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Rapid intensification of its production and sub-optimal husbandry practices can cause stress, impairing overall fish performance and raising issues related to sustainability, animal welfare, and food safety. The advent of next-generation sequencing technologies has greatly revolutionized the study of fish stress biology, allowing a deeper understanding of the molecular stress responses. Here, we characterized for the first time, using RNA-seq, the different hepatic transcriptome responses of gilthead seabream to common aquaculture challenges, namely overcrowding, net handling, and hypoxia, further integrating them with the liver proteome and metabolome responses. After reference-guided transcriptome assembly, annotation, and differential gene expression analysis, 7, 343, and 654 genes were differentially expressed (adjusted p-value &lt; 0.01, log2|fold-change| &gt;1) in the fish from the overcrowding, net handling, and hypoxia challenged groups, respectively. Gene set enrichment analysis (FDR &lt; 0.05) suggested a scenario of challenge-specific responses, that is, net handling induced ribosomal assembly stress, whereas hypoxia induced DNA replication stress in gilthead seabream hepatocytes, consistent with proteomics and metabolomics\u2019 results. However, both responses converged upon the downregulation of insulin growth factor signalling and induction of endoplasmic reticulum stress. These results demonstrate the high phenotypic plasticity of this species and its differential responses to distinct challenging environments at the transcriptomic level. Furthermore, it provides significant resources for characterizing and identifying potentially novel genes that are important for gilthead seabream resilience and aquaculture production efficiency with regard to fish welfare.<\/jats:p>","DOI":"10.1371\/journal.pone.0300472","type":"journal-article","created":{"date-parts":[[2024,3,22]],"date-time":"2024-03-22T17:32:27Z","timestamp":1711128747000},"page":"e0300472","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":9,"title":["Transcriptomic changes behind Sparus aurata hepatic response to different aquaculture challenges: An RNA-seq study and multiomics integration"],"prefix":"10.1371","volume":"19","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-7751-2870","authenticated-orcid":true,"given":"Cl\u00e1udia","family":"Raposo de Magalh\u00e3es","sequence":"first","affiliation":[]},{"given":"Kenneth","family":"Sandoval","sequence":"additional","affiliation":[]},{"given":"Ferenc","family":"Kagan","sequence":"additional","affiliation":[]},{"given":"Grace","family":"McCormack","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0274-5957","authenticated-orcid":true,"given":"Denise","family":"Schrama","sequence":"additional","affiliation":[]},{"given":"Raquel","family":"Carrilho","sequence":"additional","affiliation":[]},{"given":"Ana Paula","family":"Farinha","sequence":"additional","affiliation":[]},{"given":"Marco","family":"Cerqueira","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9668-1204","authenticated-orcid":true,"given":"Pedro M.","family":"Rodrigues","sequence":"additional","affiliation":[]}],"member":"340","published-online":{"date-parts":[[2024,3,22]]},"reference":[{"key":"pone.0300472.ref001","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1089\/omi.2013.0110","article-title":"RNA-seq technology and its application in fish transcriptomics","volume":"18","author":"X Qian","year":"2014","journal-title":"OMICS"},{"key":"pone.0300472.ref002","doi-asserted-by":"crossref","first-page":"1379","DOI":"10.1111\/raq.12298","article-title":"Transcriptomics in aquaculture: current status and applications","volume":"11","author":"S Chandhini","year":"2019","journal-title":"Rev Aquac"},{"key":"pone.0300472.ref003","volume-title":"The State of World Fisheries and Aquaculture (SOFIA) 2022.","author":"FAO","year":"2022"},{"key":"pone.0300472.ref004","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1016\/j.applanim.2004.02.003","article-title":"Stress and the welfare of cultured fish","volume":"86","author":"FS Conte","year":"2004","journal-title":"Appl Anim Behav Sci"},{"key":"pone.0300472.ref005","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1016\/j.applanim.2006.09.001","article-title":"Fish welfare: Current issues in aquaculture","volume":"104","author":"PJ Ashley","year":"2007","journal-title":"Appl Anim Behav Sci"},{"key":"pone.0300472.ref006","doi-asserted-by":"crossref","first-page":"777","DOI":"10.1046\/j.1365-2109.2002.00717.x","article-title":"Increased stocking density influences the acute physiological stress response of common carp Cyprinus carpio (L.).","volume":"33","author":"NM Ruane","year":"2002","journal-title":"Aquac Res"},{"key":"pone.0300472.ref007","first-page":"416","article-title":"Targeting the Mild-Hypoxia Driving Force for Metabolic and Muscle Transcriptional Reprogramming of Gilthead Sea Bream (Sparus aurata) Juveniles.","volume":"10","author":"F Naya-Catal\u00e0","year":"2021","journal-title":"Biology (Basel)."},{"key":"pone.0300472.ref008","first-page":"1","article-title":"R.F.; L. 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