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. 2020 Oct 27;21(1):742.
doi: 10.1186/s12864-020-07093-w.

Ontogeny of hepatic metabolism in mule ducks highlights different gene expression profiles between carbohydrate and lipid metabolic pathways

William Massimino  1 , Stéphane Davail  1 , Aurélie Secula  2 , Charlotte Andrieux  1 , Marie-Dominique Bernadet  3 , Tracy Pioche  1 , Karine Ricaud  1 , Karine Gontier  1 , Mireille Morisson  4 , Anne Collin  5 , Stéphane Panserat  1 , Marianne Houssier  6
Affiliations

Ontogeny of hepatic metabolism in mule ducks highlights different gene expression profiles between carbohydrate and lipid metabolic pathways

William Massimino et al. BMC Genomics. .

Abstract

Background: The production of foie gras involves different metabolic pathways in the liver of overfed ducks such as lipid synthesis and carbohydrates catabolism, but the establishment of these pathways has not yet been described with precision during embryogenesis. The early environment can have short- and long-term impacts on the physiology of many animal species and can be used to influence physiological responses that is called programming. This study proposes to describe the basal hepatic metabolism at the level of mRNA in mule duck embryos in order to reveal potential interesting programming windows in the context of foie gras production. To this end, a kinetic study was designed to determine the level of expression of selected genes involved in steatosis-related liver functions throughout embryogenesis. The livers of 20 mule duck embryos were collected every 4 days from the 12th day of embryogenesis (E12) until 4 days after hatching (D4), and gene expression analysis was performed. The expression levels of 50 mRNAs were quantified for these 7 sampling points and classified into 4 major cellular pathways.

Results: Interestingly, most mRNAs involved in lipid metabolism are overexpressed after hatching (FASN, SCD1, ACOX1), whereas genes implicated in carbohydrate metabolism (HK1, GAPDH, GLUT1) and development (HGF, IGF, FGFR2) are predominantly overexpressed from E12 to E20. Finally, regarding cellular stress, gene expression appears quite stable throughout development, contrasting with strong expression after hatching (CYP2E1, HSBP1, HSP90AA1).

Conclusion: For the first time we described the kinetics of hepatic ontogenesis at mRNA level in mule ducks and highlighted different expression patterns depending on the cellular pathway. These results could be particularly useful in the design of embryonic programming for the production of foie gras.

Keywords: Embryogenesis; Liver; Transcriptome.

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Conflict of interest statement

The authors declare that the research was conducted with the partial support of the “Comité Interprofessionel des Palmipèdes à Foie gras” (CIFOG).

Figures

Fig. 1
Fig. 1
Relative hepatic expression of development-related genes from E12 to D4. 1. Heatmap illustration of liver gene expressions at different stages in mule ducks. Low gene expression is indicated in yellow, while high expression is in red, according to the color key. 2. Box-and-whisker plots representations of expression profile of RELN (a), FGFR2 (b), IGF (c), GATA6 (d), HGF (e), PROX1 (f), STAB2 (g), ACTB (h), TUBa (j), MEF2C (j), MAPK1 (k), NR5A2 (l) in the liver of mule duck during development. The boxes extend from the 25th to the 75th percentiles, and the whiskers range from the lowest value to the highest
Fig. 2
Fig. 2
Relative hepatic expression of carbohydrate-related genes from E12 to D4. 1. Heatmap illustration of liver gene expressions at different stages in mule ducks. Low gene expression is indicated in yellow, while high expression is in red, according to the color key. 2. Box-and-whisker plots representation of expression profile of GLUT2 (a), HK1 (b), GAPDH (c), GLUT1 (d), ALDH3A2 (e), AMPK (f), INSR (g), CREB2/ATF2 (h), ALDHA7 (i), AKT (j), ChREBP (k) in the liver of mule duck during development. The boxes extend from the 25th to the 75th percentiles, and the whiskers range from the lowest value to the highest
Fig. 3
Fig. 3
Relative hepatic expression of lipid-related genes from E12 to D4. 1. Heatmap illustration of liver gene expressions at different stages in mule ducks. Low gene expression is indicated in yellow, while high expression is in red, according to the color key. 2. Box-and-whisker plots representations of expression profile of FASN (a), SCD1 (b), PPARG (c), LDLR4 (d), CEPT1 (e), ACOX1 (f), ACLY (g), ACSL1 (h), FABP4 (j), PPARA (j), LIPC (k), LXRA (l), ACAD11 (m), CPT1A (n), GPAT1 (o), ACAA2 (p), FAT/CD36 (q), ACAT1 (r), ACSS1 (s), DGAT2 (t) in the liver of mule duck during development. The boxes extend from the 25th to the 75th percentiles, and the whiskers range from the lowest value to the highest
Fig. 4
Fig. 4
Correlation matrix of lipid and carbohydrate gene expressions. This color-coded correlation matrix illustrates the pairwise correlations between levels of gene expression throughout the kinetics (Pearson method, the presence of colored dot means p > 0.01). The color scale on the right indicates the strengths of the correlations (blue for positive correlation, red for negative correlation)
Fig. 5
Fig. 5
Relative hepatic expression of stress-related genes from E12 to D4. 1. Heatmap illustration of liver gene expressions at different stages in mule ducks. Low gene expression is indicated in yellow, while high expression is in red, according to the color key. 2. Box-and-whisker plots representations of expression profile of GSTK1 (a), HSP90AA1 (b), ST13 (c), DNAJA2 (d), GSTT1 (e), HSBP1 (f), CYP2E1 (g) in the liver of mule duck during development. The boxes extend from the 25th to the 75th percentiles, and the whiskers range from the lowest value to the highest
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