Integrative responses of pig adipose tissues to high-fat high-fiber diet: towards key regulators of energy flexibility

The competition between food and feed challenges the use of alternative resources such asfibrous feedstuffs in diets for pigs. Adding fat to high fiber diets appears as a relevant strategyto improve dietary energy value and feed efficiency, but this changes the nutrients and energysource compared to a standard low fat diet. This study aimed to elucidate the transcriptionalmechanisms involved in variations of adiposity when pigs were fed a high fat high fiber diet.Growing barrows (Large White, n = 48) divergently selected for feed efficiency were offeredduring 10 weeks either a low fat, low fiber diet (LF) or a high fat, high fiber diet (HF) whereoils and wheat straw were used to partially substitute cereals (n = 24 per diet). At 132 days ofage, HF pigs displayed lower (P < 0.001) proportions of perirenal (PRAT; -16%) andsubcutaneous (SCAT; -28%) fat tissues than LF pigs. Analyses using a porcine microarrayshowed that diet had pronounced effects on adipose tissue transcriptomes. The number ofdifferentially-expressed genes (DEG) was greater in PRAT than in SCAT, with 1,251 and 825unique genes being up-regulated and 2,440 and 1,279 unique genes being down-regulated bythe HF diet in PRAT and SCAT, respectively (cutoffs for p corrected BH < 0.10, raw p < 0.01and fold-changes between conditions > 1.1 or < 0.9). A multiple factor analysis revealed largesimilarities between the two adipose tissues in response to diets. Notably, different genesrelated to protein catabolism (33 DEG), protein transport (33 DEG), apoptosis (31 DEG),phosphate metabolic process including ATP synthesis (34 DEG), response to stress (26 DEG)and glucose metabolism (13 DEG) were commonly down-regulated in HF pigs. Conversely,IGF1R participating to the negative regulation of apoptotic process was up-regulated by theHF diet in the two adipose tissues. Correlation modules also stressed the up-regulation by theHF diet of genes related to immunity and defense response specifically in PRAT. Causalitygraph analysis highlighted MLXIPL, SREBF1, peroxisome proliferator-activated receptors(PPARG, PPARD) and their heterodimer partner RXRA as candidate upstream regulators ofthese processes. qPCR analyses confirmed dietary-related differences in expression levels ofthese regulators in the two adipose tissues. Altogether, high fiber intake in growing pigs wasassociated with lower body fatness, which was related to lower glucose metabolism in adiposetissues; its effect on immune factors in the perirenal fat deserves further studies.