{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,25]],"date-time":"2026-09-25T17:14:08Z","timestamp":1790356448445,"version":"4.1.0"},"reference-count":65,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2026,1,26]],"date-time":"2026-01-26T00:00:00Z","timestamp":1769385600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"State Key Laboratory of Mariculture Biobreeding and Sustainable Goods","award":["BRESG202303"],"award-info":[{"award-number":["BRESG202303"]}]},{"name":"Shandong Key R&D Program","award":["2023ZLYS02"],"award-info":[{"award-number":["2023ZLYS02"]}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32230107"],"award-info":[{"award-number":["32230107"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100007129","name":"Natural Science Foundation of Shandong Province","doi-asserted-by":"publisher","award":["ZR2022QC037"],"award-info":[{"award-number":["ZR2022QC037"]}],"id":[{"id":"10.13039\/501100007129","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>The wnt gene family encodes a group of highly conserved secreted glycoproteins that play essential roles in vertebrate development, including tissue patterning, cell differentiation, and gonadal regulation. However, the genomic organization, evolutionary dynamics, and functional roles of Wnt signaling components in flatfish remain poorly understood. In this study, we performed a comprehensive genome-wide identification, evolutionary characterization, expression profiling, and functional analysis of wnt genes in Cynoglossus semilaevis, a flatfish species exhibiting ZW\/ZZ sex determination and temperature-induced sex reversal. A total of 20 wnt genes were identified and classified into 13 subfamilies, displaying conserved structural organization and phylogenetic relationships consistent with other teleosts. Chromosomal mapping revealed lineage-specific WNT clusters, including a unique wnt3\u2013wnt7b\u2013wnt5b\u2013wnt16 block, as well as syntenic associations with reproduction-related genes (e.g., adipor2, sema3a, nape-pld, erc2, lamb2), suggesting coordinated genomic regulation. Tissue transcriptome analysis demonstrated strong sex- and tissue-biased expression patterns, with wnt5a predominantly expressed in ovaries and wnt5b specifically upregulated in pseudo-male testes. Functional assays revealed that knockdown of wnt5a or wnt5b induced testis-specific genes (sox9b, tesk1) and suppressed ovarian markers (foxl2, cyp19a1a), indicating antagonistic regulatory roles in gonadal fate determination. Promoter analysis identified yy1a as a selective repressor of wnt5b, but not wnt5a, providing a mechanistic basis for paralog divergence. Furthermore, pull-down combined with LC\u2013MS\/MS analysis showed that WNT5b interacts with proteins enriched in ribosome biogenesis and ubiquitin-mediated proteolysis, suggesting a role in translational regulation and protein turnover during spermatogenesis. Together, these findings establish WNT5 signaling\u2014particularly wnt5b\u2014as a key driver of testicular development in C. semilaevis and provide new insights into the molecular mechanisms underlying sex differentiation and sex reversal in flatfish.<\/jats:p>","DOI":"10.3390\/ani16030387","type":"journal-article","created":{"date-parts":[[2026,1,26]],"date-time":"2026-01-26T15:48:30Z","timestamp":1769442510000},"page":"387","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Genome-Wide Characterization of the wnt Gene Family Reveals a wnt5b-Mediated Regulatory Mechanism of Testicular Development in Cynoglossus semilaevis"],"prefix":"10.3390","volume":"16","author":[{"given":"Zhengjie","family":"Li","sequence":"first","affiliation":[{"name":"School of Marine Science and Engineering, Qingdao Agricultural University, Qingdao 266109, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Junhao","family":"Wang","sequence":"additional","affiliation":[{"name":"School of Marine Science and Engineering, Qingdao Agricultural University, Qingdao 266109, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chao","family":"Li","sequence":"additional","affiliation":[{"name":"School of Marine Science and Engineering, Qingdao Agricultural University, Qingdao 266109, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0000-5518-8512","authenticated-orcid":false,"given":"Ying","family":"Zhu","sequence":"additional","affiliation":[{"name":"School of Marine Science and Engineering, Qingdao Agricultural University, Qingdao 266109, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,1,26]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"3286","DOI":"10.1101\/gad.11.24.3286","article-title":"Wnt signaling: A common theme in animal development","volume":"11","author":"Cadigan","year":"1997","journal-title":"Genes Dev."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1016\/S0168-9525(01)02349-6","article-title":"An ancient cluster of Wnt paralogues","volume":"17","author":"Nusse","year":"2001","journal-title":"TRENDS Genet."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1007\/s004270050025","article-title":"Three Wnt genes expressed in a wide variety of tissues during development of the zebrafish, Danio rerio: Developmental and evolutionary perspectives","volume":"206","author":"Blader","year":"1996","journal-title":"Dev. Genes Evol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1016\/j.fsi.2018.03.034","article-title":"Wnt gene family members and their expression profiling in Litopenaeus vannamei","volume":"77","author":"Du","year":"2018","journal-title":"Fish Shellfish. Immunol."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Fu, Y., He, J., Liu, L., Huang, X., Xu, Y., and Wang, C. (2022). Comprehensive genome-wide analysis of Wnt gene family and expression profiling during limb regeneration in Portunus trituberculatus. Fishes, 7.","DOI":"10.3390\/fishes7050258"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1624","DOI":"10.1016\/j.cub.2008.09.057","article-title":"Multiple Wnt genes are required for segmentation in the short-germ embryo of Tribolium castaneum","volume":"18","author":"Bolognesi","year":"2008","journal-title":"Curr. Biol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1126\/science.1222879","article-title":"Structural Basis of Wnt Recognition by Frizzled","volume":"337","author":"Janda","year":"2012","journal-title":"Science"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1186\/s12964-024-01704-9","article-title":"Inhibition of WNT\/\u03b2-catenin signalling during sex-specific gonadal differentiation is essential for normal human fetal testis development","volume":"22","author":"Riis","year":"2024","journal-title":"Cell Commun. Signal."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Song, Z., Wang, F., Yang, C., Guo, Y., Li, J., Huang, R., Ling, H., Cheng, G., Chen, Z., and Zhu, Z. (2025). Meta-Analysis of Multi-Center Transcriptomic Profiles and Machine Learning Reveal Phospholipase C\u03b24 as a Wnt\/Ca2\u207a Signaling Mediator in Glioblastoma Immunotherapy. Front. Immunol., 16.","DOI":"10.3389\/fimmu.2025.1610683"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Shi, D.-L. (2024). Canonical and non-canonical Wnt signaling generates molecular and cellular asymmetries to establish embryonic axes. J. Dev. Biol., 12.","DOI":"10.3390\/jdb12030020"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"e2421772122","DOI":"10.1073\/pnas.2421772122","article-title":"Double assurance in the induction of axial development by egg dorsal determinants in Xenopus embryos","volume":"122","author":"Azbazdar","year":"2025","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"RP104164","DOI":"10.7554\/eLife.104164.3","article-title":"Drosophila hamlet mediates epithelial tissue assembly of the reproductive system","volume":"13","author":"Wang","year":"2025","journal-title":"eLife"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1016\/j.ygeno.2018.11.006","article-title":"A comparative transcriptomic study on developmental gonads provides novel insights into sex change in the protandrous black porgy (Acanthopagrus schlegelii)","volume":"111","author":"Zhang","year":"2019","journal-title":"Genomics"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1055\/s-0032-1324722","article-title":"WNT4, RSPO1, and FOXL2 in sex development","volume":"30","year":"2012","journal-title":"Semin. Reprod. Med."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"152684","DOI":"10.1016\/j.bbrc.2025.152684","article-title":"Systematic analysis of Wnt family genes reveals the potential role of Wnt4 in driving female differentiation in Spotted knifejaw","volume":"785","author":"Zhao","year":"2025","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1530\/JOE-16-0104","article-title":"Expression of wnt4\/5 during reproductive cycle of catfish and wnt5 promoter analysis","volume":"232","author":"Prathibha","year":"2017","journal-title":"J. Endocrinol."},{"key":"ref_17","unstructured":"Najafabadi, A.A. (2026, January 18). Elucidation of the Biological Roles of Wnt5a Signaling in Follicle Development. Available online: http:\/\/hdl.handle.net\/1866\/13371."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1530\/JOE-18-0447","article-title":"Fsh stimulates Leydig cell Wnt5a production, enriching zebrafish type A spermatogonia","volume":"239","author":"Safian","year":"2018","journal-title":"J. Endocrinol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1095\/biolreprod.112.105809","article-title":"Regulated Wnt\/beta-catenin signaling sustains adult spermatogenesis in mice","volume":"90","author":"Kerr","year":"2014","journal-title":"Biol. Reprod."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1007\/s10142-018-0595-y","article-title":"Transcriptomics analysis revealing candidate networks and genes for the body size sexual dimorphism of Chinese tongue sole (Cynoglossus semilaevis)","volume":"18","author":"Wang","year":"2018","journal-title":"Funct. Integr. Genom."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"781","DOI":"10.1146\/annurev.cellbio.20.010403.113126","article-title":"The Wnt signaling pathway in development and disease","volume":"20","author":"Logan","year":"2004","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"a007922","DOI":"10.1101\/cshperspect.a007922","article-title":"The evolution of the Wnt pathway","volume":"4","author":"Holstein","year":"2012","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1016\/S0168-9525(97)01093-7","article-title":"WNTs modulate cell fate and behavior during vertebrate development","volume":"13","author":"Moon","year":"1997","journal-title":"Trends Genet."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1016\/S0925-4773(98)00013-6","article-title":"Zebrafish wnt11: Pattern and regulation of the expression by the yolk cell and No tail activity","volume":"71","author":"Makita","year":"1998","journal-title":"Mech. Dev."},{"key":"ref_25","first-page":"879","article-title":"Comparative genomics on WNT11 gene","volume":"15","author":"Katoh","year":"2005","journal-title":"Int. J. Mol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"741258","DOI":"10.1016\/j.aquaculture.2024.741258","article-title":"Transcriptomic analysis of gonads in Malabar red snapper (Lutjanus malabaricus) reveals genes associated with gonad development","volume":"592","author":"Liang","year":"2024","journal-title":"Aquaculture"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"434","DOI":"10.1007\/s12032-025-02950-8","article-title":"Evolutionary conservation and cancer implications of the WNT signaling pathway","volume":"42","author":"Prajapati","year":"2025","journal-title":"Med. Oncol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1645","DOI":"10.1093\/molbev\/msq052","article-title":"Evolutionary dynamics of the wnt gene family: A lophotrochozoan perspective","volume":"27","author":"Cho","year":"2010","journal-title":"Mol. Biol. Evol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"610","DOI":"10.1242\/jeb.02056","article-title":"Asymmetric craniofacial remodeling and lateralized behavior in larval flatfish","volume":"209","author":"Schreiber","year":"2006","journal-title":"J. Exp. Biol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/S0925-4773(01)00416-6","article-title":"Antagonistic regulation of convergent extension movements in Xenopus by Wnt\/\u03b2-catenin and Wnt\/Ca2+ signaling","volume":"106","author":"Geis","year":"2001","journal-title":"Mech. Dev."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"856","DOI":"10.1038\/35101621","article-title":"Frizzled-7 signalling controls tissue separation during Xenopus gastrulation","volume":"413","author":"Winklbauer","year":"2001","journal-title":"Nature"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"18588","DOI":"10.1002\/jcb.29217","article-title":"Roles of Wnt7a in embryo development, tissue homeostasis, and human diseases","volume":"120","author":"Lan","year":"2019","journal-title":"J. Cell. Biochem."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1038\/nature07564","article-title":"WNT11 acts as a directional cue to organize the elongation of early muscle fibres","volume":"457","author":"Gros","year":"2009","journal-title":"Nature"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"220235","DOI":"10.1098\/rsob.220235","article-title":"The genetic basis and potential molecular mechanism of yellow-albino northern snakehead (Channa argus)","volume":"13","author":"Sun","year":"2023","journal-title":"Open Biol."},{"key":"ref_35","first-page":"579","article-title":"Wnt3-Wnt14B and Wnt3A-Wnt14 gene clusters","volume":"9","author":"Katoh","year":"2002","journal-title":"Int. J. Mol. Med."},{"key":"ref_36","first-page":"947","article-title":"Molecular cloning and characterization of WNT14B, a novel member of the WNT gene family","volume":"19","author":"Kirikoshi","year":"2001","journal-title":"Int. J. Oncol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"e11148","DOI":"10.1002\/ece3.11148","article-title":"The spotted parrotfish genome provides insights into the evolution of a coral reef dietary specialist (Teleostei: Labridae: Scarini: Cetoscarus ocellatus)","volume":"14","author":"Tea","year":"2024","journal-title":"Ecol. Evol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1155","DOI":"10.1007\/s10126-024-10363-3","article-title":"Exploitation and application of a new genetic sex marker based on intron insertion variation of erc2 gene in Oplegnathus punctatus","volume":"26","author":"Xu","year":"2024","journal-title":"Mar. Biotechnol."},{"key":"ref_39","unstructured":"Fogg, L.G., Policarpo, M., and Salzburger, W. (2025). Evolutionary dynamics of the vertebrate Wnt gene repertoire. bioRxiv."},{"key":"ref_40","first-page":"1249","article-title":"Census of vertebrate Wnt genes: Isolation and developmental expression of Xenopus Wnt2, Wnt3, Wnt9a, Wnt9b, Wnt10a, and Wnt16","volume":"236","author":"Garriock","year":"2007","journal-title":"Dev. Dyn. Off. Publ. Am. Assoc. Anat."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"131892","DOI":"10.1016\/j.ijbiomac.2024.131892","article-title":"Multi-omics analysis identifies sex-specific hepatic protein-metabolite networks in yellow catfish (Pelteobagrus fulvidraco) exposed to chronic hypoxia","volume":"268","author":"Zhao","year":"2024","journal-title":"Int. J. Biol. Macromol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"E475","DOI":"10.1152\/ajpendo.00086.2012","article-title":"Anandamide regulates the expression of GnRH1, GnRH2, and GnRH-Rs in frog testis","volume":"303","author":"Chianese","year":"2012","journal-title":"Am. J. Physiol.-Endocrinol. Metab."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"5052","DOI":"10.1210\/en.2007-1799","article-title":"Expression of the endocannabinoid system in human first trimester placenta and its role in trophoblast proliferation","volume":"149","author":"Habayeb","year":"2008","journal-title":"Endocrinology"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1159\/000334515","article-title":"Expression profiling of Wnt signaling genes during gonadal differentiation and gametogenesis in rainbow trout","volume":"5","author":"Nicol","year":"2012","journal-title":"Sex. Dev."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1046\/j.1440-169X.2003.00674.x","article-title":"Cloning and embryonic expression of six wnt genes in the medaka (Oryzias latipes) with special reference to expression of wnt5a in the pectoral fin buds","volume":"45","author":"Yokoi","year":"2003","journal-title":"Dev. Growth Differ."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Zanardini, M., and Habibi, H.R. (2025). The Role of Neurohypophysial Hormones in the Endocrine and Paracrine Control of Gametogenesis in Fish. Cells, 14.","DOI":"10.3390\/cells14141061"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1095\/biolreprod.111.095232","article-title":"Loss of Wnt5a disrupts primordial germ cell migration and male sexual development in mice","volume":"86","author":"Chawengsaksophak","year":"2012","journal-title":"Biol. Reprod."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"2937","DOI":"10.1111\/are.15809","article-title":"Characterization and expression pattern of Wnt5b gene in Pelodiscus sinensis","volume":"53","author":"Chen","year":"2022","journal-title":"Aqua C. Res."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/j.theriogenology.2020.11.014","article-title":"Interactive role of Wnt signaling and Zn in regulating testicular function of the common carp, Cyprinus carpio","volume":"161","author":"Deepa","year":"2021","journal-title":"Theriogenol"},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Guo, H., Wei, M., Liu, Y., Zhu, Y., Xu, W., Meng, L., Wang, N., Shao, C., Lu, S., and Gao, F. (2017). Molecular cloning and expression analysis of the aqp1aa gene in half-smooth tongue sole (Cynoglossus semilaevis). PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0175033"},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Meng, L., Zhu, Y., Zhang, N., Liu, W., Liu, Y., Shao, C., Wang, N., and Chen, S. (2014). Cloning and characterization of tesk1, a novel spermatogenesis-related gene, in the tongue sole (Cynoglossus semilaevis). PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0107922"},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Li, X., Li, L., Cui, Z., Li, M., and Xu, W. (2023). Phosphoproteomics reveal new candidates in abnormal spermatogenesis of pseudomales in Cynoglossus semilaevis. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms241411430"},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Tao, W., Chen, J., Tan, D., Yang, J., Sun, L., Wei, J., Conte, M.A., Kocher, T.D., and Wang, D. (2018). Transcriptome display during tilapia sex determination and differentiation as revealed by RNA-Seq analysis. BMC Genom., 19.","DOI":"10.1186\/s12864-018-4756-0"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"86","DOI":"10.2108\/zs160070","article-title":"Sex reversal and analyses of possible involvement of sex steroids in scallop gonadal development in newly established organ-culture systems","volume":"34","author":"Otani","year":"2017","journal-title":"Zool. Sci."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1080\/19768354.2009.9647240","article-title":"Sex-and tissue-related expression of two types of p450 aromatase mRNA in the protandrous black porgy, Acanthopagrus schlegeli, during sex reversal: Expression profiles following exogenous hormone administration","volume":"13","author":"Min","year":"2009","journal-title":"Anim. Cells Syst."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"417","DOI":"10.2108\/zsj.21.417","article-title":"Characterization of two types of cytochrome P450 aromatase in the serial-sex changing gobiid fish, Trimma okinawae","volume":"21","author":"Kobayashi","year":"2004","journal-title":"Zool. Sci."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1007\/s00438-021-01840-8","article-title":"Localization and regulatory function of Yin Yang 1 (YY1) in chicken testis","volume":"297","author":"Chen","year":"2022","journal-title":"Mol. Genet. Genom."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"249","DOI":"10.12717\/DR.2020.24.4.249","article-title":"YY1 and CP2c in unidirectional spermatogenesis and stemness","volume":"24","author":"Cheon","year":"2020","journal-title":"Dev. Reprod."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"R39","DOI":"10.1530\/REP-23-0065","article-title":"Molecular functions of Mrhl lncRNA in mouse spermatogenesis","volume":"166","author":"Kayyar","year":"2023","journal-title":"Reproduction"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"127201","DOI":"10.1016\/j.ijbiomac.2023.127201","article-title":"Genome-wide analysis of BMP\/GDF family and DAP-seq of YY1 suggest their roles in Cynoglossus semilaevis sexual size dimorphism","volume":"253","author":"Shi","year":"2023","journal-title":"Int. J. Biol. Macromol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"111844","DOI":"10.1016\/j.cbpa.2025.111844","article-title":"Comprehensive identification and characterization of ribosomal protein genes in the Pacific oyster (Crassostrea gigas): Potential roles in reproduction and development","volume":"304","author":"Zhang","year":"2025","journal-title":"Comp. Biochem. Physiol. Part A Mol. Integr. Physiol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1038\/s41586-022-05508-0","article-title":"A male germ-cell-specific ribosome controls male fertility","volume":"612","author":"Li","year":"2022","journal-title":"Nature"},{"key":"ref_63","doi-asserted-by":"crossref","unstructured":"Mercer, M., Jang, S., Ni, C., and Buszczak, M. (2021). The dynamic regulation of mRNA translation and ribosome biogenesis during germ cell development and reproductive aging. Front. Cell Dev. Biol., 9.","DOI":"10.3389\/fcell.2021.710186"},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Zheng, W., Xu, H., Lam, S.H., Luo, H., Karuturi, R.K.M., and Gong, Z. (2013). Transcriptomic analyses of sexual dimorphism of the zebrafish liver and the effect of sex hormones. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0053562"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"480","DOI":"10.1016\/j.ydbio.2005.03.034","article-title":"Testicular expression of small ubiquitin-related modifier-1 (SUMO-1) supports multiple roles in spermatogenesis: Silencing of sex chromosomes in spermatocytes, spermatid microtubule nucleation, and nuclear reshaping","volume":"282","author":"Vigodner","year":"2005","journal-title":"Dev. Biol."}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/16\/3\/387\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,1,26]],"date-time":"2026-01-26T16:02:06Z","timestamp":1769443326000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/16\/3\/387"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,1,26]]},"references-count":65,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2026,2]]}},"alternative-id":["ani16030387"],"URL":"https:\/\/doi.org\/10.3390\/ani16030387","relation":{},"ISSN":["2076-2615"],"issn-type":[{"value":"2076-2615","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,1,26]]}}}