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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ftluke:oai:jukuri.luke.fi:10024/554742 2024-09-15T17:55:45+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. orcid:0000-0002-7843-0364 4100111210 Luonnonvarakeskus true https://jukuri.luke.fi/handle/10024/554742 https://doi.org/10.1111/mec.17313 en eng Wiley-Blackwell Molecular ecology 10.1111/mec.17313 0962-1083 1365-294X e17313 How to cite: 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, 00, e17313. https://doi.org/10.1111/mec.17313 https://jukuri.luke.fi/handle/10024/554742 URN:NBN:fi-fe2024082366229 http://dx.doi.org/10.1111/mec.17313 CC BY 4.0 adipose tissue Atlantic salmon ecology gene expression Hippo pathway seasonality sexual maturation vgll3 publication fi=A1 Alkuperäisartikkeli tieteellisessä aikakauslehdessä|sv=A1 Originalartikel i en vetenskaplig tidskrift|en=A1 Journal article (refereed), original research| fi=Publisher's version|sv=Publisher's version|en=Publisher's version| ftluke https://doi.org/10.1111/mec.17313 2024-08-26T23:38:34Z 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. Article in Journal/Newspaper Atlantic salmon Natural Resources Institute Finland: Jukuri Molecular Ecology |
institution |
Open Polar |
collection |
Natural Resources Institute Finland: Jukuri |
op_collection_id |
ftluke |
language |
English |
topic |
adipose tissue Atlantic salmon ecology gene expression Hippo pathway seasonality sexual maturation vgll3 |
spellingShingle |
adipose tissue Atlantic salmon ecology gene expression Hippo pathway seasonality sexual maturation vgll3 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 |
adipose tissue Atlantic salmon ecology gene expression Hippo pathway seasonality sexual maturation vgll3 |
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. |
author2 |
orcid:0000-0002-7843-0364 4100111210 Luonnonvarakeskus |
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-Blackwell |
url |
https://jukuri.luke.fi/handle/10024/554742 https://doi.org/10.1111/mec.17313 |
genre |
Atlantic salmon |
genre_facet |
Atlantic salmon |
op_relation |
Molecular ecology 10.1111/mec.17313 0962-1083 1365-294X e17313 How to cite: 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, 00, e17313. https://doi.org/10.1111/mec.17313 https://jukuri.luke.fi/handle/10024/554742 URN:NBN:fi-fe2024082366229 http://dx.doi.org/10.1111/mec.17313 |
op_rights |
CC BY 4.0 |
op_doi |
https://doi.org/10.1111/mec.17313 |
container_title |
Molecular Ecology |
_version_ |
1810431990728491008 |