{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,28]],"date-time":"2026-07-28T08:03:40Z","timestamp":1785225820865,"version":"3.55.0"},"reference-count":34,"publisher":"MDPI AG","issue":"15","license":[{"start":{"date-parts":[[2026,7,27]],"date-time":"2026-07-27T00:00:00Z","timestamp":1785110400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100012166","name":"National Key R&D Program of China","doi-asserted-by":"publisher","award":["2022YFD2400402"],"award-info":[{"award-number":["2022YFD2400402"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100005906","name":"Central Public-Interest Scientific Institution Basal Research Fund, CAFS","doi-asserted-by":"publisher","award":["2023TD25"],"award-info":[{"award-number":["2023TD25"]}],"id":[{"id":"10.13039\/501100005906","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Int. J. Mol. Sci.","IJMS"],"abstract":"<jats:p>Turbot (Scophthalmus maximus) is a key farmed flatfish species in North China, where growth performance directly determines aquaculture profitability. To elucidate the genetic architecture underlying growth traits, we performed whole-genome resequencing of 177 turbot individuals and obtained 5.29 million high-quality single nucleotide polymorphisms (SNPs). Genome-wide association studies (GWAS) were conducted for eleven growth traits\u2014body weight (BW), total length (TL), body length (BL), body depth (BD), trunk length (TUL), head length (HL), snout length (SnL), caudal peduncle depth (CPD), eye diameter (ED), post-orbital head length (PoL), and interorbital width (IW)\u2014using both single-trait and multi-trait approaches. Heritability estimates ranged from 0.001 (IW) to 0.259 (BW), with BW showing the highest heritability, and genetic correlation analysis revealed strong positive correlations between BW and most body size traits (rg &gt; 0.7). Critically, extensive genetic pleiotropy governing these traits was uncovered. In single-trait GWAS, two pleiotropic loci\u201419:16017254 (within fam81b) and 15:2921091 (within atrn)\u2014were repeatedly associated with the same six body-size traits (BD, BL, CPD, HL, TL, and TUL), demonstrating that single variants can exert coordinated effects across multiple morphological dimensions. Furthermore, multi-trait GWAS captured additional pleiotropic signals that remained undetected in single-trait analyses, identifying 20 novel loci encompassing key candidates such as iqgap1 (cytoskeletal signaling), enah (actin organization), and baz2a (chromatin remodeling). KEGG enrichment further consolidated these findings, with candidate genes significantly enriched in the \u201cRegulation of actin cytoskeleton\u201d pathway, while amd1 emerged as a hub gene integrating three metabolic pathways. Collectively, these results highlight the pervasive pleiotropy underlying turbot growth and serve as promising candidate loci for marker-assisted selection, although independent validation in larger populations is required before practical application.<\/jats:p>","DOI":"10.3390\/ijms27156689","type":"journal-article","created":{"date-parts":[[2026,7,27]],"date-time":"2026-07-27T11:54:26Z","timestamp":1785153266000},"page":"6689","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Genetic Architecture of Growth Traits in Turbot (Scophthalmus maximus) Revealed by Genome-Wide Association Studies"],"prefix":"10.3390","volume":"27","author":[{"given":"Ao","family":"Chen","sequence":"first","affiliation":[{"name":"National Demonstration Center for Experimental Fisheries Science Education, Shanghai Ocean University, Shanghai 201306, China"},{"name":"Research Centre for Aquatic Biotechnology, Chinese Academy of Fishery Sciences, Beijing 100141, China"},{"name":"Beijing Key Laboratory of Fishery Biotechnology, Chinese Academy of Fishery Sciences, Beijing 100141, China"},{"name":"Key Laboratory of Aquatic Genomics, Ministry of Agriculture and Rural Affairs, Beijing 100125, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuo","family":"Liang","sequence":"additional","affiliation":[{"name":"National Demonstration Center for Experimental Fisheries Science Education, Shanghai Ocean University, Shanghai 201306, China"},{"name":"Research Centre for Aquatic Biotechnology, Chinese Academy of Fishery Sciences, Beijing 100141, China"},{"name":"Beijing Key Laboratory of Fishery Biotechnology, Chinese Academy of Fishery Sciences, Beijing 100141, China"},{"name":"Key Laboratory of Aquatic Genomics, Ministry of Agriculture and Rural Affairs, Beijing 100125, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Li","family":"Jiang","sequence":"additional","affiliation":[{"name":"Research Centre for Aquatic Biotechnology, Chinese Academy of Fishery Sciences, Beijing 100141, China"},{"name":"Beijing Key Laboratory of Fishery Biotechnology, Chinese Academy of Fishery Sciences, Beijing 100141, China"},{"name":"Key Laboratory of Aquatic Genomics, Ministry of Agriculture and Rural Affairs, Beijing 100125, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,7,27]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"351","DOI":"10.4194\/1303-2712-v20_5_03","article-title":"Reproductive Performance of Wild and Hatchery-Reared Black Sea Turbot, Psetta maxima, in the Southern Black Sea Coast","volume":"20","author":"Aydin","year":"2020","journal-title":"Turk. J. Fish. Aquat. Sci."},{"key":"ref_2","unstructured":"FAO (2020). Cultured Aquatic Species Information Programme (Psetta maxima), FAO Fisheries and Aquaculture Department."},{"key":"ref_3","unstructured":"Bouza, C., Vandamme, S., Hermida, M., Cabaleiro, S., Volckaert, F., and Mart\u00ednez, P. (2014). AquaTrace Species Leaflet Turbot (Scoph-thalmus maximus)."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1287","DOI":"10.1007\/s10499-016-9985-0","article-title":"A comprehensive survey on selective breeding programs and seed market in the European aquaculture fish industry","volume":"24","author":"Chavanne","year":"2016","journal-title":"Aquac. Int."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1016\/j.aquaculture.2016.03.012","article-title":"Impact of selective breeding on European aquaculture","volume":"472","author":"Janssen","year":"2017","journal-title":"Aquaculture"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1007\/s00438-017-1406-1","article-title":"Identification of novel genes significantly affecting growth in catfish through GWAS analysis","volume":"293","author":"Li","year":"2017","journal-title":"Mol. Genet. Genom."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"655","DOI":"10.1007\/s10126-019-09910-0","article-title":"Genome-Wide Association Study of Growth and Body-Shape-Related Traits in Large Yellow Croaker (Larimichthys crocea) Using ddRAD Sequencing","volume":"21","author":"Zhou","year":"2019","journal-title":"Mar. Biotechnol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"288","DOI":"10.7755\/FB.114.3.3","article-title":"Evaluation of nucleic acids and plasma IGF1 levels for estimating short-term responses of postsmolt Atlantic salmon (Salmo salar) to food availability","volume":"114","author":"Caldarone","year":"2016","journal-title":"Fish. Bull."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1011","DOI":"10.1007\/s10695-021-00961-6","article-title":"Insulin-like growth factor signalling and its significance as a biomarker in fish and shellfish research","volume":"47","author":"Chandhini","year":"2021","journal-title":"Fish Physiol. Biochem."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.aquaculture.2007.08.036","article-title":"Candidate growth genes in finfish\u2014Where should we be looking?","volume":"272","author":"Jerry","year":"2007","journal-title":"Aquaculture"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1131","DOI":"10.1387\/ijdb.041913ee","article-title":"Insulin-like growth factor (IGF) signalling is required for early dorso-anterior development of the zebrafish embryo","volume":"48","author":"Eivers","year":"2004","journal-title":"Int. J. Dev. Biol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1007\/s10126-024-10322-y","article-title":"Association Between Muscle Growth and Transcription of a Mutant MSTN Gene in Olive Flounder (Paralichthys olivaceus)","volume":"26","author":"Kim","year":"2024","journal-title":"Mar. Biotechnol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"38290","DOI":"10.1016\/j.aquaculture.2022.738290","article-title":"CRISPR\/Cas-9 induced knockout of myostatin gene improves growth and disease resistance in channel catfish (Ictalurus punctatus)","volume":"557","author":"Coogan","year":"2022","journal-title":"Aquaculture"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"737423","DOI":"10.1016\/j.aquaculture.2021.737423","article-title":"Muscle growth in targeted knockout common carp (Cyprinus carpio) mstn gene with low off-target effects","volume":"547","author":"Shahi","year":"2022","journal-title":"Aquaculture"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"735672","DOI":"10.1016\/j.aquaculture.2020.735672","article-title":"Growth performance of myostatin knockout red sea bream Pagrus major juveniles produced by genome editing with CRISPR\/Cas9","volume":"529","author":"Ohama","year":"2020","journal-title":"Aquaculture"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"bbaa338","DOI":"10.1093\/bib\/bbaa338","article-title":"A genome-wide association study to identify candidate genes for erectile dysfunction","volume":"22","author":"Kazemi","year":"2020","journal-title":"Brief. Bioinform."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"e14505","DOI":"10.1111\/ele.14505","article-title":"Inheritance of Material Wealth in a Natural Population","volume":"27","author":"McFarlane","year":"2024","journal-title":"Ecol. Lett."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1007\/s12038-020-00089-4","article-title":"Advancements in molecular marker technologies and their applications in diversity studies","volume":"45","author":"Ramesh","year":"2020","journal-title":"J. Biosci."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Lahai, P.M., Aikpokpodion, P.O., Bah, A.M., Lahai, M.T., Meinhardt, L.W., Lim, S., Ahn, E., Zhang, D., and Park, S. (2024). Unveiling the Genetic Diversity and Demographic History of Coffea stenophylla in Sierra Leone Using Genotyping-By-Sequencing. Plants, 14.","DOI":"10.3390\/plants14010050"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"738257","DOI":"10.1016\/j.aquaculture.2022.738257","article-title":"Genome-wide association study (GWAS) of growth traits in olive flounder (Paralichthys olivaceus)","volume":"555","author":"Omeka","year":"2022","journal-title":"Aquaculture"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1007\/s10126-016-9718-4","article-title":"Genomic Selection Using Extreme Phenotypes and Pre-Selection of SNPs in Large Yellow Croaker (Larimichthys crocea)","volume":"18","author":"Dong","year":"2016","journal-title":"Mar. Biotechnol."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Gonzalez-Pena, D., Gao, G., Baranski, M., Moen, T., Cleveland, B.M., Kenney, P.B., Vallejo, R.L., Palti, Y., and Leeds, T.D. (2016). Genome-Wide Association Study for Identifying Loci that Affect Fillet Yield, Carcass, and Body Weight Traits in Rainbow Trout (Oncorhynchus mykiss). Front. Genet., 7.","DOI":"10.3389\/fgene.2016.00203"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Gutierrez, A.P., Y\u00e1\u00f1ez, J.M., Fukui, S., Swift, B., and Davidson, W.S. (2015). Genome-Wide Association Study (GWAS) for Growth Rate and Age at Sexual Maturation in Atlantic Salmon (Salmo salar). PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0119730"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Palaiokostas, C., Kocour, M., Prchal, M., and Houston, R.D. (2018). Accuracy of Genomic Evaluations of Juvenile Growth Rate in Common Carp (Cyprinus carpio) Using Genotyping by Sequencing. Front. Genet., 9.","DOI":"10.3389\/fgene.2018.00082"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Chang, Z., Chen, A., Liang, S., Ma, C., Zhou, T., Zhao, Y., and Jiang, L. (2026). Single- and Multi-Trait Genome-Wide Association Analyses Identify the Genetic Loci and Candidate Genes for Growth Traits in Plecoglossus altivelis. Animals, 16.","DOI":"10.3390\/ani16040670"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"6093","DOI":"10.3168\/jds.2011-5249","article-title":"A recursive algorithm for decomposition and creation of the inverse of the genomic relationship matrix","volume":"95","author":"Faux","year":"2012","journal-title":"J. Dairy Sci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"111834","DOI":"10.1016\/j.celrep.2022.111834","article-title":"Pro-prion, as a membrane adaptor protein for E3 ligase c-Cbl, facilitates the ubiquitination of IGF-1R, promoting melanoma metastasis","volume":"41","author":"Li","year":"2022","journal-title":"Cell Rep."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"101486","DOI":"10.1016\/j.gendis.2024.101486","article-title":"RNA-seq identifies Amd1 as a regulator of hepatocyte proliferation via Skp2 during liver development and hepatocellular carcinoma progression in zebrafish","volume":"12","author":"Zhang","year":"2025","journal-title":"Genes Dis."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1007\/BF02811413","article-title":"An automated annotation tool for genomic DNA sequences using GeneScan and BLAST","volume":"80","author":"Lynn","year":"2001","journal-title":"J. Genet."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"739194","DOI":"10.1016\/j.aquaculture.2022.739194","article-title":"First genome-wide association study and genomic prediction for growth traits in spotted sea bass (Lateolabrax maculatus) using whole-genome resequencing","volume":"566","author":"Zhang","year":"2022","journal-title":"Aquaculture"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"2499","DOI":"10.1093\/brain\/awab207","article-title":"Common molecular mechanisms of SLC6A1 variant-mediated neurodevelopmental disorders in astrocytes and neurons","volume":"144","author":"Mermer","year":"2021","journal-title":"Brain"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1007\/s43069-024-00363-3","article-title":"A Simple Method of Estimation and Testing Based on Q\u2013Q Plots","volume":"5","author":"Nair","year":"2024","journal-title":"SN Oper. Res. Forum"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"149334","DOI":"10.1016\/j.brainres.2024.149334","article-title":"DLGAP3 suppresses malignant behaviors of glioma cells via inhibiting RGS12-mediated MAPK\/ERK signaling","volume":"1848","author":"Wei","year":"2024","journal-title":"Brain Res."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Grace, C., Farrall, M., Watkins, H., and Goel, A. (2019). Manhattan++: Displaying genome-wide association summary statistics with multiple annotation layers. BMC Bioinform., 20.","DOI":"10.1186\/s12859-019-3201-y"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/27\/15\/6689\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,7,28]],"date-time":"2026-07-28T07:57:28Z","timestamp":1785225448000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/27\/15\/6689"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,7,27]]},"references-count":34,"journal-issue":{"issue":"15","published-online":{"date-parts":[[2026,8]]}},"alternative-id":["ijms27156689"],"URL":"https:\/\/doi.org\/10.3390\/ijms27156689","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,7,27]]}}}