Gene co-expression patterns in Atlantic salmon adipose tissue provide a molecular link among seasonal changes, energy balance and age at maturity
Sexual maturation in many fishes requires a major physiological change that involves a rapid transition between energy storage and usage. In Atlantic salmon, this transition for the initiation of maturation is tightly controlled by seasonality and requires a high-energy status. Lipid metabolism is a...
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ftunivhelsihelda:oai:helda.helsinki.fi:10138/573635 2024-04-28T08:13:09+00:00 Gene co-expression patterns in Atlantic salmon adipose tissue provide a molecular link among seasonal changes, energy balance and age at maturity Ahi, Ehsan Pashay Verta, Jukka-Pekka Kurko, Johanna Ruokolainen, Annukka Singh, Pooja Debes, Paul Vincent Erkinaro, Jaakko Primmer, Craig R. Organismal and Evolutionary Biology Research Programme Evolution, Conservation, and Genomics Helsinki Institute of Sustainability Science (HELSUS) Institute of Biotechnology 2024-03-26T07:11:03Z 16 application/pdf http://hdl.handle.net/10138/573635 eng eng Wiley 10.1111/mec.17313 Funding was provided by Academy of Finland (grant numbers 307593, 302873, 327255 and 342851), and the European Research Council under the European Articles Union's Horizon 2020 and Horizon Europe research and innovation programs (grant numbers 742312 and 101054307). Views and opinions expressed are however those of the authors only and do not necessarily reflect those of the European Union or the European Research Council Executive Agency. Neither the European Union nor the granting authority can be held responsible for them. Ahi , E P , Verta , J-P , Kurko , J , Ruokolainen , A , Singh , P , Debes , P V , Erkinaro , J & Primmer , C R 2024 , ' Gene co-expression patterns in Atlantic salmon adipose tissue provide a molecular link among seasonal changes, energy balance and age at maturity ' , Molecular Ecology . https://doi.org/10.1111/mec.17313 ORCID: /0000-0003-1701-6124/work/156646673 ORCID: /0000-0002-3687-8435/work/156647452 ORCID: /0000-0002-6528-1187/work/156653070 http://hdl.handle.net/10138/573635 0af7a68c-964b-40d0-ae43-9bf47bbb6995 38429895 001176246700001 cc_by info:eu-repo/semantics/openAccess openAccess Atlantic salmon Hippo pathway Adipose tissue Ecology Gene expression Seasonality Sexual maturation Vgll3 1181 Ecology evolutionary biology 1182 Biochemistry cell and molecular biology Article publishedVersion 2024 ftunivhelsihelda 2024-04-03T15:21:21Z Sexual maturation in many fishes requires a major physiological change that involves a rapid transition between energy storage and usage. In Atlantic salmon, this transition for the initiation of maturation is tightly controlled by seasonality and requires a high-energy status. Lipid metabolism is at the heart of this transition since lipids are the main energy storing molecules. The balance between lipogenesis (lipid accumulation) and lipolysis (lipid use) determines energy status transitions. A genomic region containing a transcription co-factor of the Hippo pathway, vgll3, is the main determinant of maturation timing in Atlantic salmon. Interestingly, vgll3 acts as an inhibitor of adipogenesis in mice and its genotypes are potentially associated with seasonal heterochrony in lipid storage and usage in juvenile Atlantic salmon. Here, we explored changes in expression of more than 300 genes directly involved in the processes of adipogenesis, lipogenesis and lipolysis, as well as the Hippo pathway in the adipose tissue of immature and mature Atlantic salmon with distinct vgll3 genotypes. We found molecular evidence consistent with a scenario in which immature males with different vgll3 genotypes exhibit contrasting seasonal dynamics in their lipid profiles. We also identified components of the Hippo signalling pathway as potential major drivers of vgll3 genotype-specific differences in adipose tissue gene expression. This study demonstrates the importance of adipose gene expression patterns for directly linking environmental changes with energy balance and age at maturity through genetic factors bridging lipid metabolism, seasonality and sexual maturation. Peer reviewed Article in Journal/Newspaper Atlantic salmon HELDA – University of Helsinki Open Repository |
institution |
Open Polar |
collection |
HELDA – University of Helsinki Open Repository |
op_collection_id |
ftunivhelsihelda |
language |
English |
topic |
Atlantic salmon Hippo pathway Adipose tissue Ecology Gene expression Seasonality Sexual maturation Vgll3 1181 Ecology evolutionary biology 1182 Biochemistry cell and molecular biology |
spellingShingle |
Atlantic salmon Hippo pathway Adipose tissue Ecology Gene expression Seasonality Sexual maturation Vgll3 1181 Ecology evolutionary biology 1182 Biochemistry cell and molecular biology Ahi, Ehsan Pashay Verta, Jukka-Pekka Kurko, Johanna Ruokolainen, Annukka Singh, Pooja Debes, Paul Vincent Erkinaro, Jaakko Primmer, Craig R. Gene co-expression patterns in Atlantic salmon adipose tissue provide a molecular link among seasonal changes, energy balance and age at maturity |
topic_facet |
Atlantic salmon Hippo pathway Adipose tissue Ecology Gene expression Seasonality Sexual maturation Vgll3 1181 Ecology evolutionary biology 1182 Biochemistry cell and molecular biology |
description |
Sexual maturation in many fishes requires a major physiological change that involves a rapid transition between energy storage and usage. In Atlantic salmon, this transition for the initiation of maturation is tightly controlled by seasonality and requires a high-energy status. Lipid metabolism is at the heart of this transition since lipids are the main energy storing molecules. The balance between lipogenesis (lipid accumulation) and lipolysis (lipid use) determines energy status transitions. A genomic region containing a transcription co-factor of the Hippo pathway, vgll3, is the main determinant of maturation timing in Atlantic salmon. Interestingly, vgll3 acts as an inhibitor of adipogenesis in mice and its genotypes are potentially associated with seasonal heterochrony in lipid storage and usage in juvenile Atlantic salmon. Here, we explored changes in expression of more than 300 genes directly involved in the processes of adipogenesis, lipogenesis and lipolysis, as well as the Hippo pathway in the adipose tissue of immature and mature Atlantic salmon with distinct vgll3 genotypes. We found molecular evidence consistent with a scenario in which immature males with different vgll3 genotypes exhibit contrasting seasonal dynamics in their lipid profiles. We also identified components of the Hippo signalling pathway as potential major drivers of vgll3 genotype-specific differences in adipose tissue gene expression. This study demonstrates the importance of adipose gene expression patterns for directly linking environmental changes with energy balance and age at maturity through genetic factors bridging lipid metabolism, seasonality and sexual maturation. Peer reviewed |
author2 |
Organismal and Evolutionary Biology Research Programme Evolution, Conservation, and Genomics Helsinki Institute of Sustainability Science (HELSUS) Institute of Biotechnology |
format |
Article in Journal/Newspaper |
author |
Ahi, Ehsan Pashay Verta, Jukka-Pekka Kurko, Johanna Ruokolainen, Annukka Singh, Pooja Debes, Paul Vincent Erkinaro, Jaakko Primmer, Craig R. |
author_facet |
Ahi, Ehsan Pashay Verta, Jukka-Pekka Kurko, Johanna Ruokolainen, Annukka Singh, Pooja Debes, Paul Vincent Erkinaro, Jaakko Primmer, Craig R. |
author_sort |
Ahi, Ehsan Pashay |
title |
Gene co-expression patterns in Atlantic salmon adipose tissue provide a molecular link among seasonal changes, energy balance and age at maturity |
title_short |
Gene co-expression patterns in Atlantic salmon adipose tissue provide a molecular link among seasonal changes, energy balance and age at maturity |
title_full |
Gene co-expression patterns in Atlantic salmon adipose tissue provide a molecular link among seasonal changes, energy balance and age at maturity |
title_fullStr |
Gene co-expression patterns in Atlantic salmon adipose tissue provide a molecular link among seasonal changes, energy balance and age at maturity |
title_full_unstemmed |
Gene co-expression patterns in Atlantic salmon adipose tissue provide a molecular link among seasonal changes, energy balance and age at maturity |
title_sort |
gene co-expression patterns in atlantic salmon adipose tissue provide a molecular link among seasonal changes, energy balance and age at maturity |
publisher |
Wiley |
publishDate |
2024 |
url |
http://hdl.handle.net/10138/573635 |
genre |
Atlantic salmon |
genre_facet |
Atlantic salmon |
op_relation |
10.1111/mec.17313 Funding was provided by Academy of Finland (grant numbers 307593, 302873, 327255 and 342851), and the European Research Council under the European Articles Union's Horizon 2020 and Horizon Europe research and innovation programs (grant numbers 742312 and 101054307). Views and opinions expressed are however those of the authors only and do not necessarily reflect those of the European Union or the European Research Council Executive Agency. Neither the European Union nor the granting authority can be held responsible for them. Ahi , E P , Verta , J-P , Kurko , J , Ruokolainen , A , Singh , P , Debes , P V , Erkinaro , J & Primmer , C R 2024 , ' Gene co-expression patterns in Atlantic salmon adipose tissue provide a molecular link among seasonal changes, energy balance and age at maturity ' , Molecular Ecology . https://doi.org/10.1111/mec.17313 ORCID: /0000-0003-1701-6124/work/156646673 ORCID: /0000-0002-3687-8435/work/156647452 ORCID: /0000-0002-6528-1187/work/156653070 http://hdl.handle.net/10138/573635 0af7a68c-964b-40d0-ae43-9bf47bbb6995 38429895 001176246700001 |
op_rights |
cc_by info:eu-repo/semantics/openAccess openAccess |
_version_ |
1797579772342042624 |