Modulation of Energy Metabolism and Epigenetic Landscape in Rainbow Trout Fry by a Parental Low Protein/High Carbohydrate Diet

It is now recognized that parental diets could highly affect offspring metabolism and growth. Studies in fish are, however, lacking. In particular, the effect of a parental diet high in carbohydrate (HC) and low in protein (LP) on progeny has never been examined in higher trophic level teleost fish....

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Main Authors: Thérèse Callet, Hongyan Li, Pascale Coste, Stéphane Glise, Cécile Heraud, Patrick Maunas, Yvan Mercier, Nicolas Turonnet, Chloé Zunzunegui, Stéphane Panserat, Valérie Bolliet, Lucie Marandel
Format: Article
Language:English
Published: MDPI AG 2021-06-01
Series:Biology
Subjects:
Online Access:https://www.mdpi.com/2079-7737/10/7/585
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author Thérèse Callet
Hongyan Li
Pascale Coste
Stéphane Glise
Cécile Heraud
Patrick Maunas
Yvan Mercier
Nicolas Turonnet
Chloé Zunzunegui
Stéphane Panserat
Valérie Bolliet
Lucie Marandel
author_facet Thérèse Callet
Hongyan Li
Pascale Coste
Stéphane Glise
Cécile Heraud
Patrick Maunas
Yvan Mercier
Nicolas Turonnet
Chloé Zunzunegui
Stéphane Panserat
Valérie Bolliet
Lucie Marandel
author_sort Thérèse Callet
collection DOAJ
description It is now recognized that parental diets could highly affect offspring metabolism and growth. Studies in fish are, however, lacking. In particular, the effect of a parental diet high in carbohydrate (HC) and low in protein (LP) on progeny has never been examined in higher trophic level teleost fish. Thus, two-year old male and female rainbow trout (<i>Oncorhynchus mykiss</i>) were fed either a control diet (0% carbohydrate and 63.89% protein) or a diet containing 35% carbohydrate and 42.96% protein (HC/LP) for a complete reproductive cycle for females and over a 5-month period for males. Cross-fertilizations were then carried out. To evaluate the effect of the parental diet on their offspring, different phenotypic and metabolic traits were recorded for offspring before their first feeding and again three weeks later. When considering the paternal and maternal HC/LP nutrition independently, fry phenotypes and transcriptomes were only slightly affected. The combination of the maternal and paternal HC/LP diets altered the energy metabolism and mitochondrial dynamics of their progeny, demonstrating the existence of a synergistic effect. The global DNA methylation of whole fry was also highly affected by the HC/LP parental diet, indicating that it could be one of the fundamental mechanisms responsible for the effects of nutritional programming.
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spelling doaj.art-39cf4cc8a83a4b3bbaf9b71673cf1f902023-11-22T01:46:43ZengMDPI AGBiology2079-77372021-06-0110758510.3390/biology10070585Modulation of Energy Metabolism and Epigenetic Landscape in Rainbow Trout Fry by a Parental Low Protein/High Carbohydrate DietThérèse Callet0Hongyan Li1Pascale Coste2Stéphane Glise3Cécile Heraud4Patrick Maunas5Yvan Mercier6Nicolas Turonnet7Chloé Zunzunegui8Stéphane Panserat9Valérie Bolliet10Lucie Marandel11INRAE, Université de Pau et des Pays de L’Adour, E2S UPPA, NUMEA, 64310 Saint-Pée-sur-Nivelle, FranceINRAE, Université de Pau et des Pays de L’Adour, E2S UPPA, NUMEA, 64310 Saint-Pée-sur-Nivelle, FranceINRAE, Université de Pau et des Pays de L’Adour, E2S UPPA, ECOBIOP, 64310 Saint-Pée-sur-Nivelle, FranceINRAE, Université de Pau et des Pays de L’Adour, E2S UPPA, ECOBIOP, 64310 Saint-Pée-sur-Nivelle, FranceINRAE, Université de Pau et des Pays de L’Adour, E2S UPPA, NUMEA, 64310 Saint-Pée-sur-Nivelle, FranceINRAE, Université de Pau et des Pays de L’Adour, E2S UPPA, NUMEA, 64310 Saint-Pée-sur-Nivelle, FranceINRAE, Université de Pau et des Pays de L’Adour, E2S UPPA, NUMEA, 64310 Saint-Pée-sur-Nivelle, FranceINRAE, Université de Pau et des Pays de L’Adour, E2S UPPA, NUMEA, 64310 Saint-Pée-sur-Nivelle, FranceINRAE, Université de Pau et des Pays de L’Adour, E2S UPPA, NUMEA, 64310 Saint-Pée-sur-Nivelle, FranceINRAE, Université de Pau et des Pays de L’Adour, E2S UPPA, NUMEA, 64310 Saint-Pée-sur-Nivelle, FranceINRAE, Université de Pau et des Pays de L’Adour, E2S UPPA, ECOBIOP, 64310 Saint-Pée-sur-Nivelle, FranceINRAE, Université de Pau et des Pays de L’Adour, E2S UPPA, NUMEA, 64310 Saint-Pée-sur-Nivelle, FranceIt is now recognized that parental diets could highly affect offspring metabolism and growth. Studies in fish are, however, lacking. In particular, the effect of a parental diet high in carbohydrate (HC) and low in protein (LP) on progeny has never been examined in higher trophic level teleost fish. Thus, two-year old male and female rainbow trout (<i>Oncorhynchus mykiss</i>) were fed either a control diet (0% carbohydrate and 63.89% protein) or a diet containing 35% carbohydrate and 42.96% protein (HC/LP) for a complete reproductive cycle for females and over a 5-month period for males. Cross-fertilizations were then carried out. To evaluate the effect of the parental diet on their offspring, different phenotypic and metabolic traits were recorded for offspring before their first feeding and again three weeks later. When considering the paternal and maternal HC/LP nutrition independently, fry phenotypes and transcriptomes were only slightly affected. The combination of the maternal and paternal HC/LP diets altered the energy metabolism and mitochondrial dynamics of their progeny, demonstrating the existence of a synergistic effect. The global DNA methylation of whole fry was also highly affected by the HC/LP parental diet, indicating that it could be one of the fundamental mechanisms responsible for the effects of nutritional programming.https://www.mdpi.com/2079-7737/10/7/585nutritional programmingteleost fishoffspringbroodstockmitochondria
spellingShingle Thérèse Callet
Hongyan Li
Pascale Coste
Stéphane Glise
Cécile Heraud
Patrick Maunas
Yvan Mercier
Nicolas Turonnet
Chloé Zunzunegui
Stéphane Panserat
Valérie Bolliet
Lucie Marandel
Modulation of Energy Metabolism and Epigenetic Landscape in Rainbow Trout Fry by a Parental Low Protein/High Carbohydrate Diet
Biology
nutritional programming
teleost fish
offspring
broodstock
mitochondria
title Modulation of Energy Metabolism and Epigenetic Landscape in Rainbow Trout Fry by a Parental Low Protein/High Carbohydrate Diet
title_full Modulation of Energy Metabolism and Epigenetic Landscape in Rainbow Trout Fry by a Parental Low Protein/High Carbohydrate Diet
title_fullStr Modulation of Energy Metabolism and Epigenetic Landscape in Rainbow Trout Fry by a Parental Low Protein/High Carbohydrate Diet
title_full_unstemmed Modulation of Energy Metabolism and Epigenetic Landscape in Rainbow Trout Fry by a Parental Low Protein/High Carbohydrate Diet
title_short Modulation of Energy Metabolism and Epigenetic Landscape in Rainbow Trout Fry by a Parental Low Protein/High Carbohydrate Diet
title_sort modulation of energy metabolism and epigenetic landscape in rainbow trout fry by a parental low protein high carbohydrate diet
topic nutritional programming
teleost fish
offspring
broodstock
mitochondria
url https://www.mdpi.com/2079-7737/10/7/585
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