{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,2]],"date-time":"2026-10-02T08:05:17Z","timestamp":1790928317681,"version":"4.1.0"},"reference-count":51,"publisher":"MDPI AG","issue":"18","license":[{"start":{"date-parts":[[2022,9,18]],"date-time":"2022-09-18T00:00:00Z","timestamp":1663459200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"China Agriculture Research System","award":["CARS-47-G06"],"award-info":[{"award-number":["CARS-47-G06"]}]},{"name":"National Marine Genetic Resource Center, China","award":["CARS-47-G06"],"award-info":[{"award-number":["CARS-47-G06"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>As lower vertebrates, teleost species could be affected by dynamic aquatic environments and may respond to environmental changes through the hypothalamus\u2013pituitary\u2013gonad (HPG) axis to ensure their normal growth and sexual development. Chinese sea bass (Lateolabrax maculatus), euryhaline marine teleosts, have an extraordinary ability to deal with a wide range of salinity changes, whereas the salinity decrease during their sex-maturation season may interfere with the HPG axis and affect their steroid hormone metabolism, resulting in abnormal reproductive functioning. To this end, in this study, 40 HPG axis genes in the L. maculatus genome were systematically characterized and their copy numbers, phylogenies, gene structures, and expression patterns were investigated, revealing the conservation of the HPG axis among teleost lineages. In addition, freshwater acclimation was carried out with maturing male L. maculatus, and their serum cortisol and 11-ketotestosterone (11-KT) levels were both increased significantly after the salinity change, while their testes were found to be partially degraded. After salinity reduction, the expression of genes involved in cortisol and 11-KT synthesis (cyp17a, hsd3b1, cyp21a, cyp11c, hsd11b2, and hsd17b3) showed generally upregulated expression in the head kidneys and testes, respectively. Moreover, cyp11c and hsd11b2 were involved in the synthesis and metabolism of both cortisol and 11-KT, and after salinity change their putative interaction may contribute to steroid hormone homeostasis. Our results proved the effects of salinity change on the HPG axis and steroidogenic pathway in L. maculatus and revealed the gene interactions involved in the regulation of steroid hormone levels. The coordinated interaction of steroidogenic genes provides comprehensive insights into steroidogenic pathway regulation, as well as sexual development, in teleost species.<\/jats:p>","DOI":"10.3390\/ijms231810905","type":"journal-article","created":{"date-parts":[[2022,9,18]],"date-time":"2022-09-18T23:39:22Z","timestamp":1663544362000},"page":"10905","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":20,"title":["Steroidogenic Effects of Salinity Change on the Hypothalamus\u2013Pituitary\u2013Gonad (HPG) Axis of Male Chinese Sea Bass (Lateolabrax maculatus)"],"prefix":"10.3390","volume":"23","author":[{"given":"Zhenru","family":"Fang","sequence":"first","affiliation":[{"name":"Key Laboratory of Marine Genetics and Breeding (Ocean University of China), Ministry of Education, 5 Yushan Road, Qingdao 266003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xujian","family":"Li","sequence":"additional","affiliation":[{"name":"Key Laboratory of Marine Genetics and Breeding (Ocean University of China), Ministry of Education, 5 Yushan Road, Qingdao 266003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yapeng","family":"Wang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Marine Genetics and Breeding (Ocean University of China), Ministry of Education, 5 Yushan Road, Qingdao 266003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wei","family":"Lu","sequence":"additional","affiliation":[{"name":"Key Laboratory of Marine Genetics and Breeding (Ocean University of China), Ministry of Education, 5 Yushan Road, Qingdao 266003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Juncheng","family":"Hou","sequence":"additional","affiliation":[{"name":"Key Laboratory of Marine Genetics and Breeding (Ocean University of China), Ministry of Education, 5 Yushan Road, Qingdao 266003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8835-3171","authenticated-orcid":false,"given":"Jie","family":"Cheng","sequence":"additional","affiliation":[{"name":"Key Laboratory of Marine Genetics and Breeding (Ocean University of China), Ministry of Education, 5 Yushan Road, Qingdao 266003, China"},{"name":"Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao), 1 Wenhai Road, Qingdao 266237, China"},{"name":"Key Laboratory of Tropical Aquatic Germplasm of Hainan Province, Sanya Oceanographic Institution, Ocean University of China, Sanya 572024, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,9,18]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"607","DOI":"10.1111\/jfb.14439","article-title":"From gametogenesis to spawning: How climate-driven warming affects teleost reproductive biology","volume":"97","author":"Alix","year":"2020","journal-title":"J. Fish Biol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2142","DOI":"10.1111\/raq.12563","article-title":"Testicular development and spermatogenesis in fish: Insights into molecular aspects and regulation of gene expression by different exogenous factors","volume":"13","author":"Bhat","year":"2021","journal-title":"Rev. Aquac."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"113439","DOI":"10.1016\/j.ygcen.2020.113439","article-title":"Climate change impacts on fish reproduction are mediated at multiple levels of the brain-pituitary-gonad axis","volume":"291","author":"Servili","year":"2020","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1016\/j.steroids.2015.06.011","article-title":"Steroids in teleost fishes: A functional point of view","volume":"103","author":"Tokarz","year":"2015","journal-title":"Steroids"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"803","DOI":"10.1007\/s10695-019-00752-0","article-title":"Steroidogenesis and its regulation in teleost\u2014A review","volume":"46","author":"Rajakumar","year":"2020","journal-title":"Fish Physiol. Biochem."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"113322","DOI":"10.1016\/j.ygcen.2019.113322","article-title":"Hypothalamic- and pituitary-derived growth and reproductive hormones and the control of energy balance in fish","volume":"287","author":"Blanco","year":"2020","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"322","DOI":"10.1016\/j.yfrne.2010.04.002","article-title":"GnRH signaling, the gonadotrope and endocrine control of fertility","volume":"31","author":"Bliss","year":"2010","journal-title":"Front. Neuroendocrinol."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Cheng, J., Yang, F., Liu, S., Zhao, H., Lu, W., and Zhang, Q. (2022). Transcriptomic Analysis Reveals Functional Interaction of mRNA-lncRNA-miRNA in Steroidogenesis and Spermatogenesis of Gynogenetic Japanese Flounder (Paralichthys olivaceus). Biology, 11.","DOI":"10.3390\/biology11020213"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Yang, F., Wang, Y., Lu, W., Zong, W., Zhu, Q., and Cheng, J. (2022). The comparative survey of coordinated regulation of steroidogenic pathway in Japanese flounder (Paralichthys olivaceus) and Chinese tongue sole (Cynoglossus Semilaevis). Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23105520"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1677\/joe.0.1640247","article-title":"The role of the StAR protein in steroidogenesis: Challenges for the future","volume":"164","author":"Stocco","year":"2000","journal-title":"J. Endocrinol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1016\/j.aaf.2020.09.004","article-title":"Development and organization of gonadal steroidogenesis in bony fishes\u2014A review","volume":"6","author":"Tenugu","year":"2021","journal-title":"Aquac. Fish."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Goldstone, J.V., McArthur, A.G., Kubota, A., Zanette, J., Parente, T., J\u00f6nsson, M.E., Nelson, D.R., and Stegeman, J.J. (2010). Identification and developmental expression of the full complement of Cytochrome P450 genes in Zebrafish. BMC Genom., 11.","DOI":"10.1186\/1471-2164-11-643"},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Liang, D., Fan, Z., Zou, Y., Tan, X., Wu, Z., Jiao, S., Li, J., Zhang, P., and You, F. (2018). Characteristics of Cyp11a during Gonad Differentiation of the Olive Flounder Paralichthys olivaceus. Int. J. Mol. Sci., 19.","DOI":"10.3390\/ijms19092641"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1016\/j.cbpb.2014.07.007","article-title":"Expression analysis of cyp11a1 during gonadal development, recrudescence and after hCG induction and sex steroid analog treatment in the catfish (Clarias batrachus)","volume":"176","author":"Rajakumar","year":"2014","journal-title":"Comp. Biochem. Physiol. Part B Biochem. Mol. Biol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1530\/JOE-19-0438","article-title":"Loss of Cyp11c1 causes delayed spermatogenesis due to the absence of 11-ketotestosterone","volume":"244","author":"Zheng","year":"2020","journal-title":"J. Endocrinol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1016\/j.bbrc.2007.08.044","article-title":"Characterization, expression and transcriptional regulation of P450c17-I and -II in the medaka (Oryzias latipes)","volume":"362","author":"Zhou","year":"2007","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"4282","DOI":"10.1210\/en.2007-0487","article-title":"A novel type of P450c17 lacking the lyase activity is responsible for C21-steroid biosynthesis in the fish ovary and head kidney","volume":"148","author":"Zhou","year":"2007","journal-title":"Endocrinology"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"2268","DOI":"10.1093\/molbev\/mst124","article-title":"Expression and sequence evolution of aromatase cyp19a1 and other sexual development genes in East African cichlid fishes","volume":"30","author":"Heule","year":"2013","journal-title":"Mol. Biol. Evol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"352","DOI":"10.1016\/j.ygcen.2009.03.002","article-title":"Ovarian aromatase and estrogens: A pivotal role for gonadal sex differentiation and sex change in fish","volume":"165","author":"Guiguen","year":"2010","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"161","DOI":"10.3389\/fgene.2020.00161","article-title":"Beta-Hydroxysteroid Dehydrogenase Genes in Orange-Spotted Grouper (Epinephelus coioides): Genome-Wide Identification and Expression Analysis during Sex Reversal","volume":"11","author":"Xiao","year":"2020","journal-title":"Front. Genet."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"17926","DOI":"10.3390\/ijms140917926","article-title":"Regulation of 3\u03b2-hydroxysteroid dehydrogenase\/\u0394\u2075-\u0394\u2074 isomerase: A review","volume":"14","author":"Rasmussen","year":"2013","journal-title":"Int. J. Mol. Sci."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.jsbmb.2010.02.014","article-title":"Cloning, expression and enzyme activity analysis of testicular 11beta-hydroxysteroid dehydrogenase during seasonal cycle and after hCG induction in air-breathing catfish (Clarias gariepinus)","volume":"120","author":"Rasheeda","year":"2010","journal-title":"J. Steroid Biochem. Mol. Biol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0303-7207(00)00383-X","article-title":"A guide to 17\u03b2-hydroxysteroid dehydrogenases","volume":"171","author":"Adamski","year":"2001","journal-title":"Mol. Cell. Endocrinol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1016\/j.mce.2003.12.006","article-title":"The role of 17 beta-hydroxysteroid dehydrogenases","volume":"218","author":"Mindnich","year":"2004","journal-title":"Mol. Cell. Endocrinol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1677\/jme.1.01801","article-title":"Cloning, expression and characterization of three types of 17beta-hydroxysteroid dehydrogenases from the Nile tilapia, Oreochromis niloticus","volume":"35","author":"Zhou","year":"2005","journal-title":"J. Mol. Endocrinol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1002\/jez.2350","article-title":"The cellular stress response in fish exposed to salinity fluctuations","volume":"333","author":"Evans","year":"2020","journal-title":"J. Exp. Zool. Part A Ecol. Integr. Physiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1907","DOI":"10.1242\/jeb.118695","article-title":"Physiological mechanisms used by fish to cope with salinity stress","volume":"218","year":"2015","journal-title":"J. Exp. Biol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.theriogenology.2019.03.013","article-title":"Influence of salinity on spermatogenesis in adult Nile tilapia (Oreochromis niloticus) testis","volume":"131","author":"Vieira","year":"2019","journal-title":"Theriogenology"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Li, X., Liu, S., Wang, Y., Lu, W., Zhang, Q., and Cheng, J. (2022). Genomic and transcriptomic landscape and evolutionary dynamics of heat shock proteins in spotted sea bass (Lateolabrax maculatus) under salinity change and alkalinity stress. Biology, 11.","DOI":"10.3390\/biology11030353"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Zhang, X., Wen, H., Wang, H., Ren, Y., Zhao, J., and Li, Y. (2017). RNA-Seq analysis of salinity stress-responsive transcriptome in the liver of spotted sea bass (Lateolabrax maculatus). PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0173238"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"3517","DOI":"10.1111\/are.13817","article-title":"Blood physiological responses and steroidogenetic effects of decreasing salinity on maturing male spotted sea bass (Lateolabrax maculatus)","volume":"49","author":"Chi","year":"2018","journal-title":"Aquac. Res."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1093\/genetics\/154.1.459","article-title":"The probability of duplicate gene preservation by subfunctionalization","volume":"154","author":"Lynch","year":"2000","journal-title":"Genetics"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"542","DOI":"10.1093\/oxfordjournals.molbev.a003833","article-title":"Two Cyp19 (P450 aromatase) genes on duplicated zebrafish chromosomes are expressed in ovary or brain","volume":"18","author":"Chiang","year":"2001","journal-title":"Mol. Biol. Evol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1016\/j.ygcen.2017.06.026","article-title":"Estrogen-regulated expression of cyp19a1a and cyp19a1b genes in swim-up fry of Labeo rohita","volume":"251","author":"Gupta","year":"2017","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"105974","DOI":"10.1016\/j.jsbmb.2021.105974","article-title":"The role of StAR2 gene in testicular differentiation and spermatogenesis in Nile tilapia (Oreochromis niloticus)","volume":"214","author":"Li","year":"2021","journal-title":"J. Steroid Biochem. Mol. Biol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1016\/j.mce.2014.05.013","article-title":"Characterization of two paralogous StAR genes in a teleost, Nile tilapia (Oreochromis niloticus)","volume":"392","author":"Yu","year":"2014","journal-title":"Mol. Cell. Endocrinol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"110822","DOI":"10.1016\/j.mce.2020.110822","article-title":"Substrate multispecificity among 20\u03b2-hydroxysteroid dehydrogenase type 2 members","volume":"510","author":"Tokarz","year":"2020","journal-title":"Mol. Cell. Endocrinol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1387\/ijdb.200072jf","article-title":"Stress and sex determination in fish: From brain to gonads","volume":"65","author":"Fernandino","year":"2021","journal-title":"Int. J. Dev. Biol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"R149","DOI":"10.1530\/REP-17-0408","article-title":"Stress and sex: Does cortisol mediate sex change in fish?","volume":"154","author":"Goikoetxea","year":"2017","journal-title":"Reproduction"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1496","DOI":"10.1111\/jfb.14599","article-title":"Temperature increase and its effects on fish stress physiology in the context of global warming","volume":"98","author":"Alfonso","year":"2021","journal-title":"J. Fish Biol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"820241","DOI":"10.3389\/fendo.2022.820241","article-title":"Sex Specific Transcriptional Regulation of Gonadal Steroidogenesis in Teleost Fishes","volume":"13","author":"Sharma","year":"2022","journal-title":"Front. Endocrinol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"456","DOI":"10.1002\/mrd.10145","article-title":"Molecular cloning and expression during spermatogenesis of a cDNA encoding testicular 11\u03b2-hydroxylase (P45011beta) in rainbow trout (Oncorhynchus mykiss)","volume":"62","author":"Kusakabe","year":"2002","journal-title":"Mol. Reprod. Dev."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"5139","DOI":"10.1210\/en.2006-0391","article-title":"Roles of 11beta-hydroxysteroid dehydrogenase in fish spermatogenesis","volume":"147","author":"Ozaki","year":"2006","journal-title":"Endocrinology"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1194","DOI":"10.1016\/j.molp.2020.06.009","article-title":"TBtools: An integrative toolkit developed for interactive analyses of big biological data","volume":"13","author":"Chen","year":"2020","journal-title":"Mol. Plant"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1792","DOI":"10.1093\/nar\/gkh340","article-title":"MUSCLE: Multiple sequence alignment with high accuracy and high throughput","volume":"32","author":"Edgar","year":"2004","journal-title":"Nucleic Acids Res."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1870","DOI":"10.1093\/molbev\/msw054","article-title":"MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets","volume":"33","author":"Kumar","year":"2016","journal-title":"Mol. Biol. Evol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"W232","DOI":"10.1093\/nar\/gkw256","article-title":"W-IQ-TREE: A fast online phylogenetic tool for maximum likelihood analysis","volume":"44","author":"Trifinopoulos","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"W293","DOI":"10.1093\/nar\/gkab301","article-title":"Interactive Tree of Life (iTOL) v5: An online tool for phylogenetic tree display and annotation","volume":"49","author":"Letunic","year":"2021","journal-title":"Nucleic Acids Res."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1650","DOI":"10.1038\/nprot.2016.095","article-title":"Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown","volume":"11","author":"Pertea","year":"2016","journal-title":"Nat. Protoc."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"e5631","DOI":"10.7717\/peerj.5631","article-title":"Evaluation of potential reference genes for quantitative RT-PCR analysis in spotted sea bass (Lateolabrax maculatus) under normal and salinity stress conditions","volume":"6","author":"Wang","year":"2018","journal-title":"PeerJ"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"2498","DOI":"10.1101\/gr.1239303","article-title":"Cytoscape: A software environment for integrated models of biomolecular interaction networks","volume":"13","author":"Shannon","year":"2003","journal-title":"Genome Res."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/18\/10905\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T00:33:46Z","timestamp":1760142826000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/18\/10905"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,9,18]]},"references-count":51,"journal-issue":{"issue":"18","published-online":{"date-parts":[[2022,9]]}},"alternative-id":["ijms231810905"],"URL":"https:\/\/doi.org\/10.3390\/ijms231810905","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,9,18]]}}}