Identification of genomic regions associated with fatty acid metabolism across blood, liver, backfat and muscle in pigs

Abstract

Background: The composition and distribution of fatty acids (FA) are important factors determining the quality, flavor, and nutrient value of meat. In addition, FAs synthesized in the body participate in energy metabolism and are involved in different regulatory pathways in the form of signaling molecules or by acting as agonist or antagonist ligands of different nuclear receptors. Finally, synthesis and catabolism of FAs affect adaptive immunity by regulating lymphocyte metabolism. The present study performed genome-wide association studies using FA profiles of blood, liver, backfat and muscle from 432 commercial Duroc pigs.

Results: Twenty-five genomic regions located on 15 Sus scrofa chromosomes (SSC) were detected. Annotation of the quantitative trait locus (QTL) regions identified 49 lipid metabolism-related candidate genes. Among these QTLs, four were identified in more than one tissue. The ratio of C20:4n-6/C20:3n-6 was associated with the region on SSC2 at 7.56-14.26 Mb for backfat, liver, and muscle. Members of the fatty acid desaturase gene cluster (FADS1, FADS2, and FADS3) are the most promising candidate genes in this region. Two QTL regions on SSC14 (103.81-115.64 Mb and 100.91-128.14 Mb) were identified for FA desaturation in backfat and muscle. In addition, two separate regions on SSC9 at 0 - 14.55 Mb and on SSC12 at 0-1.91 Mb were both associated with the same multiple FA traits for backfat, with candidate genes involved in de novo FA synthesis and triacylglycerol (TAG) metabolism, such as DGAT2 and FASN. The ratio C20:0/C18:0 was associated with the region on SSC5 at 64.84-78.32 Mb for backfat. Furthermore, the association of the C16:0 content with the region at 118.92-123.95 Mb on SSC4 was blood specific. Finally, candidate genes involved in de novo lipogenesis regulate T cell differentiation and promote the generation of palmitoleate, an adipokine that alleviates inflammation.

Conclusions: Several SNPs and candidate genes were associated with lipid metabolism in blood, liver, backfat, and muscle. These results contribute to elucidating the molecular mechanisms implicated in the determination of the FA profile in different pig tissues and can be useful in selection programs that aim to improve health and energy metabolism in pigs.

Fig. 1

Pig chromosomal regions associated with fatty acid composition in blood, liver, adipose tissue, and muscle. Shapes indicate tissues and colors indicate phenotypic traits

Fig. 2

Candidate genes in significant QTL regions and their role in fatty acid metabolic pathways

Fig. 3

Inter-organ crosstalk regulated by adipokines. Adipokines are released into circulation by adipose tissue and target muscle and liver. In muscle, adiponectin activates the p38 mitogen-activated protein kinase (MAPK) and peroxisome proliferator-activated receptor alpha (PPARα), stimulating fatty acid (FA) oxidation. High expression of the FASN and SCD genes promotes the production of palmitoleate, which increases the phosphorylation of insulin receptor substrate (IRS) and facilitates the translocation of the Glucose transporter type 4 (GLUT4) via Akt (protein kinase B) to assist glucose uptake. In the liver, adiponectin activates AMP protein kinase (AMPK) and decreases SREBP1c expression to inhibit hepatic lipogenesis. In addition, activated AMPK phosphorylates acetyl CoA carboxylase-1 (ACC1), which inhibits and decreases the production of malonyl-CoA and promotes FA transport into mitochondria for beta-oxidation