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Why Do Some Rainbow Trout Genotypes Grow Better With a Complete Plant-Based Diet? Transcriptomic and Physiological Analyses on Three Isogenic Lines

Within the context of a growing aquaculture production coupled with a plateau of the production in the main components of aquafeeds (fish oil and fishmeal), recent studies have typically focused on replacing these feedstuffs with terrestrial plant ingredients for cultured carnivorous aquatic species...

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Autores principales: Callet, Thérèse, Dupont-Nivet, Mathilde, Danion, Morgane, Burel, Christine, Cluzeaud, Marianne, Surget, Anne, Aguirre, Pierre, Kerneis, Thierry, Labbé, Laurent, Panserat, Stephane, Quillet, Edwige, Geurden, Inge, Skiba-Cassy, Sandrine, Médale, Françoise
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8440921/
https://www.ncbi.nlm.nih.gov/pubmed/34539452
http://dx.doi.org/10.3389/fphys.2021.732321
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author Callet, Thérèse
Dupont-Nivet, Mathilde
Danion, Morgane
Burel, Christine
Cluzeaud, Marianne
Surget, Anne
Aguirre, Pierre
Kerneis, Thierry
Labbé, Laurent
Panserat, Stephane
Quillet, Edwige
Geurden, Inge
Skiba-Cassy, Sandrine
Médale, Françoise
author_facet Callet, Thérèse
Dupont-Nivet, Mathilde
Danion, Morgane
Burel, Christine
Cluzeaud, Marianne
Surget, Anne
Aguirre, Pierre
Kerneis, Thierry
Labbé, Laurent
Panserat, Stephane
Quillet, Edwige
Geurden, Inge
Skiba-Cassy, Sandrine
Médale, Françoise
author_sort Callet, Thérèse
collection PubMed
description Within the context of a growing aquaculture production coupled with a plateau of the production in the main components of aquafeeds (fish oil and fishmeal), recent studies have typically focused on replacing these feedstuffs with terrestrial plant ingredients for cultured carnivorous aquatic species, such as rainbow trout (Oncorhynchus mykiss). Substitution rates without adverse effects have, however, reached their limit. One potential way forward would be to take advantage of the genetic variability that exists in the salmonid population. However, to date, little is known about the underlying molecular mechanisms responsible for this genetic variability. The aim of the present research was to understand why some genotypes are better able to utilize plant-based diets devoid of marine resources. In this regard, three isogenic lines of rainbow trout (R23h, AB1h, and A22h), with similar growth when fed marine resources-based diets and which differ greatly in their responses to a plant-based diet, were fed with either a complete plant-based diet (V diet) or a marine resources-based diet (M diet) since first-feeding. Fish traits and the hepatic transcriptome of these three genotypes were compared after 5 months of feeding. First, differences in the ability to grow with the V diet observed amongst genotypes was not due to higher feed intake, but instead due to differences in feed efficiency. The comparison of transcriptome profiles revealed 575 (R23h vs. AB1h), 1,770 (R23h vs. A22h), and 2,973 (AB1h vs. A22h) probes differentially expressed amongst the three genotypes when fed the V diet. Interestingly, R23h and AB1h fish, which were the least affected by the V diet, exhibited the highest growth. These results demonstrate that these fish were able to maintain a high level of energy production and protein synthesis. Moreover, these genotypes were also able to activate pathways linked to lipid and cholesterol metabolisms, such as the biosynthesis of long-chain polyunsaturated fatty acids. Finally, as previously, immunity seems to also play an important role in the ability of fish to use the V diet, and further studies are needed to understand the mechanisms by which immunity interacts with growth.
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spelling pubmed-84409212021-09-16 Why Do Some Rainbow Trout Genotypes Grow Better With a Complete Plant-Based Diet? Transcriptomic and Physiological Analyses on Three Isogenic Lines Callet, Thérèse Dupont-Nivet, Mathilde Danion, Morgane Burel, Christine Cluzeaud, Marianne Surget, Anne Aguirre, Pierre Kerneis, Thierry Labbé, Laurent Panserat, Stephane Quillet, Edwige Geurden, Inge Skiba-Cassy, Sandrine Médale, Françoise Front Physiol Physiology Within the context of a growing aquaculture production coupled with a plateau of the production in the main components of aquafeeds (fish oil and fishmeal), recent studies have typically focused on replacing these feedstuffs with terrestrial plant ingredients for cultured carnivorous aquatic species, such as rainbow trout (Oncorhynchus mykiss). Substitution rates without adverse effects have, however, reached their limit. One potential way forward would be to take advantage of the genetic variability that exists in the salmonid population. However, to date, little is known about the underlying molecular mechanisms responsible for this genetic variability. The aim of the present research was to understand why some genotypes are better able to utilize plant-based diets devoid of marine resources. In this regard, three isogenic lines of rainbow trout (R23h, AB1h, and A22h), with similar growth when fed marine resources-based diets and which differ greatly in their responses to a plant-based diet, were fed with either a complete plant-based diet (V diet) or a marine resources-based diet (M diet) since first-feeding. Fish traits and the hepatic transcriptome of these three genotypes were compared after 5 months of feeding. First, differences in the ability to grow with the V diet observed amongst genotypes was not due to higher feed intake, but instead due to differences in feed efficiency. The comparison of transcriptome profiles revealed 575 (R23h vs. AB1h), 1,770 (R23h vs. A22h), and 2,973 (AB1h vs. A22h) probes differentially expressed amongst the three genotypes when fed the V diet. Interestingly, R23h and AB1h fish, which were the least affected by the V diet, exhibited the highest growth. These results demonstrate that these fish were able to maintain a high level of energy production and protein synthesis. Moreover, these genotypes were also able to activate pathways linked to lipid and cholesterol metabolisms, such as the biosynthesis of long-chain polyunsaturated fatty acids. Finally, as previously, immunity seems to also play an important role in the ability of fish to use the V diet, and further studies are needed to understand the mechanisms by which immunity interacts with growth. Frontiers Media S.A. 2021-09-01 /pmc/articles/PMC8440921/ /pubmed/34539452 http://dx.doi.org/10.3389/fphys.2021.732321 Text en Copyright © 2021 Callet, Dupont-Nivet, Danion, Burel, Cluzeaud, Surget, Aguirre, Kerneis, Labbé, Panserat, Quillet, Geurden, Skiba-Cassy and Médale. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Callet, Thérèse
Dupont-Nivet, Mathilde
Danion, Morgane
Burel, Christine
Cluzeaud, Marianne
Surget, Anne
Aguirre, Pierre
Kerneis, Thierry
Labbé, Laurent
Panserat, Stephane
Quillet, Edwige
Geurden, Inge
Skiba-Cassy, Sandrine
Médale, Françoise
Why Do Some Rainbow Trout Genotypes Grow Better With a Complete Plant-Based Diet? Transcriptomic and Physiological Analyses on Three Isogenic Lines
title Why Do Some Rainbow Trout Genotypes Grow Better With a Complete Plant-Based Diet? Transcriptomic and Physiological Analyses on Three Isogenic Lines
title_full Why Do Some Rainbow Trout Genotypes Grow Better With a Complete Plant-Based Diet? Transcriptomic and Physiological Analyses on Three Isogenic Lines
title_fullStr Why Do Some Rainbow Trout Genotypes Grow Better With a Complete Plant-Based Diet? Transcriptomic and Physiological Analyses on Three Isogenic Lines
title_full_unstemmed Why Do Some Rainbow Trout Genotypes Grow Better With a Complete Plant-Based Diet? Transcriptomic and Physiological Analyses on Three Isogenic Lines
title_short Why Do Some Rainbow Trout Genotypes Grow Better With a Complete Plant-Based Diet? Transcriptomic and Physiological Analyses on Three Isogenic Lines
title_sort why do some rainbow trout genotypes grow better with a complete plant-based diet? transcriptomic and physiological analyses on three isogenic lines
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8440921/
https://www.ncbi.nlm.nih.gov/pubmed/34539452
http://dx.doi.org/10.3389/fphys.2021.732321
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