Expression and structural analysis of taste receptor genes in Iberian and Duroc pigs

Abstract

Background: Taste receptor genes are expressed in sensory cells located in the tongue and influence food preferences, voluntary feed intake, and other relevant traits. Taste perception may differ between livestock breeds that show differences in eating behaviour and between animals that receive different diets or show phenotypic variation in feed intake or related-traits. The objectives of this work were to deepen the understanding of the regulation of the function of taste receptor genes in the circumvallate papillae of obese Iberian pigs in comparison to Duroc pigs, and to characterize their genetic variation and associations with relevant production traits.

Results: We performed a gene expression and structural analysis of ten taste receptor genes in Iberian and Duroc pigs. Gene expression was quantified in the circumvallate papillae of 48 growing Iberian and Duroc pigs maintained under identical management conditions but fed isocaloric diets differing in energy source: either high concentration of fat rich in oleic acid (HO) or carbohydrates (CH); and sacrificed after 47 days of treatment (50.5 kg live weight). Gene expression differed between the two breeds for most of the analyzed genes, with the TAS1R1, TAS1R2, TAS1R3, TAS2R4, TAS2R38, TAS2R39, GPR84, and CD36 genes being overexpressed in Duroc pigs. The diet effect was modulated by breed, with TAS1R1, TAS1R3, and TAS2R4 genes being overexpressed only in Duroc pigs fed the HO diet. Detection of genetic variants (single nucleotide polymorphisms, SNPs) for this panel of genes was performed on muscle RNA-seq data, and three SNPs in the TAS1R1, TAS1R3, and CD36 genes were selected for association studies. All three SNPs were associated with various growth, fattening, tissue fat content, and composition traits. Moreover, the CD36:c.910G/T SNP was associated with oral CD36 gene expression and with differences in the predicted mRNA secondary structure.

Conclusions: Most taste receptor genes are expressed at lower level in circumvallate papillae from Iberian than Duroc pigs. This aligns with lower overall taste sensitivity, higher feed intake, and obese nature of Iberian pigs. Significant association results were observed for SNPs in the TAS1R1 and TAS1R3 genes with meat quality traits and liver composition, which showed segregation in world-wide distributed breeds, but particularly for a potential causal SNP in the CD36 gene, associated with growth and tissue composition, which segregates in Iberian populations.

Fig. 1

Effects of diet and breed on the expression of taste receptor genes. Fold change in the relative expression of candidate genes according to the two tested factors. a Breed effect; values higher than 1 indicate higher expression in Duroc pigs. b Diet effect; values higher than 1 indicate greater expression in HO diet group. P value: +  < 0.10; * < 0.05; ** < 0.01; *** < 0.001

Fig. 2

Breed x diet interaction effects on relative gene expression. Figures show the fold change in gene expression according to diet in different breed groups (values higher than 1 indicate higher expression in HO): G (global population: Duroc + Iberians), D (Duroc), I (Iberian), P value: +  < 0.10; * < 0.05; ** < 0.01

Fig. 3

Correlation of the levels of expression of taste receptor genes. Correlations of normalized gene expression data between all pairs of analyzed genes in the Iberian and Duroc breeds. The tables below the figures include correlations significantly different from zero after multiple test correction (q < 0.05)

Fig. 4

Correlations of levels of expression of taste receptor genes with phenotypic traits. Correlations of normalized gene expression data with phenotypic traits in Iberian and Duroc pigs. AS: age at slaughter; BW: body weight; DFI: daily feed intake, BFT: backfat depth; HFT: ham fat depth; IMF_LD: intramuscular fat in the L. dorsi muscle; IMF_BF: intramuscular fat in the B. femoris muscle. Tables beside the figures include correlations significantly different from zero after multiple test correction (q < 0.05)

Fig. 5

Prediction of the secondary structure of CD36 mRNA. Secondary structure of mRNAs corresponding to both alleles of the CD36c.910G/T polymorphism, as predicted in silico with the RNAfold tool. The location of the SNP is marked with a yellow circle