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Genotype-specific responses in Atlantic salmon (Salmo salar) subject to dietary fish oil replacement by vegetable oil: a liver transcriptomic analysis.

Morais S, Pratoomyot J, Taggart JB, Bron JE, Guy DR, Bell JG, Tocher DR - BMC Genomics (2011)

Bottom Line: Expansion of aquaculture is seriously limited by reductions in fish oil (FO) supply for aquafeeds.Replacement of dietary FO by VO caused an up-regulation of long-chain polyunsaturated fatty acid biosynthesis, but there was a clear genotype effect as fatty acyl elongase (elovl2) was only up-regulated and desaturases (Δ5 fad and Δ6 fad) showed a higher magnitude of response in Lean fish, which was reflected in liver fatty acid composition.Fatty acid synthase (FAS) was also up-regulated by VO and the effect was independent of genotype.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Aquaculture, University of Stirling, UK. sofia.morais@stir.ac.uk

ABSTRACT

Background: Expansion of aquaculture is seriously limited by reductions in fish oil (FO) supply for aquafeeds. Terrestrial alternatives such as vegetable oils (VO) have been investigated and recently a strategy combining genetic selection with changes in diet formulations has been proposed to meet growing demands for aquaculture products. This study investigates the influence of genotype on transcriptomic responses to sustainable feeds in Atlantic salmon.

Results: A microarray analysis was performed to investigate the liver transcriptome of two family groups selected according to their estimated breeding values (EBVs) for flesh lipid content, 'Lean' or 'Fat', fed diets containing either FO or a VO blend. Diet principally affected metabolism genes, mainly of lipid and carbohydrate, followed by immune response genes. Genotype had a much lower impact on metabolism-related genes and affected mostly signalling pathways. Replacement of dietary FO by VO caused an up-regulation of long-chain polyunsaturated fatty acid biosynthesis, but there was a clear genotype effect as fatty acyl elongase (elovl2) was only up-regulated and desaturases (Δ5 fad and Δ6 fad) showed a higher magnitude of response in Lean fish, which was reflected in liver fatty acid composition. Fatty acid synthase (FAS) was also up-regulated by VO and the effect was independent of genotype. Genetic background of the fish clearly affected regulation of lipid metabolism, as PPARα and PPARβ were down-regulated by the VO diet only in Lean fish, while in Fat salmon SREBP-1 expression was up-regulated by VO. In addition, all three genes had a lower expression in the Lean family group than in the Fat, when fed VO. Differences in muscle adiposity between family groups may have been caused by higher levels of hepatic fatty acid and glycerophospholipid synthesis in the Fat fish, as indicated by the expression of FAS, 1-acyl-sn-glycerol-3-phosphate acyltransferase and lipid phosphate phosphohydrolase 2.

Conclusions: This study has identified metabolic pathways and key regulators that may respond differently to alternative plant-based feeds depending on genotype. Further studies are required but data suggest that it will be possible to identify families better adapted to alternative diet formulations that might be appropriate for future genetic selection programmes.

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Related in: MedlinePlus

Functional categories of genes differentially expressed in Atlantic salmon liver. The top 100 most significant clones (two-way ANOVA analysis; p < 0.05) which were differentially expressed between the two diets (A) and family groups (B) were categorized according to biological function. Non-annotated clones, those representing the same gene or with a miscellaneous function (Tables 2 and 3) are not represented.
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Figure 1: Functional categories of genes differentially expressed in Atlantic salmon liver. The top 100 most significant clones (two-way ANOVA analysis; p < 0.05) which were differentially expressed between the two diets (A) and family groups (B) were categorized according to biological function. Non-annotated clones, those representing the same gene or with a miscellaneous function (Tables 2 and 3) are not represented.

Mentions: Two-way ANOVA of the cDNA microarray dataset returned a high number of features showing evidence of differential expression for each factor - 713 for diet and 788 for genotype - and hence a more detailed analysis was restricted to the top 100 most significant hits for each factor, which were then categorised according to function (excluding 33-35% non-annotated features) (Figure 1). The functional category most affected by diet was that of metabolism (mainly lipid and carbohydrate metabolism), while immune response and intracellular trafficking were also affected. Within lipid metabolism, the affected genes are involved in PUFA, fatty acid and cholesterol biosynthesis (fatty acyl desaturases - Δ5 fad and Δ6 fad, fatty acid synthase - FAS, squalene monooxygenase and possibly cytochrome P450 reductase), glycerophospholipid metabolism (phospholipase D3) and acylglycerol homeostasis (angiopoietin-like 3). Some genes related to carbohydrate metabolism, implicated in glycolysis, glutamine/fructose 6-phosphate and glycerol-3-phosphate metabolism, such as alpha-enolase, glutamine-fructose-6-phosphate transaminase 1(GFPT1) and glycerol kinase, respectively, were also identified as being significantly affected by diet. Genotype had a lower impact on metabolism-related genes (primarily lipid and protein metabolism) and affected mostly genes involved in signalling. Regarding lipid metabolism, primary roles of affected genes are in glycerophospholipid metabolism (N-acylethanolamine-hydrolyzing acid amidase precursor, lipid phosphate phosphohydrolase 2 - LPP2 and 1-acyl-sn-glycerol-3-phosphate acyltransferase - AGPAT), fatty acid transport (intestinal fatty acid binding protein) and lipoprotein metabolism (apolipoprotein B - ApoB and endothelial lipase - EL). In addition, both factors had an effect on a relatively high number of transcription-related genes. Detailed lists of the top 100 most significant genes for diet and genotype, organised by biological function and including the normalised expression ratio between treatments, are shown in Tables 1 and 2, respectively. Gene Ontology enrichment analysis, which enables the identification of GO terms significantly enriched in the input entity list when compared to the whole array dataset, was performed for both factors, providing evidence for which biological processes may be particularly altered in the experimental conditions being compared. For diet, seven significant GO terms, all interrelated, were identified: oxidoreductase activity, stearoyl-CoA 9-desaturase activity, unsaturated fatty acid biosynthetic and metabolic processes, very long chain fatty acid (VLCFA) biosynthetic and metabolic processes. This is explained by the high number of Δ5 fad and Δ6 fad features that were significantly altered when dietary FO was replaced by VO (Table 1). In contrast, no GO terms were significantly enriched in the genotype list.


Genotype-specific responses in Atlantic salmon (Salmo salar) subject to dietary fish oil replacement by vegetable oil: a liver transcriptomic analysis.

Morais S, Pratoomyot J, Taggart JB, Bron JE, Guy DR, Bell JG, Tocher DR - BMC Genomics (2011)

Functional categories of genes differentially expressed in Atlantic salmon liver. The top 100 most significant clones (two-way ANOVA analysis; p < 0.05) which were differentially expressed between the two diets (A) and family groups (B) were categorized according to biological function. Non-annotated clones, those representing the same gene or with a miscellaneous function (Tables 2 and 3) are not represented.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3113789&req=5

Figure 1: Functional categories of genes differentially expressed in Atlantic salmon liver. The top 100 most significant clones (two-way ANOVA analysis; p < 0.05) which were differentially expressed between the two diets (A) and family groups (B) were categorized according to biological function. Non-annotated clones, those representing the same gene or with a miscellaneous function (Tables 2 and 3) are not represented.
Mentions: Two-way ANOVA of the cDNA microarray dataset returned a high number of features showing evidence of differential expression for each factor - 713 for diet and 788 for genotype - and hence a more detailed analysis was restricted to the top 100 most significant hits for each factor, which were then categorised according to function (excluding 33-35% non-annotated features) (Figure 1). The functional category most affected by diet was that of metabolism (mainly lipid and carbohydrate metabolism), while immune response and intracellular trafficking were also affected. Within lipid metabolism, the affected genes are involved in PUFA, fatty acid and cholesterol biosynthesis (fatty acyl desaturases - Δ5 fad and Δ6 fad, fatty acid synthase - FAS, squalene monooxygenase and possibly cytochrome P450 reductase), glycerophospholipid metabolism (phospholipase D3) and acylglycerol homeostasis (angiopoietin-like 3). Some genes related to carbohydrate metabolism, implicated in glycolysis, glutamine/fructose 6-phosphate and glycerol-3-phosphate metabolism, such as alpha-enolase, glutamine-fructose-6-phosphate transaminase 1(GFPT1) and glycerol kinase, respectively, were also identified as being significantly affected by diet. Genotype had a lower impact on metabolism-related genes (primarily lipid and protein metabolism) and affected mostly genes involved in signalling. Regarding lipid metabolism, primary roles of affected genes are in glycerophospholipid metabolism (N-acylethanolamine-hydrolyzing acid amidase precursor, lipid phosphate phosphohydrolase 2 - LPP2 and 1-acyl-sn-glycerol-3-phosphate acyltransferase - AGPAT), fatty acid transport (intestinal fatty acid binding protein) and lipoprotein metabolism (apolipoprotein B - ApoB and endothelial lipase - EL). In addition, both factors had an effect on a relatively high number of transcription-related genes. Detailed lists of the top 100 most significant genes for diet and genotype, organised by biological function and including the normalised expression ratio between treatments, are shown in Tables 1 and 2, respectively. Gene Ontology enrichment analysis, which enables the identification of GO terms significantly enriched in the input entity list when compared to the whole array dataset, was performed for both factors, providing evidence for which biological processes may be particularly altered in the experimental conditions being compared. For diet, seven significant GO terms, all interrelated, were identified: oxidoreductase activity, stearoyl-CoA 9-desaturase activity, unsaturated fatty acid biosynthetic and metabolic processes, very long chain fatty acid (VLCFA) biosynthetic and metabolic processes. This is explained by the high number of Δ5 fad and Δ6 fad features that were significantly altered when dietary FO was replaced by VO (Table 1). In contrast, no GO terms were significantly enriched in the genotype list.

Bottom Line: Expansion of aquaculture is seriously limited by reductions in fish oil (FO) supply for aquafeeds.Replacement of dietary FO by VO caused an up-regulation of long-chain polyunsaturated fatty acid biosynthesis, but there was a clear genotype effect as fatty acyl elongase (elovl2) was only up-regulated and desaturases (Δ5 fad and Δ6 fad) showed a higher magnitude of response in Lean fish, which was reflected in liver fatty acid composition.Fatty acid synthase (FAS) was also up-regulated by VO and the effect was independent of genotype.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Aquaculture, University of Stirling, UK. sofia.morais@stir.ac.uk

ABSTRACT

Background: Expansion of aquaculture is seriously limited by reductions in fish oil (FO) supply for aquafeeds. Terrestrial alternatives such as vegetable oils (VO) have been investigated and recently a strategy combining genetic selection with changes in diet formulations has been proposed to meet growing demands for aquaculture products. This study investigates the influence of genotype on transcriptomic responses to sustainable feeds in Atlantic salmon.

Results: A microarray analysis was performed to investigate the liver transcriptome of two family groups selected according to their estimated breeding values (EBVs) for flesh lipid content, 'Lean' or 'Fat', fed diets containing either FO or a VO blend. Diet principally affected metabolism genes, mainly of lipid and carbohydrate, followed by immune response genes. Genotype had a much lower impact on metabolism-related genes and affected mostly signalling pathways. Replacement of dietary FO by VO caused an up-regulation of long-chain polyunsaturated fatty acid biosynthesis, but there was a clear genotype effect as fatty acyl elongase (elovl2) was only up-regulated and desaturases (Δ5 fad and Δ6 fad) showed a higher magnitude of response in Lean fish, which was reflected in liver fatty acid composition. Fatty acid synthase (FAS) was also up-regulated by VO and the effect was independent of genotype. Genetic background of the fish clearly affected regulation of lipid metabolism, as PPARα and PPARβ were down-regulated by the VO diet only in Lean fish, while in Fat salmon SREBP-1 expression was up-regulated by VO. In addition, all three genes had a lower expression in the Lean family group than in the Fat, when fed VO. Differences in muscle adiposity between family groups may have been caused by higher levels of hepatic fatty acid and glycerophospholipid synthesis in the Fat fish, as indicated by the expression of FAS, 1-acyl-sn-glycerol-3-phosphate acyltransferase and lipid phosphate phosphohydrolase 2.

Conclusions: This study has identified metabolic pathways and key regulators that may respond differently to alternative plant-based feeds depending on genotype. Further studies are required but data suggest that it will be possible to identify families better adapted to alternative diet formulations that might be appropriate for future genetic selection programmes.

Show MeSH
Related in: MedlinePlus