:italic>\n and the application of this important egg parasitoid in biological insect pest control programs.\n <\/jats:p>","DOI":"10.3389\/fphys.2023.1243753","type":"journal-article","created":{"date-parts":[[2023,8,25]],"date-time":"2023-08-25T07:37:36Z","timestamp":1692949056000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":8,"title":["The identification and expression pattern of the sex determination genes and their sex-specific variants in the egg parasitoid Trichogramma dendrolimi Matsumura (Hymenoptera: Trichogrammatidae)"],"prefix":"10.3389","volume":"14","author":[{"given":"Su-Fang","family":"Ning","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liang-Xiao","family":"Huo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lin","family":"Lv","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ying","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Li-Sheng","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wu-Nan","family":"Che","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hui","family":"Dong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jin-Cheng","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,8,25]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"eaau3753","DOI":"10.1126\/sciadv.aau3753","article-title":"Genetic architecture and sex-specific selection govern modular, male-biased evolution of doublesex","volume":"5","author":"Baral","year":"2019","journal-title":"Sci. Adv."},{"key":"B2","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1016\/j.semcdb.2006.12.015","article-title":"Sex determination in the haplodiploid wasp Nasonia vitripennis (Hymenoptera: chalcidoidea): A critical consideration of models and evidence","volume":"18","author":"Beukeboom","year":"2007","journal-title":"Semin. Cell. Dev. Biol."},{"key":"B3","doi-asserted-by":"publisher","first-page":"419","DOI":"10.1016\/s0092-8674(03)00606-8","article-title":"The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein","volume":"114","author":"Beye","year":"2003","journal-title":"Cell."},{"key":"B4","doi-asserted-by":"publisher","first-page":"msac145","DOI":"10.1093\/molbev\/msac145","article-title":"Evolutionary history of sexual differentiation mechanism in insects","volume":"39","author":"Chikami","year":"2022","journal-title":"Mol. Biol. Evol."},{"key":"B5","doi-asserted-by":"publisher","first-page":"eaaz9808","DOI":"10.1126\/sciadv.aaz9808","article-title":"Genome elimination mediated by gene expression from a selfish chromosome","volume":"6","author":"Dalla Benetta","year":"2020","journal-title":"Sci. Adv."},{"key":"B6","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1016\/j.ibmb.2017.09.007","article-title":"Maternal provision of transformer-2 is required for female development and embryo viability in the wasp Nasonia vitripennis","volume":"90","author":"Geuverink","year":"","journal-title":"Insect biochem. Mol. Biol."},{"key":"B7","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1111\/imb.12352","article-title":"Maternal provision of non-sex-specific transformer messenger RNA in sex determination of the wasp Asobara tabida","volume":"27","author":"Geuverink","year":"","journal-title":"Insect Mol. Biol."},{"key":"B8","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1016\/j.cois.2021.02.009","article-title":"Founder effects on sex determination systems in invasive social insects","volume":"46","author":"Hagan","year":"2021","journal-title":"Curr. Opin. Insect. Sci."},{"key":"B9","doi-asserted-by":"publisher","first-page":"519","DOI":"10.1038\/nature07052","article-title":"Evidence for the evolutionary nascence of a novel sex determination pathway in honeybees","volume":"454","author":"Hasselmann","year":"2008","journal-title":"Nature"},{"key":"B10","doi-asserted-by":"publisher","first-page":"209","DOI":"10.1146\/annurev.ento.53.103106.093441","article-title":"Sex determination in the Hymenoptera","volume":"53","author":"Heimpel","year":"2008","journal-title":"Annu. Rev. Entomol."},{"key":"B11","doi-asserted-by":"publisher","first-page":"178","DOI":"10.1038\/35012066","article-title":"Infectious parthenogenesis","volume":"405","author":"Huigens","year":"2000","journal-title":"Nature"},{"key":"B12","doi-asserted-by":"publisher","DOI":"10.7287\/peerj.preprints.27871v1","article-title":"Absence of complementary sex determination in Trichogramma dendrolimi matsumura (Hymenoptera: trichogrammatidae)","author":"Liu","year":"2019","journal-title":"PeerJ"},{"key":"B13","doi-asserted-by":"publisher","first-page":"2954","DOI":"10.1093\/gbe\/evz219","article-title":"Mapping of multiple complementary sex determination loci in a parasitoid wasp","volume":"11","author":"Matthey-Doret","year":"2019","journal-title":"Genome Biol. Evol."},{"key":"B14","doi-asserted-by":"publisher","first-page":"268","DOI":"10.1093\/molbev\/msu300","article-title":"IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies","volume":"32","author":"Nguyen","year":"2015","journal-title":"Mol. Biol. Evol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"932","DOI":"10.1038\/s41467-020-14622-4","article-title":"miRNA-1-3p is an early embryonic male sex-determining factor in the Oriental fruit fly Bactrocera dorsalis","volume":"11","author":"Peng","year":"2020","journal-title":"Nat. Commun."},{"key":"B16","doi-asserted-by":"publisher","first-page":"1054","DOI":"10.1038\/s41587-020-0508-1","article-title":"A male-biased sex-distorter gene drive for the human malaria vector Anopheles gambiae","volume":"38","author":"Simoni","year":"2020","journal-title":"Nat. Biotechnol."},{"key":"B17","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1146\/annurev.micro.53.1.71","article-title":"Wolbachia pipientis: microbial manipulator of arthropod reproduction","volume":"53","author":"Stouthamer","year":"1999","journal-title":"Annu. Rev. Microbiol."},{"key":"B18","doi-asserted-by":"publisher","first-page":"580","DOI":"10.1139\/g03-044","article-title":"The paternal sex ratio chromosome in the parasitic wasp Trichogramma kaykai condenses the paternal chromosomes into a dense chromatin mass","volume":"46","author":"van Vugt","year":"2003","journal-title":"Genome"},{"key":"B19","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1742-9994-3-1","article-title":"Single locus complementary sex determination in Hymenoptera: an \u2018unintelligent\u2019 design?","volume":"3","author":"van Wilgenburg","year":"2006","journal-title":"Front. Zool."},{"key":"B20","doi-asserted-by":"publisher","first-page":"620","DOI":"10.1126\/science.1185805","article-title":"Maternal control of haplodiploid sex determination in the wasp Nasonia","volume":"328","author":"Verhulst","year":"","journal-title":"Science"},{"key":"B21","doi-asserted-by":"publisher","first-page":"376","DOI":"10.1016\/j.gde.2010.05.001","article-title":"Insect sex determination: it all evolves around transformer","volume":"20","author":"Verhulst","year":"","journal-title":"Curr. Opin. Genet. Dev."},{"key":"B22","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1002\/bies.950170113","article-title":"Moving up the hierarchy: A hypothesis on the evolution of a genetic sex determination pathway","volume":"17","author":"Wilkins","year":"1995","journal-title":"Bioessays"},{"key":"B23","doi-asserted-by":"publisher","first-page":"463","DOI":"10.1146\/annurev-ento-060120-091620","article-title":"Biological control with Trichogramma in China: history, present status and perspectives","volume":"66","author":"Zang","year":"2020","journal-title":"Annu. Rev. Entomol."},{"key":"B24","doi-asserted-by":"publisher","first-page":"751","DOI":"10.1127\/entomologia\/2022\/1464","article-title":"Decreased Wolbachia titers cause gradual change in masculinization of intersex individuals of thelytokous Trichogramma dendrolimi","volume":"42","author":"Zhang","year":"2022","journal-title":"Entomol. Gen."},{"key":"B25","doi-asserted-by":"publisher","first-page":"348","DOI":"10.1111\/1755-0998.13096","article-title":"PhyloSuite: an integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies","volume":"20","author":"Zhang","year":"","journal-title":"Mol. Ecol. Resour."},{"key":"B26","doi-asserted-by":"publisher","first-page":"875","DOI":"10.1016\/j.cell.2020.09.043","article-title":"Genomes of the banyan tree and pollinator wasp provide insights into fig-wasp coevolution","volume":"183","author":"Zhang","year":"","journal-title":"Cell."},{"key":"B27","doi-asserted-by":"publisher","first-page":"742","DOI":"10.1016\/j.aspen.2019.06.001","article-title":"Effect of wind time on the dispersal capacity of Trichogramma dendrolimi Matsumura (Hymenoptera Trichogrammatidae)","volume":"22","author":"Zhou","year":"","journal-title":"J. Asia Pac. Entomol."},{"key":"B28","doi-asserted-by":"publisher","first-page":"18114","DOI":"10.1038\/s41598-019-54719-5","article-title":"Effects of temperature and superparasitism on quality and characteristics of thelytokous Wolbachia-infected Trichogramma dendrolimi Matsumura (Hymenoptera: trichogrammatidae) during mass rearing","volume":"9","author":"Zhou","year":"","journal-title":"Sci. Rep."},{"key":"B29","doi-asserted-by":"publisher","first-page":"2635","DOI":"10.1002\/ps.5805","article-title":"Optimal clutch size for quality control of bisexual and Wolbachia-infected thelytokous lines of Trichogramma dendrolimi Matsumura (Hymenoptera: trichogrammatidae) mass reared on eggs of a substitutive host, Antheraea pernyi Gu\u00e9rin-M\u00e9neville (Lepidoptera: saturniidae)","volume":"76","author":"Zhou","year":"2020","journal-title":"Pest Manag. Sci."},{"key":"B30","doi-asserted-by":"publisher","first-page":"1005","DOI":"10.1002\/ps.7269","article-title":"Wolbachia-infected Trichogramma dendrolimi is outcompeted by its uninfected counterpart in superparasitism but does not have developmental delay","volume":"79","author":"Zhou","year":"2023","journal-title":"Pest Manag. Sci."},{"key":"B31","doi-asserted-by":"publisher","first-page":"3080","DOI":"10.1002\/ps.6934","article-title":"Penetrance during Wolbachia-mediated parthenogenesis of Trichogramma wasps is reduced by continuous oviposition, associated with exhaustion of Wolbachia titers in ovary and offspring eggs","volume":"78","author":"Zhou","year":"","journal-title":"Pest Manag. Sci."},{"key":"B32","doi-asserted-by":"publisher","first-page":"e0236222","DOI":"10.1128\/mbio.02362-22","article-title":"Wolbachia-driven memory loss in a parasitic wasp increases superparasitism to enhance horizontal transmission","volume":"13","author":"Zhou","year":"","journal-title":"mBio"},{"key":"B33","doi-asserted-by":"publisher","first-page":"1115","DOI":"10.1126\/science.abb8949","article-title":"A chimeric gene paternally instructs female sex determination in the haplodiploid wasp Nasonia","volume":"370","author":"Zou","year":"2020","journal-title":"Science"}],"container-title":["Frontiers in Physiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fphys.2023.1243753\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,8,25]],"date-time":"2023-08-25T07:37:45Z","timestamp":1692949065000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fphys.2023.1243753\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,8,25]]},"references-count":33,"alternative-id":["10.3389\/fphys.2023.1243753"],"URL":"https:\/\/doi.org\/10.3389\/fphys.2023.1243753","relation":{},"ISSN":["1664-042X"],"issn-type":[{"value":"1664-042X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,8,25]]},"article-number":"1243753"}}