An insight on the impact of teleost whole genome duplication on the regulation of the molecular networks controlling skeletal muscle growth

Detalhes bibliográficos
Autor(a) principal: Duran, Bruno Oliveira Silva [UNESP]
Data de Publicação: 2021
Outros Autores: de la Serrana, Daniel Garcia, Zanella, Bruna Tereza Thomazini [UNESP], Perez, Erika Stefani [UNESP], Mareco, Edson Assunção, Santos, Vander Bruno, Carvalho, Robson Francisco [UNESP], Dal-Pai-Silva, Maeli [UNESP]
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
Texto Completo: http://dx.doi.org/10.1371/journal.pone.0255006
http://hdl.handle.net/11449/233299
Resumo: 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 physiology 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 ohnologs of regulatory pathways than initially thought. Also, comparison to non-duplicated orthologs 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 ohnologs related to muscle growth their functions might be very similar.
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spelling An insight on the impact of teleost whole genome duplication on the regulation of the molecular networks controlling skeletal muscle growthFish 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 physiology 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 ohnologs of regulatory pathways than initially thought. Also, comparison to non-duplicated orthologs 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 ohnologs related to muscle growth their functions might be very similar.Department of Histology Embryology and Cell Biology Institute of Biological Sciences Federal University of Goiás (UFG), GoiásDepartment of Structural and Functional Biology Institute of Biosciences São Paulo State University (UNESP), BotucatuDepartment of Cell Biology Physiology and Immunology Faculty of Biology University of BarcelonaUniversity of Western São Paulo (UNOESTE), Presidente PrudenteFisheries Institute (IP-APTA)Department of Structural and Functional Biology Institute of Biosciences São Paulo State University (UNESP), BotucatuUniversidade Federal de Goiás (UFG)Universidade Estadual Paulista (UNESP)University of BarcelonaUniversity of Western São Paulo (UNOESTE)Fisheries Institute (IP-APTA)Duran, Bruno Oliveira Silva [UNESP]de la Serrana, Daniel GarciaZanella, Bruna Tereza Thomazini [UNESP]Perez, Erika Stefani [UNESP]Mareco, Edson AssunçãoSantos, Vander BrunoCarvalho, Robson Francisco [UNESP]Dal-Pai-Silva, Maeli [UNESP]2022-05-01T06:31:27Z2022-05-01T06:31:27Z2021-07-01info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://dx.doi.org/10.1371/journal.pone.0255006PLoS ONE, v. 16, n. 7 July, 2021.1932-6203http://hdl.handle.net/11449/23329910.1371/journal.pone.02550062-s2.0-85111052897Scopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengPLoS ONEinfo:eu-repo/semantics/openAccess2022-05-01T06:31:27Zoai:repositorio.unesp.br:11449/233299Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462024-08-05T15:09:14.798877Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv An insight on the impact of teleost whole genome duplication on the regulation of the molecular networks controlling skeletal muscle growth
title An insight on the impact of teleost whole genome duplication on the regulation of the molecular networks controlling skeletal muscle growth
spellingShingle An insight on the impact of teleost whole genome duplication on the regulation of the molecular networks controlling skeletal muscle growth
Duran, Bruno Oliveira Silva [UNESP]
title_short An insight on the impact of teleost whole genome duplication on the regulation of the molecular networks controlling skeletal muscle growth
title_full An insight on the impact of teleost whole genome duplication on the regulation of the molecular networks controlling skeletal muscle growth
title_fullStr An insight on the impact of teleost whole genome duplication on the regulation of the molecular networks controlling skeletal muscle growth
title_full_unstemmed An insight on the impact of teleost whole genome duplication on the regulation of the molecular networks controlling skeletal muscle growth
title_sort An insight on the impact of teleost whole genome duplication on the regulation of the molecular networks controlling skeletal muscle growth
author Duran, Bruno Oliveira Silva [UNESP]
author_facet Duran, Bruno Oliveira Silva [UNESP]
de la Serrana, Daniel Garcia
Zanella, Bruna Tereza Thomazini [UNESP]
Perez, Erika Stefani [UNESP]
Mareco, Edson Assunção
Santos, Vander Bruno
Carvalho, Robson Francisco [UNESP]
Dal-Pai-Silva, Maeli [UNESP]
author_role author
author2 de la Serrana, Daniel Garcia
Zanella, Bruna Tereza Thomazini [UNESP]
Perez, Erika Stefani [UNESP]
Mareco, Edson Assunção
Santos, Vander Bruno
Carvalho, Robson Francisco [UNESP]
Dal-Pai-Silva, Maeli [UNESP]
author2_role author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Universidade Federal de Goiás (UFG)
Universidade Estadual Paulista (UNESP)
University of Barcelona
University of Western São Paulo (UNOESTE)
Fisheries Institute (IP-APTA)
dc.contributor.author.fl_str_mv Duran, Bruno Oliveira Silva [UNESP]
de la Serrana, Daniel Garcia
Zanella, Bruna Tereza Thomazini [UNESP]
Perez, Erika Stefani [UNESP]
Mareco, Edson Assunção
Santos, Vander Bruno
Carvalho, Robson Francisco [UNESP]
Dal-Pai-Silva, Maeli [UNESP]
description 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 physiology 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 ohnologs of regulatory pathways than initially thought. Also, comparison to non-duplicated orthologs 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 ohnologs related to muscle growth their functions might be very similar.
publishDate 2021
dc.date.none.fl_str_mv 2021-07-01
2022-05-01T06:31:27Z
2022-05-01T06:31:27Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://dx.doi.org/10.1371/journal.pone.0255006
PLoS ONE, v. 16, n. 7 July, 2021.
1932-6203
http://hdl.handle.net/11449/233299
10.1371/journal.pone.0255006
2-s2.0-85111052897
url http://dx.doi.org/10.1371/journal.pone.0255006
http://hdl.handle.net/11449/233299
identifier_str_mv PLoS ONE, v. 16, n. 7 July, 2021.
1932-6203
10.1371/journal.pone.0255006
2-s2.0-85111052897
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv PLoS ONE
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.source.none.fl_str_mv Scopus
reponame:Repositório Institucional da UNESP
instname:Universidade Estadual Paulista (UNESP)
instacron:UNESP
instname_str Universidade Estadual Paulista (UNESP)
instacron_str UNESP
institution UNESP
reponame_str Repositório Institucional da UNESP
collection Repositório Institucional da UNESP
repository.name.fl_str_mv Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)
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