RESEARCH ARTICLE An insight on the impact of teleost whole genome duplication on the regulation of the molecular networks controlling skeletal muscle growth Bruno Oliveira Silva Duran ID 1,2☯ , Daniel Garcia de la serrana 3☯ , Bruna Tereza Thomazini Zanella 2 , Erika Stefani Perez ID 2 , Edson Assunc ¸ ão Mareco 4 , Vander Bruno Santos 5 , Robson Francisco Carvalho 2 , Maeli Dal-Pai-Silva ID 2 * 1 Department of Histology, Embryology and Cell Biology, Institute of Biological Sciences, Federal University of Goia ´ s (UFG), Goia ˆ nia, Goia ´ s, Brazil, 2 Department of Structural and Functional Biology, Institute of Biosciences, São Paulo State University (UNESP), Botucatu, São Paulo, Brazil, 3 Department of Cell Biology, Physiology and Immunology, Faculty of Biology, University of Barcelona, Barcelona, Spain, 4 University of Western São Paulo (UNOESTE), Presidente Prudente, São Paulo, Brazil, 5 Fisheries Institute (IP-APTA), São Paulo, São Paulo, Brazil ☯ These authors contributed equally to this work. * maeli.dal-pai@unesp.br Abstract Fish muscle growth is a complex process regulated by multiple pathways, resulting on the net accumulation of proteins and the activation of myogenic progenitor cells. Around 350– 320 million years ago, teleost fish went through a specific whole genome duplication (WGD) that expanded the existent gene repertoire. Duplicated genes can be retained by different molecular mechanisms such as subfunctionalization, neofunctionalization or redundancy, each one with different functional implications. While the great majority of ohnolog genes have been identified in the teleost genomes, the effect of gene duplication in the fish physiol- ogy is still not well characterized. In the present study we studied the effect of WGD on the transcription of the duplicated components controlling muscle growth. We compared the expression of lineage-specific ohnologs related to myogenesis and protein balance in the fast-skeletal muscle of pacus (Piaractus mesopotamicus—Ostariophysi) and Nile tilapias (Oreochromis niloticus—Acanthopterygii) fasted for 4 days and refed for 3 days. We studied the expression of 20 ohnologs and found that in the great majority of cases, duplicated genes had similar expression profiles in response to fasting and refeeding, indicating that their functions during growth have been conserved during the period after the WGD. Our results suggest that redundancy might play a more important role in the retention of ohno- logs of regulatory pathways than initially thought. Also, comparison to non-duplicated ortho- logs showed that it might not be uncommon for the duplicated genes to gain or loss new regulatory elements simultaneously. Overall, several of duplicated ohnologs have similar transcription profiles in response to pro-growth signals suggesting that evolution tends to conserve ohnolog regulation during muscle development and that in the majority of ohno- logs related to muscle growth their functions might be very similar. PLOS ONE PLOS ONE | https://doi.org/10.1371/journal.pone.0255006 July 22, 2021 1 / 19 a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Duran BOS, Garcia de la serrana D, Zanella BTT, Perez ES, Mareco EA, Santos VB, et al. (2021) An insight on the impact of teleost whole genome duplication on the regulation of the molecular networks controlling skeletal muscle growth. PLoS ONE 16(7): e0255006. https://doi. org/10.1371/journal.pone.0255006 Editor: Atsushi Asakura, University of Minnesota Medical School, UNITED STATES Received: April 10, 2021 Accepted: July 7, 2021 Published: July 22, 2021 Copyright: © 2021 Duran et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All data generated during this study are included in this published article. The datasets analysed for this study can be found in the Ensembl Genome Browser 102 (https://www.ensembl.org) and pacu skeletal muscle transcriptome (ENA accession number PRJEB6656). Funding: This work was supported by the São Paulo Research Foundation (FAPESP) (https:// fapesp.br/) [grant numbers #2015/03234-8,