{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,23]],"date-time":"2026-06-23T02:57:06Z","timestamp":1782183426245,"version":"3.54.5"},"reference-count":70,"publisher":"MDPI AG","issue":"15","license":[{"start":{"date-parts":[[2022,8,4]],"date-time":"2022-08-04T00:00:00Z","timestamp":1659571200000},"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":["3217210108"],"award-info":[{"award-number":["3217210108"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Smolting is an important development stage of salmonid, and an energy trade-off occurs between osmotic regulation and growth during smolting in rainbow trout (Oncorhynchus mykiss). Growth hormone releasing hormone, somatostatin, growth hormone and insulin-like growth factor (GHRH-SST-GH-IGF) axis exhibit pleiotropic effects in regulating growth and osmotic adaptation. Due to salmonid specific genome duplication, increased paralogs are identified in the ghrh-sst-gh-igf axis, however, their physiology in modulating osmoregulation has yet to be investigated. In this study, seven sst genes (sst1a, sst1b, sst2, sst3a, sst3b, sst5, sst6) were identified in trout. We further investigated the ghrh-sst-gh-igf axis of diploid and triploid trout in response to seawater challenge. Kidney sst (sst1b, sst2, sst5) and sstr (sstr1b1, sstr5a, sstr5b) expressions were changed (more than 2-fold increase (except for sstr5a with 1.99-fold increase) or less than 0.5-fold decrease) due to osmoregulation, suggesting a pleiotropic physiology of SSTs in modulating growth and smoltification. Triploid trout showed significantly down-regulated brain sstr1b1 and igfbp2a1 (p &lt; 0.05), while diploid trout showed up-regulated brain igfbp1a1 (~2.61-fold, p = 0.057) and igfbp2a subtypes (~1.38-fold, p &lt; 0.05), suggesting triploid trout exhibited a better acclimation to the seawater environment. The triploid trout showed up-regulated kidney igfbp5a subtypes (~6.62 and 7.25-fold, p = 0.099 and 0.078) and significantly down-regulated igfbp5b2 (~0.37-fold, p &lt; 0.05), showing a conserved physiology of teleost IGFBP5a in regulating osmoregulation. The IGFBP6 subtypes are involved in energy and nutritional regulation. Distinctive igfbp6 subtypes patterns (p &lt; 0.05) potentially indicated trout triggered energy redistribution in brain and kidney during osmoregulatory regulation. In conclusion, we showed that the GHRH-SST-GH-IGF axis exhibited pleiotropic effects in regulating growth and osmoregulatory regulation during trout smolting, which might provide new insights into seawater aquaculture of salmonid species.<\/jats:p>","DOI":"10.3390\/ijms23158691","type":"journal-article","created":{"date-parts":[[2022,8,4]],"date-time":"2022-08-04T21:52:48Z","timestamp":1659649968000},"page":"8691","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":15,"title":["Crosstalk between Growth and Osmoregulation of GHRH-SST-GH-IGF Axis in Triploid Rainbow Trout (Oncorhynchus mykiss)"],"prefix":"10.3390","volume":"23","author":[{"given":"Kaiwen","family":"Xiang","sequence":"first","affiliation":[{"name":"Key Laboratory of Mariculture, Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qian","family":"Yang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Mariculture, Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mengqun","family":"Liu","sequence":"additional","affiliation":[{"name":"Key Laboratory of Mariculture, Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaodong","family":"Yang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Mariculture, Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jifang","family":"Li","sequence":"additional","affiliation":[{"name":"Key Laboratory of Mariculture, Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhishuai","family":"Hou","sequence":"additional","affiliation":[{"name":"Key Laboratory of Mariculture, Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haishen","family":"Wen","sequence":"additional","affiliation":[{"name":"Key Laboratory of Mariculture, Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,8,4]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"778","DOI":"10.1134\/S0032945208090099","article-title":"On the problem of ratio of anadromy and residence in salmonids (Salmonidae)","volume":"48","author":"Pavlov","year":"2008","journal-title":"J. Ichthyol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1139\/cjfas-2014-0192","article-title":"Anadromy and residency in steelhead and rainbow trout (Oncorhynchus mykiss): A review of the processes and patterns","volume":"72","author":"Kendall","year":"2015","journal-title":"Can. J. Fish. Aquat. Sci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1038\/nature09440","article-title":"Global threats to human water security and river biodiversity","volume":"467","author":"McIntyre","year":"2010","journal-title":"Nature"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"651","DOI":"10.1038\/s41586-018-0123-1","article-title":"Emerging trends in global freshwater availability","volume":"557","author":"Rodell","year":"2018","journal-title":"Nature"},{"key":"ref_5","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_6","doi-asserted-by":"crossref","first-page":"360","DOI":"10.1038\/s41586-018-0383-9","article-title":"Marine heatwaves under global warming","volume":"560","author":"Fischer","year":"2018","journal-title":"Nature"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"718","DOI":"10.1038\/nclimate3382","article-title":"Climatic vulnerability of the world\u2019s freshwater and marine fishes","volume":"7","author":"Comte","year":"2017","journal-title":"Nat. Clim. Chang."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1701","DOI":"10.1038\/s41467-021-21655-w","article-title":"Threats of global warming to the world\u2019s freshwater fishes","volume":"12","author":"Barbarossa","year":"2021","journal-title":"Nat. Commun."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"626893","DOI":"10.1155\/2015\/626893","article-title":"Data assimilation in numerical weather and climate models","volume":"2015","author":"Zhang","year":"2015","journal-title":"Adv. Meteorol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1016\/S1546-5098(08)60308-8","article-title":"8 Chromosome Set Manipulation and Sex Control in Fish","volume":"9","author":"Thorgaard","year":"1983","journal-title":"Fish Physiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"491","DOI":"10.1577\/1548-8659(1999)128<0491:BGIAFD>2.0.CO;2","article-title":"Better growth in all-female diploid and triploid rainbow trout","volume":"128","author":"Sheehan","year":"1999","journal-title":"Trans. Am. Fish. Soc."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1641\/0006-3568(2005)055[0427:FSATRO]2.0.CO;2","article-title":"Fugitive salmon: Assessing the risks of escaped fish from net-pen aquaculture","volume":"55","author":"Naylor","year":"2005","journal-title":"BioScience"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"192","DOI":"10.1080\/10641262.2012.704598","article-title":"Welfare considerations of triploid fish","volume":"20","author":"Fraser","year":"2012","journal-title":"Rev. Fish. Sci."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1016\/j.ygcen.2010.07.003","article-title":"Environmental endocrinology of salmon smoltification","volume":"170","author":"Stefansson","year":"2011","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1016\/B978-0-12-396951-4.00005-0","article-title":"Smolt physiology and endocrinology","volume":"32","author":"McCormick","year":"2012","journal-title":"Fish Physiol."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Mancera, J.M., and McCormick, S.D. (2019). Role of prolactin, growth hormone, insulin-like growth factor I and cortisol in teleost osmoregulation. Fish Osmoregulation, CRC Press.","DOI":"10.1201\/9780429063909-16"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"2278","DOI":"10.1210\/en.2011-0047","article-title":"Evolution of the insulin-like growth factor binding protein (IGFBP) family","volume":"152","author":"Daza","year":"2011","journal-title":"Endocrinology"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1942","DOI":"10.1210\/en.2015-2024","article-title":"Cross talk between growth and immunity: Coupling of the IGF axis to conserved cytokine pathways in rainbow trout","volume":"157","author":"Alzaid","year":"2016","journal-title":"Endocrinology"},{"key":"ref_19","first-page":"781","article-title":"Endocrine control of osmoregulation in teleost fish","volume":"41","author":"McCormick","year":"2001","journal-title":"Am. Zool."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1366","DOI":"10.1016\/j.dci.2011.07.002","article-title":"Stress and immune modulation in fish","volume":"35","author":"Tort","year":"2011","journal-title":"Dev. Comp. Immunol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1024","DOI":"10.1186\/s12864-019-6408-4","article-title":"Effect of growth rate on transcriptomic responses to immune stimulation in wild-type, domesticated, and GH-transgenic coho salmon","volume":"20","author":"Kim","year":"2019","journal-title":"BMC Genom."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1006\/gcen.1996.0002","article-title":"Effects of growth hormone and insulin-like growth factor I on salinity tolerance and gill Na+, K+-ATPase in Atlantic salmon (Salmo salar): Interaction with cortisol","volume":"101","author":"McCormick","year":"1996","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1006\/gcen.1996.6854","article-title":"Osmoregulatory actions of growth hormone and prolactin in an advanced teleost","volume":"106","author":"Sakamoto","year":"1997","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"80","DOI":"10.3389\/fendo.2018.00080","article-title":"Insulin-Like Growth Factor-Binding Proteins of Teleost Fishes","volume":"9","author":"Macqueen","year":"2018","journal-title":"Front. Endocrinol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/j.ygcen.2011.08.005","article-title":"Circulating salmon 28- and 22-kDa insulin-like growth factor binding proteins (IGFBPs) are co-orthologs of IGFBP-1","volume":"174","author":"Shimizu","year":"2011","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1007\/s10126-015-9649-5","article-title":"Differential gene expression in liver, gill, and olfactory rosettes of coho salmon (Oncorhynchus kisutch) after acclimation to salinity","volume":"17","author":"Maryoung","year":"2015","journal-title":"Mar. Biotechnol."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Breves, J.P., Fujimoto, C.K., Phipps-Costin, S.K., Einarsdottir, I.E., Bjornsson, B.T., and McCormick, S.D. (2017). Variation in branchial expression among insulin-like growth-factor binding proteins (igfbps) during Atlantic salmon smoltification and seawater exposure. BMC Physiol., 17.","DOI":"10.1186\/s12899-017-0028-5"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"110989","DOI":"10.1016\/j.mce.2020.110989","article-title":"Cortisol regulates insulin-like growth-factor binding protein (igfbp) gene expression in Atlantic salmon parr","volume":"518","author":"Breves","year":"2020","journal-title":"Mol. Cell. Endocrinol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"696893","DOI":"10.3389\/fgene.2021.696893","article-title":"Quantitative Genetics of Smoltification Status at the Time of Seawater Transfer in Atlantic Salmon (Salmo Salar)","volume":"12","author":"Khaw","year":"2021","journal-title":"Front. Genet."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1016\/S1546-5098(08)60216-2","article-title":"4 The physiology of smolting salmonids","volume":"11","author":"Hoar","year":"1988","journal-title":"Fish Physiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1060","DOI":"10.1093\/molbev\/mst017","article-title":"Evolution of ancient functions in the vertebrate insulin-like growth factor system uncovered by study of duplicated salmonid fish genomes","volume":"30","author":"Macqueen","year":"2013","journal-title":"Mol. Biol. Evol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/j.ygcen.2017.01.017","article-title":"Divergent regulation of insulin-like growth factor binding protein genes in cultured Atlantic salmon myotubes under different models of catabolism and anabolism","volume":"247","author":"Fuentes","year":"2017","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"34806","DOI":"10.1038\/srep34806","article-title":"The complete salmonid IGF-IR gene repertoire and its transcriptional response to disease","volume":"6","author":"Alzaid","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/j.gene.2010.04.016","article-title":"The evolution of somatostatin in vertebrates","volume":"463","author":"Liu","year":"2010","journal-title":"Gene"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1016\/j.ygcen.2012.12.015","article-title":"Impact of gene\/genome duplications on the evolution of the urotensin II and somatostatin families","volume":"188","author":"Tostivint","year":"2013","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1016\/j.ygcen.2019.02.022","article-title":"Revisiting the evolution of the somatostatin family: Already five genes in the gnathostome ancestor","volume":"279","author":"Tostivint","year":"2019","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"20132881","DOI":"10.1098\/rspb.2013.2881","article-title":"A well-constrained estimate for the timing of the salmonid whole genome duplication reveals major decoupling from species diversification","volume":"281","author":"Macqueen","year":"2014","journal-title":"Proc. R. Soc. B"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"473","DOI":"10.1016\/0016-6480(91)90175-6","article-title":"Effects of nutritional state on in vivo lipid and carbohydrate metabolism of coho salmon (Oncorhynchus kisutch)","volume":"81","author":"Sheridan","year":"1991","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"360","DOI":"10.1016\/j.ygcen.2009.09.002","article-title":"Somatostatin and somatostatin receptors in fish growth","volume":"167","author":"Sheridan","year":"2010","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1006\/frne.1999.0183","article-title":"Somatostatin and its receptor family","volume":"20","author":"Patel","year":"1999","journal-title":"Front. Neuroendocrinol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1023\/B:FISH.0000009261.30672.3a","article-title":"Nutritional regulation of somatostatin expression in rainbow trout (Oncorhynchus mykiss)","volume":"26","author":"Ehrman","year":"2002","journal-title":"Fish Physiol. Biochem."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"e59","DOI":"10.1308\/rcsann.2018.0192","article-title":"The use of the somatostatin analogue octreotide for the conservative management of symptomatic cholecystocolonic fistula: A case report","volume":"101","author":"Kong","year":"2019","journal-title":"Ann. R. Coll. Surg."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.ygcen.2006.12.010","article-title":"Neuroendocrine control of growth hormone in fish","volume":"151","author":"Canosa","year":"2007","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/S0074-7696(05)43004-1","article-title":"Insulin-like growth factor signaling in fish","volume":"243","author":"Wood","year":"2005","journal-title":"Int. Rev. Cytol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.ygcen.2005.01.016","article-title":"Growth hormone and insulin-like growth factors in fish: Where we are and where to go","volume":"142","author":"Reinecke","year":"2005","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1677\/joe.1.06869","article-title":"Coordinated regulation of the GH\/IGF system genes during refeeding in rainbow trout (Oncorhynchus mykiss)","volume":"191","author":"Gabillard","year":"2006","journal-title":"J. Endocrinol."},{"key":"ref_47","first-page":"E637","article-title":"Characterization of three IGFBP mRNAs in Atlantic croaker and their regulation during hypoxic stress: Potential mechanisms of their upregulation by hypoxia","volume":"301","author":"Rahman","year":"2011","journal-title":"Am. J. Physiol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"2722","DOI":"10.1210\/endo.143.7.8905","article-title":"Structure, developmental expression, and physiological regulation of zebrafish IGF binding protein-1","volume":"143","author":"Maures","year":"2002","journal-title":"Endocrinology"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"568","DOI":"10.1038\/cdd.2013.177","article-title":"Calcium deficiency-induced and TRP channel-regulated IGF1R-PI3K-Akt signaling regulates abnormal epithelial cell proliferation","volume":"21","author":"Dai","year":"2014","journal-title":"Cell Death Differ."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/j.cbpb.2016.11.008","article-title":"Two grass carp (Ctenopharyngodon idella) insulin-like growth factor-binding protein 5 genes exhibit different yet conserved functions in development and growth","volume":"204","author":"Zheng","year":"2017","journal-title":"Comp. Biochem. Physiol. Part B Biochem. Mol. Biol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1096\/fj.09-141929","article-title":"Tlr2 is critical for diet-induced metabolic syndrome in a murine model","volume":"24","author":"Himes","year":"2010","journal-title":"FASEB J."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1016\/j.fsi.2016.08.049","article-title":"A comparison of the response of diploid and triploid Atlantic salmon (Salmo salar) siblings to a commercial furunculosis vaccine and subsequent experimental infection with Aeromonas salmonicida","volume":"57","author":"Chalmers","year":"2016","journal-title":"Fish Shellfish Immunol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1111\/j.1749-6632.2009.05331.x","article-title":"Central role of the brain in stress and adaptation: Links to socioeconomic status, health, and disease","volume":"1186","author":"McEwen","year":"2010","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1024","DOI":"10.1210\/me.2004-0392","article-title":"Targeted knockdown of insulin-like growth factor binding protein-2 disrupts cardiovascular development in zebrafish embryos","volume":"19","author":"Wood","year":"2005","journal-title":"Mol. Endocrinol."},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Zhou, J., Li, W., Kamei, H., and Duan, C. (2008). Duplication of the IGFBP-2 gene in teleost fish: Protein structure and functionality conservation and gene expression divergence. PLoS ONE, 3.","DOI":"10.1371\/journal.pone.0003926"},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Bower, N.I., and Johnston, I.A. (2010). Transcriptional regulation of the IGF signaling pathway by amino acids and insulin-like growth factors during myogenesis in Atlantic salmon. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0011100"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"304","DOI":"10.1111\/mec.13875","article-title":"Genetic basis for variation in salinity tolerance between stickleback ecotypes","volume":"26","author":"Kusakabe","year":"2017","journal-title":"Mol. Ecol."},{"key":"ref_58","first-page":"53","article-title":"Divergence of insulin superfamily ligands, receptors and Igf binding proteins in marine versus freshwater stickleback: Evidence of selection in known and novel genes","volume":"25","author":"Pellissier","year":"2018","journal-title":"Comp. Biochem. Physiol. Part D Genom. Proteom"},{"key":"ref_59","doi-asserted-by":"crossref","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"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"550","DOI":"10.1186\/s13059-014-0550-8","article-title":"Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2","volume":"15","author":"Love","year":"2014","journal-title":"Genome Biol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"3022","DOI":"10.1093\/molbev\/msab120","article-title":"MEGA11: Molecular Evolutionary Genetics Analysis Version 11","volume":"38","author":"Tamura","year":"2021","journal-title":"Mol. Biol. Evol."},{"key":"ref_62","first-page":"406","article-title":"The neighbor-joining method: A new method for reconstructing phylogenetic trees","volume":"4","author":"Saitou","year":"1987","journal-title":"Mol. Biol. Evol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"103987","DOI":"10.1016\/j.dci.2020.103987","article-title":"Identification and characterization of caspases genes in rainbow trout (Oncorhynchus mykiss) and their expression profiles after Aeromonas salmonicida and Vibrio anguillarum infection","volume":"118","author":"Zeng","year":"2021","journal-title":"Dev. Comp. Immunol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and the 2\u2212\u0394\u0394CT method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1016\/j.aquaculture.2019.01.003","article-title":"Transcriptome and physiological analysis reveal alterations in muscle metabolisms and immune responses of grass carp (Ctenopharyngodon idellus) cultured at different stocking densities","volume":"503","author":"Zhao","year":"2019","journal-title":"Aquaculture"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1007\/s00395-019-0715-4","article-title":"Fibroblast polarization over the myocardial infarction time continuum shifts roles from inflammation to angiogenesis","volume":"114","author":"Mouton","year":"2019","journal-title":"Basic Res. Cardiol."},{"key":"ref_67","unstructured":"Anders, S., and Huber, W. (2012). Differential Expression of RNA-Seq Data at the Gene Level\u2014The DESeq Package, European Molecular Biology Laboratory (EMBL)."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"e86","DOI":"10.1002\/cpbi.86","article-title":"Using MetaboAnalyst 4.0 for comprehensive and integrative metabolomics data analysis","volume":"68","author":"Chong","year":"2019","journal-title":"Curr. Protoc. Bioinform."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.fsi.2021.12.049","article-title":"Identification and characterization of mkk genes and their expression profiles in rainbow trout (Oncorhynchus mykiss) symptomatically or asymptomatically infected with Vibrio anguillarum","volume":"121","author":"Yang","year":"2022","journal-title":"Fish Shellfish Immunol."},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Liu, M., Yang, X., Zeng, C., Zhao, H., Li, J., Hou, Z., and Wen, H. (2022). Transcriptional Signatures of Immune, Neural, and Endocrine Functions in the Brain and Kidney of Rainbow Trout (Oncorhynchus mykiss) in Response to Aeromonas salmonicida Infection. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23031340"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/15\/8691\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T00:04:14Z","timestamp":1760141054000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/15\/8691"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,8,4]]},"references-count":70,"journal-issue":{"issue":"15","published-online":{"date-parts":[[2022,8]]}},"alternative-id":["ijms23158691"],"URL":"https:\/\/doi.org\/10.3390\/ijms23158691","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,8,4]]}}}