INTRODUCTION
Weaned piglets require a significant amount of energy for the growth and development during the nursery period [
1]. However, the stress caused by weaning leads to a decrease in feed intake, and therefore lower energy intake [
2]. As a result, a large amount of body fat is mobilized to meet the energy requirements, which is extremely detrimental to the health and growth potential of weaned piglets [
3]. The low body fat content of piglets decreases the ability of piglets to withstand cold. Furthermore, the decreased fat deposition in weaned piglets has been demonstrated to be a significant factor limiting the growth performance of pigs in the subsequent growing-finishing period [
4].
Recently, studies on the regulation of fat deposition or growth in weaning piglets mainly focused on manipulating dietary composition by supplementing dietary fat [
5]. Nevertheless, the utilization of light program management has been widely adopted to enhance the growth performance of livestock. Several studies have reported that Jinjiang cattle subjected to a long photoperiod (LP) (16 h light and 8 h darkness) show significantly increased dry matter intake (DMI) and higher backfat thickness (BF) [
6]. Moreover, it has been demonstrated that extended photoperiod (16 h of light per day) may contribute to greater live weight and carcass weight in growing-finishing pigs than those subjected to a short photoperiod (SP) (8 h of light/d) [
7]. For weaned piglets, multiple studies have shown that an extended photoperiod (23 hours of light per day) leads to heightened feed intake, reduced energy requirements for maintenance, and enhances growth performance in the early post-weaning stage [
8]. Thus, these findings suggest exposure to an extended light program may impact energy metabolism and production performance in domestic animals. However, the effects of prolonged photoperiod on lipid metabolism and growth performance of piglets at the whole nursery phase are still not well understood.
Therefore, this study was designed to characterize the effects of a prolonged photoperiod (16 h light/d vs 10 h light/d) on growth characteristics, blood lipid and hormone profiles, expression of lipid metabolism-related genes, and lipid accumulation in nursery pigs. This study provides clues for the use of light regimen management within the nursery phase to alleviate the pigs’ weaning stress.
DISCUSSION
Weaning stress has been shown to reduce feed intake, increase lipolysis, decrease body fat reserves, and impact the growth of piglets [
1,
3]. Previous studies have demonstrated that weaning stress can be mitigated and feed intake can be increased by changing the component content of the piglet diet [
14]. Additionally, apart from nutritional factors, manipulating photoperiod may offer a viable approach to enhance sow productivity and alleviate weaning stress in piglets [
15]. It is noteworthy that prior research has reported the potential of LPs to stimulate adipose tissue deposition in animals [
6]. However, limited attention has been given to investigate the influence of photoperiod on post-weaning fat metabolism in piglets. Therefore, this study aimed to investigate the effects of prolonged photoperiod on fat metabolism and performance during the entire nursery period for weaned piglets.
Photoperiod is an important environmental factor regulating energy metabolism in animals, and different photoperiod regimes can regulate the performance and fat deposition [
16]. It has been demonstrated that the feed intake of weaned piglets in the 23 L:1 D group increased in the second week after weaning compared to the 8 L:16 D group [
8]. Niekamp et al [
17] fed 4-week-old weaned piglets for six weeks and found that the daily weight gain of piglets in the 16-hour light group was higher than in the 8-hour light group. In this trial, we discovered that the body final weight and ADG of the piglets in the LP group were significantly higher than those in the SP group during 1 to 42 days, but there were no significant differences in ADFI and F/G. This is consistent with previous studies [
18], showing that prolonged photoperiod increases body weight without significantly increasing food intake. Coomans et al [
19] found that prolonged light disrupted the circadian rhythm and caused weight gain in animals, which may be related to the reduction of energy expenditure. In addition, analysis of ADG and ADFI of weaned piglets at each stage of the trial showed that during the last 2 weeks of the nursery period prolonged photoperiod significantly improved ADG and ADFI of weaned piglets. The fact that prolonged photoperiod has no effect on ADG and ADFI in the early weaning period may be due to the need for piglets to adapt to this circadian rhythm, and also suggested that the effect of prolonged photoperiod duration on growth performance of weaned piglets may occur in the late nursery period.
Multiple hormones have been shown to affect feed intake and weight gain in animals. Some studies have shown that tryptophan can through blood-brain barrier transport, increase serotonin production, and increase feed intake and ADG of weaned piglets [
20]. However, Koopmans et al [
21] study on weaned piglets showed increased serotonin levels in the experimental group, but no significant differences in ADG and ADFI between the two groups. Meanwhile, it has been found that dietary supplementation of melatonin can significantly improve the ADG and feed conversion rate of piglets weaned in the second week [
22]. In addition, it has been reported that feeding GH to growing pigs for 30 to 77 days can increase ADG, but reduce feed intake [
23]. The results of this study found that prolonged photoperiod reduced the contents of serotonin, melatonin, and GH in the blood of weaned piglets, while significantly increased ADG, but there was no significant difference in ADFI during the whole test period. The effects of serotonin, melatonin, and GH on the growth performance of weaned piglets are not consistent, and the specific mechanisms of their effects need to be further studied.
In this study, we found that prolonged photoperiod treatment could significantly increase the BF and backfat index of weaned piglets. Previous studies have shown that prolonged photoperiod can increase BF in Jinjiang cattle [
6], consistent with our findings. In addition, weaned piglets in the LP group in this study had higher plasma concentrations of TG and NEFA compared to control weaned piglets at 42 d. Consistently, increased TG and NEFA were observed in the liver, BSF, and LDM tissues from weaned piglets compared with the control group. Higher levels of TG and NEFA were linked to decreased enzyme activity of HSL and ATGL in the BSF and liver from the LP group. All these results suggest that prolonged photoperiod affects the growth development and fat deposition of weaned piglets.
The regulation of lipid metabolism has been found to be tightly linked to a number of hormones, the levels of which may be influenced by photoperiod either directly or indirectly. Research has shown that ewes exposed to the longer photoperiod have a tendency to secrete low levels of GH [
24]. Compared with an 8-h photoperiod, serum melatonin levels in goats decreased under the LP condition of 16 h [
25]. Danilenko et al [
26] have shown that seasonal changes in the photoperiod may affect the circadian amplitude and daytime levels of blood serotonin, with plasma serotonin levels higher in summer compared to winter. In the present study, we found that the serum concentrations of melatonin, serotonin and GH were decreased by the LP, which is consistent with previous research findings. In addition, higher levels of melatonin inhibit the accumulation of fatty acids, thereby inhibiting the formation of TG [
27,
28]. And GH promotes the process of lipolysis [
29]. Therefore, prolonged photoperiod decreases the levels of melatonin and GH, increases fat anabolism, and increases the levels of TG and free fatty acids, while significantly decreasing the mobilization of body fat catabolism.
In the present study, we found prolonged photoperiod induced TG accumulation in BSF tissues, as evidenced by the presence of significantly larger adipocyte size in H&E-stained BSF tissues compared to the control group. Consistent with the H&E staining results, the detection of lipid accumulation by prolonged photoperiod was further confirmed by gene expression analysis. In this experiment, prolonged photoperiod treatment significantly up-regulated the expression of
PPARγ and
C/EBPα genes and proteins in the BSF tissue, suggesting that lipid uptake and lipogenesis were increased in BSF tissues of weaned piglets. Guerrero-Vargas’ data also showed that the constant light group (24 h continuous light) up-regulated the expression of
PPARγ mRNA and increased lipid synthesis in rats [
30].
PPARγ and
C/EBPα interact to promote lipid synthesis and the expression of genes involved in lipogenesis [
31]. In addition, studies have shown that GH may negatively regulate the maturation and accumulation of lipids in adipocytes by decreasing the expression of
C/EBPα and
PPARγ [
32]. Meanwhile, cells treated with melatonin showed that the expression of
PPARγ, a specific adipogenesis regulatory gene, was significantly inhibited [
33]. This suggests that the reduced levels of GH and melatonin caused by prolonged photoperiod may be partly responsible for the increased expression of the
C/EBPα and
PPARγ genes. It is possible that GH and melatonin regulate
PPARγ expression by multiple pathways, and the specific mechanism remains to be further studied.
The lipogenesis related transcription factor
SREBP-1c regulates the endogenous production of saturated and monounsaturated fatty acids, including
FAS and
ACC [
34]. In this study, the mRNA and protein expression of SREBP-1c in the liver and LDM of weaned piglets in the LP group was higher than that in the SP group, suggesting that the increase of TG and NEFA in the liver and LDM tissues of weaned piglets in the LP group may be related to SREBP-1c. In addition, we found that prolonged photoperiod increased the expression of
ACCα and
FAS in liver and LDM tissue. This suggests that prolonged photoperiod improves the ability to resynthesise free fatty acids, leading to increased fat accumulation [
35]. Ruiz et al [
36] found that 18 hours of light exposure increased the expression of
SREBP-1c,
ACCα, and
FAS genes in rat liver compared to 6 and 12 hours of light exposure, which is consistent with the study in this article. In addition, increased melatonin content decreased the expression of
SRBEP-1c and
FAS mRNA and reduced lipid accumulation in the mouse liver [
37]. Li et al [
38] demonstrated that GH inhibited lipid accumulation and lower the expression levels of adipogenic key genes (
SCD1,
SREBP1,
PPARγ, and
C/EBPα) during adipocyte differentiation. Prolonged photoperiod decreased the secretion of GH and melatonin, increased the expression of adipogenic genes in liver and LDM tissues, and inhibited the process of lipolysis.
Another important factor affecting fat accumulation is lipolysis. Studies have shown that the expression of PPARα and CPT1α proteins and genes of guinea pigs were down-regulated by increasing light exposure (24 h) in liver and adipose tissues [
39]. In line with these results, we found that prolonged photoperiod resulted in decreased mRNA expression of the lipolysis gene
CPT1α in
BSF and liver tissues. Western blot analysis further showed that prolongation of photoperiod could promote the decrease of PPARα protein expression in liver and BSF tissue. Liu et al [
39] found that melatonin treatment markedly upregulated
CPT1A and
PPARα gene and protein expression [
39]. In addition, we found that prolonged photoperiod led to decreased expression of the lipolysis genes
ATGL and
HSL in BSF tissues, and decreased the activity of ATGL and HSL enzymes in liver and BSF tissues, reducing the rate of lipolysis. Studies have demonstrated that melatonin up-regulated the expression of lipolytic genes, such as
HSL and
ATGL, and markedly increased lipolysis [
40]. In addition, GHs may not directly affect the expression of
ATGL and
HSL, but may increase the expression of
ATGL and
HSL in vivo through indirect means [
35]. The specific mechanism remains to be further studied. Therefore, we suggest that prolonged photoperiod increases fat deposition in weaned piglets during the nursery period by regulating the expression of lipogenic genes and decreasing the expression of lipolysis genes and lipase activity by suppressing the secretion of melatonin and GHs.