Transcriptome Analysis Reveals Differential Expression of Genes Regulating Hepatic Triglyceride Metabolism in Pekin Ducks During Dietary Threonine Deficiency

Abstract

Dietary threonine (Thr) deficiency increases hepatic triglyceride accumulation in Pekin ducks, which results in fatty liver disease and impairs hepatic function. However, the underlying molecular mechanisms altered by dietary Thr deficiency are still unknown. To identify the underlying molecular changes, 180 one-day-old ducklings were divided into three groups, including Thr deficiency group (Thr-D), Thr sufficiency group (Thr-S), and pair-fed group (Pair-F) that was fed with a Thr-sufficient diet but with reduced daily feed intake. The results showed that feed intake was similar between Thr-D and Pair-F groups, but weight gain rate and final body weight in the Thr-D group were lower than those in the Pair-F group. Feed intake, weight gain, and body weight in Thr-D and Pair-F groups were lower than those in the Thr-S group. The Thr-D diet reduced abdominal fat percentage but increased hepatic triglyceride content when compared with that of the Thr-S and Pair-F groups. The Pair-F reduced hepatic levels of C15:0, C17:0, C18:0, C20:0, C20:4n6, and C22:0 and also reduced total fatty acid, saturated fatty acid, and unsaturated fatty acid content when compared with those of the Thr-D and Thr-S groups. The Thr-D diet increased hepatic content of C6:0, C17:1, C18:3n6, C20:0, C20:1n9, and C22:2, as well as reduced the content of C18:2n6t and C23:0 when compared with those of the Thr-S group. Transcriptome analysis in the liver indicated that the Thr-D diet upregulated genes related to fatty acid and triglyceride synthesis and downregulated genes related to fatty acid oxidation and triglyceride transport. Gene ontology analysis showed that more genes related to lipid metabolism processes and molecular function were differentially expressed in the Thr-D group relative to Thr-S and Pair-F groups than in the Pair-F group relative to the Thr-S group. KEGG pathway analysis showed that differentially expressed genes were enriched in signal transduction, immune, hormone, lipid, and amino acid metabolism pathways. Our findings indicated that the Thr-D diet increased hepatic triglyceride and fatty acid accumulation via increasing fatty acid and triglyceride synthesis and reducing fatty acid oxidation and triglyceride transport. These findings provide novel insights into our understanding of the molecular mechanisms underlying fat accumulation in the liver caused by dietary threonine deficiency.

Effects of genetic selection and threonine on meat quality in Pekin ducks

“…Recently, in our laboratory, it was evaluated that threonine requirement is 0.61% for Pekin duck from 1 to 21 D of age. Meanwhile, we also observed that dietary threonine deficiency would increase hepatic total lipids of Pekin ducks ( Jiang et al., 2017 , Jiang et al., 2019a ) and hepatic fatty acid profile contents ( Jiang et al., 2019b ). Whether dietary threonine supplementation affects fatty acid profile contents of breast muscle and responses of fatty-type duck to dietary threonine levels are similar to those of lean-type duck is still unknown.…”

“…Meanwhile, dietary threonine deficiency increased plasma HDLC and TCHO concentrations. A previous study from our laboratory showed that dietary threonine deficiency increased the gene expression related to fatty acid and triglyceride synthesis, and reduced the gene expression involving in fatty acid oxidation and triglyceride degradation ( Jiang et al., 2019b ), although it did not detect the changes of genes related to lipid transportation to extrahepatic tissue, we speculated that threonine deficiency influences the transfer of lipid from liver to blood by decreasing the protein synthesis in lean-type ducks, hence the lipid was deposited in the liver. Whereas, threonine-deficient diet reduced hepatic total lipids in rat ( Ross-Inta et al., 2009 ).…”

Production performance and plasma metabolite concentrations of broiler chickens fed low crude protein diets differing in Thr and Gly

“…In addition, Thr may also regulate lipid metabolism, by reducing plasma triglyceride level when supplemented at 64% ADF Thr-to-Lys ratio compared to the other Thr levels in the present study. Jiang et al., 2017 , Jiang et al., 2019 suggested that dietary Thr supplementation improved hepatic lipid metabolism of Pekin ducks by regulating lipid synthesis, transport and oxidation. Similar observations were found in mammals ( Yoshida et al., 1961 ; Xiao et al., 2016 ).…”

Physiological Functions of Threonine in Animals: Beyond Nutrition Metabolism

“…Essential amino acids have a close connection with the lipid metabolism, whereby certain amino acids (methionine, leucine, and isoleucine) can affect lipid deposition [ 23 ]. Thr similarly takes part in regulating lipid metabolism and deposition [ 24 ]. Thr supplementation has been shown to enhance hepatic lipid metabolism, while Thr deficiency may induce hepatic triglycerides accumulation, as shown in previous research [ 8 ].…”

“…Research on Pekin ducks found that dietary Thr shortage increased the expression of genes encoding 3-oxoacyl-ACP synthase ( OXSM ), very-long-chain fatty acids protein 7 ( ELOVL7 ), and long-chain fatty acyl-CoA ligase ( ACSBG2 ), which were related to fatty acid and triglyceride synthesis. However, genes participating in fatty acid oxidation, such as acyl-CoA dehydrogenase, acyl-CoA dehydrogenase family member 11 ( ACAD11 ) and cytochrome P450 ( CYP4B ), as well as genes associated with fatty acid and triglyceride transport, acyl-CoA binding protein ( DBI ), apolipoprotein D ( APOD ), and microsomal triglyceride transfer protein ( MTTP ), were downregulated under Thr deficiency in Pekin ducks [ 24 ]. The equilibrium between lipogenesis and lipolysis determines lipid homeostasis [ 25 ].…”