Abstract

Background β-Carotene exhibits distinct biological effects that enhance reproductive performance in mammals; however, the mechanisms underlying these effects remain poorly understood. This study aimed to evaluate the effect of β-carotene on ovarian development in replacement gilts and to investigate its potential mechanisms. Results A total of 20 gilts, aged 130 d, were randomly assigned to control group or β-carotene group (β-C group, diet containing 10 mg/kg of β-carotene). Each group consisted of 10 replicates, with one gilt per replicate, over a 60-d trial. β-Carotene significantly increased the number of follicles measuring 2–5 mm in diameter, elevated estradiol concentrations in both blood and follicular fluid of replacement gilts ( P  < 0.05). Compared to the control group, the β-C group exhibited a significant increase in β-carotene concentration within ovarian follicular fluid ( P  < 0.05). Transcriptomic analysis of GCs revealed that β-carotene could significantly upregulated the expression of Forkhead Box L2 (FOXL2). When β-carotene and its metabolic product were administered to granulosa cells (GCs), validation of differentially expressed genes in the transcriptome suggests the possibility that β-carotene, rather than its metabolic product, is responsible for the upregulation of FOXL2 in ovarian GCs, which subsequently may regulate StAR and enhance estradiol synthesis. Furthermore, β-carotene is likely to promote lipolysis, providing essential substrates for estradiol and adenosine triphosphate (ATP) production. Concurrently, β-carotene appears to increase the activity of the antioxidant enzymes superoxide dismutase 1 (SOD1) and glutathione peroxidase 4 (GPX4) in gilts, thereby reducing reactive oxygen species (ROS) ( P  < 0.05) and maintaining redox balance. Conclusions Our findings suggest that β-carotene could promote lipolysis, activate the FOXL2-StAR pathway to increase estradiol synthesis in GCs, and alleviate oxidative stress, thereby contributin