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. 2025 Dec 5;24:213–222. doi: 10.1016/j.aninu.2025.09.011

Effects of dietary glutamine supplementation on lipid metabolism, fatty acid composition, and taste properties in the longissimus thoracis muscle of feed-restricted yaks

Ziqi Yue a,b, Liyuan Shi a,b, Rui Hu a,b,⁎, Zhisheng Wang a,b,⁎, Quanhui Peng a,b, Huawei Zou a,b, Jianxin Xiao a,b, Yahui Jiang a,b, Fali Wu a, Yiping Tang a
PMCID: PMC12907847  PMID: 41704246

Abstract

This research aimed to explore the influence of dietary Gln supplementation on serum biochemical indices, slaughter performance, the fatty acid composition, lipid metabolism, and taste properties in the longissimus thoracis muscle of feed-restricted (FR) yaks. A total of 24 healthy yaks (age 31 months and body weight 265.35 ± 25.81 kg) were randomly divided into 3 groups with 8 replicates per group and one yak per replicate. The growth experiment lasted for 60 d in two stages of 1 to 30 d and 31 to 60 d after 15 d of pre-feeding. In the pre-feeding period, all yaks were fed a basal diet ad libitum and the dry matter intake (DMI) was recorded. The yaks in the control (Con) group were fed the basal diet ad libitum during d 0 to 60. The yaks in the feed restriction (FR) group were fed 50% DMI of the pre-feeding period during d 0 to 60, and the yaks in the feed restriction + glutamine (FR + Gln) group were fed 50% DMI of the pre-feeding period during d 0 to 30, and were fed 50% DMI of the pre-feeding + 1% Gln during d 31 to 60. The results showed that FR significantly decreased the average daily gain (ADG), serum triglyceride (TG) concentration, and backfat thickness (BT), as well as intramuscular fat (IMF) content, C18:2n6c, n-6 polyunsaturated fatty acids (PUFA), and PUFA levels in the longissimus thoracis muscle (P < 0.05). However, dietary Gln supplementation significantly increased the ADG from 31 to 60 d, serum TG concentration, BT, and IMF content, as well as up-regulated the expression of the lipid synthesis-related genes acetyl-coa carboxylase (ACC), fatty acid synthase (FAS), peroxisome proliferator-activated receptor α (PPARγ), and sterol regulatory element binding transcription factor 1 (SREBP1), and down-regulated the expression of the lipid breakdown-related genes adipose triglyceride lipase (ATGL) and hormone-sensitive triglyceride lipase (HSL) (P < 0.05). Moreover, dietary Gln supplementation also improved the C18:2n6c, PUFA, and n-6 PUFA levels (P < 0.05). Besides, Gln alleviated the reduction in the umami intensity of the longissimus thoracis muscle of FR yaks (P = 0.019). Mechanistically, the endoplasmic reticulum stress (ERS) might be involved in Gln alleviating the FR induced disturbances in lipid metabolism. These results indicated that Gln alleviated the ERS induced by FR, and relieved the changes in fat deposition, fatty acid composition, and umami intensity.

Keywords: Yak, Feed restriction, Glutamine, Longissimus thoracis muscle, Lipid metabolism, Taste properties

1. Introduction

As living standards improve, consumer expectations for meat quality are rising, and beef remains an important protein source in human diets. Compared with other types of beef, yak (Bos grunniens) meat has plenty of functional fatty acids and high protein content, making it highly nutritious and uniquely flavored (Wang et al., 2022; Xiong et al., 2022). More than 14 million yaks are found worldwide, most of which live in the Qinghai-Tibetan Plateau at elevations of 3000 to 6000 m (Wei et al., 2022). Yaks experience nutrient shortages during the cold season due to their feeding patterns, impacting their growth performance (Gao et al., 2022).

Glutamine is the most common free amino acid found in mammals, primarily stored in skeletal muscle (Manso et al., 2012). Skeletal muscle contributes 40%–50% of the total body weight of an adult mammal (Contreras et al., 2021). However, Gln is considered a “conditionally” essential amino acid. In normal physiological circumstances, the liver and skeletal muscle can synthesize sufficient of Gln (Tomaszewska et al., 2025). Under malnutrition or stress conditions, Gln synthesis in tissues and organs decreases and fails to cover the physiological needs of the organism (Cruzat et al., 2018). An earlier study has reported that dietary Gln supplementation alleviated the growth inhibition of growth-retarded yaks (Ma et al., 2021).

The amount of fat inside the muscles determines the quality of meat in farm animals (Yan et al., 2023). Meat quality can be evaluated by measuring intramuscular fat (IMF) and unsaturated fatty acid (UFA) levels (Huo et al., 2021). It has been established that the amount of intramuscular and intermuscular adipose deposited in beef remains closely linked to sensory qualities such as palatability, tenderness, juiciness, and flavor (Scollan et al., 2017). Fat degradation and synthesis are two major pathways involved in regulating adipose tissue metabolism (Ebadi and Mazurak, 2014). As a result of imbalanced fat degradation and synthesis, starved animals lose fat (Li et al., 2020). During glutaminolysis, Gln is sequentially converted into glutamate and then α-ketoglutarate, which enters the citric acid cycle to facilitate citrate production for lipogenesis (Freeman et al., 2011). A study reported that starvation could reduce Gln synthetase activity in the intestine of rats (Kong et al., 2000). It indicates that starvation could decrease the Gln concentration in animal tissues. It has been shown that Gln could change the fatty acid composition of breast meat in Japanese quail (Tomaszewska et al., 2025). In addition, Gln was able to alleviate lipid peroxidation in the breast muscle of heat-stressed broilers as well as improve hepatic lipid metabolism in post-weaning piglets (Hu et al., 2020; Qi et al., 2020). Therefore, it was investigated whether dietary Gln supplementation could affect the lipid metabolism in yak muscle under feed restriction (FR) conditions.

The endoplasmic reticulum (ER) is the primary site for lipid metabolism because many enzymes are participated in lipid metabolism (Bartelt et al., 2018). The ER experiences stress when its homeostasis is disrupted by the accumulation of misfolded proteins (Li et al., 2022b). The unfolded protein response is triggered by endoplasmic reticulum stress (ERS) through the protein kinase RNA-like endoplasmic reticulum kinase (PERK)/eukaryotic translation initiation factor 2 α (eIF2α)/activating transcription factor 4 (ATF4), inositol-requiring enzyme 1 (IRE1α)/X-box-binding protein 1 (XBP1), and activating transcription factor 6 (ATF6) signaling pathways (Zhang et al., 2022). A study on cows has reported that starvation caused ERS in the liver (Islam et al., 2021). Furthermore, a study on intestinal porcine epithelial cell line J2 (IPEC-J2) found that L-Gln reduced ERS induced by tunicamycin (Jiang et al., 2017). Therefore, it was surmised that Gln might alleviate ERS induced by FR in yak muscle.

This study examined the influence of Gln on fatty acid composition, lipid metabolism, and taste properties of the longissimus thoracis muscle induced by FR in yaks and explored its molecular mechanism.

2. Materials and methods

2.1. Animal ethics statement

The animal experiment was approved by the Animal Welfare Committee of Sichuan Agricultural University (approval number YZQ-2021114009). The experiment was conducted in accordance with an approved animal welfare protocol.

2.2. Animal feeds and experimental design

The growth experiment lasted for 60 d in two stages of 1 to 30 d and 31 to 60 d after 15 d of pre-feeding. A total of 24 yaks with a body weight 265.35 ± 25.81 kg at 31 months of age were randomly divided into 3 groups: control group (Con; fed ad libitum), feed-restricted group (FR; 50% dry matter intake [DMI] of the pre-test period), feed-restricted + 1% Gln group (FR + Gln; in first 30 d with 50% DMI of the pre-test period, in 30-60 d with 50% DMI of the pre-test period + 1% Gln (purity > 99%, chx-51, Fufeng Biotechnologies Co., Ltd., Linyi, Shandong, China). In Table S1, the formulation and nutrient composition of the diets are shown. According to national standard GB/T 6432-2018 (China National Standard, 2018b), the Kjeldahl method (Automatic Kjeldahl nitrogen analyzer, OLB9870A, Biobase Biodustry [Shandong] Co., Ltd., Jinan, Shandong, China) was used to analyze the crude protein (CP) content. The contents of neutral detergent fiber (NDF; GB/T 20806–2022) and acid detergent fiber (ADF; NY/T 1459–2022) were analyzed according to the filtration method (China National Standard, 2022; Ministry of Agriculture of the People's Republic of China, 2022) using the reflux-digestion device, suction filtration apparatus, electric heating drying oven (DHG-9123A, Shanghai Jinghong Laboratory Instrument Co., Ltd., Shanghai, China), and muffle furnace (XMT806, Longkou Xianke Instrument Co., Ltd., Longkou, Shandong, China). The Ca content was determined by the potassium permanganate titration method GB/T 6436-2018 (China National Standard, 2018a). The P content was determined by spectrophotometry GB/T 6437-2018 (China National Standard, 2018c) using an ultraviolet–visible spectrophotometer (400 nm, DU 730, Beckman Coulter Inc., Pasadena, CA, USA). Net energy for maintenance (NEm) and total digestible nutrients (TDN) were calculated according to the nutrient requirements of beef cattle (NASEM, 2016).

All yaks were raised in a formulated diet on the modern farm, and each yak was housed in an individual pen (1.2 m × 2.2 m) with an individual feed and water troughs. Before experiment, all yaks were marked with ear tags, immunized, and dewormed. The yaks were fed total mixed ration (TMR) at 08:00 and 16:00 each day and were provided free drinking water throughout the day.

2.3. Serum biochemical indices

On the final day of the experiment, 15 mL of jugular blood was extracted from each yak using a disposable vacuum blood collection tube. The samples were left for 1 h at room temperature, centrifuged at 3000 × g for 10 min to obtain serum, which was then stored at −20 °C. The kit of non-esterified fatty acid (NEFA; GS191Z) was from Beijing Jiuqiang Biotechnology Co., Ltd. (Beijing, China), and other kits of triglyceride (TG; A110-1-1), total cholesterol (TC; A111-1-1), low-density lipoprotein-cholesterol (LDL-C; A113-1-1), and high-density lipoprotein-cholesterol (HDL-C; A112-1-1) were from Nanjing Jiancheng Bioengineering Institute (Nanjing, Jiangsu, China) and analyzed using an automatic biochemistry analyzer (3100, Hitachi Ltd., Tokyo, Japan).

2.4. Backfat thickness (BT) and IMF content

As soon as the experiment ended, six yaks from each group were randomly selected and were humanely slaughtered referring to GB/T 19477-2018 (China National Standard, 2018d). In the region between the 11th and 12th ribs, BT was determined using a vernier caliper (PD-151, Prokit’s Industries Co., Ltd., Shanghai, China). Then, the longissimus thoracis muscle sample was collected and frozen at −20 °C to analyze the IMF content, which was detected through the Soxhlet extraction technique.

2.5. Oil red O staining

After fixing the longissimus thoracis muscle samples in an environmentally friendly GD fixing solution (G1111, Servicebio Technology Co., Ltd., Wuhan, Hubei, China), paraffin embedding was performed, and cut into 4-μm sections. After dewaxing the slices in xylene, gradient ethanol was used to rehydrate them in water. Oil red O kit (G1015, Servicebio Technology Co., Ltd., Wuhan, Hubei, China) was used to stain the sliced sections, then the neutral resin was sealed, and the samples were examined under a microscope (TS100, Nikon Corp., Tokyo, Japan). The diameter of myofibers was measured using ImageJ v1.80 software (National Institutes of Health, Bethesda Softworks, ML, USA).

2.6. Fatty acid analysis

The fatty acid composition and content in yak meat were analyzed using gas chromatography. Briefly, 0.2 g freeze-dried muscle sample was extracted with 1.2 mL chloroform-methanol mixture (2:1), then 2 mL KOH–CH3OH (0.5 mol/L) was added to the extracted fat and thoroughly mixed, followed by a water bath for 10 min at 95 °C. The tube was cooled to room temperature, and 2 mL of boron trifluoride-methanol (14%) solution was added and incubated for another 20 min at 85 °C to produce the fatty acid methyl esters. The solution was then cooled, and 2 mL of saturated NaCl solution was added with 2 mL of n-hexane, mixed, and centrifuged for 15 min (1006 × g). With GC-2010 Plus gas chromatography (Shimadzu Co., Ltd., Kyoto, Japan), fatty acids were analyzed as methyl esters of fatty acids. In this study, the composition of fatty acids is represented as percentage of the overall fatty acids (% total fatty acid).

2.7. Taste properties

To assess taste differences in yak longissimus thoracis muscle samples, the ASTREE electronic tongue system (ASTREE LS16/48, Alpha M.O.S, Toulouse, France) was utilized. The system has seven types of sensors, which are sourness intensity (AHS), umami intensity (NMS), saltiness intensity (CTS), sweet intensity (ANS), bitterness intensity (SCS), and other water-soluble compounds of the samples (porous potentiometric sensor [PKS] and conductive polymer sensor [CPS]). The reliability and stability of the data were confirmed by validating the e-tongue system through self-testing, diagnosis, and calibration before data collection.

The longissimus thoracis muscle samples were processed and tested by consulting and refining prior research (Li et al., 2022a; Wilson et al., 2025). Briefly, the longissimus thoracis muscle samples (20 g) were homogenized and 80 mL of distilled water was added. Then, the mixture was heated in a 50 °C water bath for 30 min. After centrifugation (3000 × g, 10 min), all the supernatant was collected and made up to 100 mL. Then the electronic tongue was used to analyse the taste properties. For electronic tongue analysis, each longissimus thoracis muscle sample was set at 120 s, and one measurement and stir were obtained per s. The output value was the average value in the last 20 s (100−120 s); each longissimus thoracis muscle sample was measured 5 times. After testing each sample, the sensor was cleaned for 120 s.

2.8. Real-time quantitative PCR (RT-qPCR)

After slaughter, the longissimus thoracis muscle samples were collected and transferred to a −80 °C refrigerator for freezing to determine the molecular measurements. In this study, total RNA was isolated from yak longissimus thoracis muscle using the Trizol (B610409–0100, Sangon Biotech Co., Ltd., Shanghai, China) method. By using a Reverse Transcription kit (A502–01, Exongen Biotechnology Co., Ltd., Chengdu, Sichuan, China), the extracted RNA was converted into complementary DNA (cDNA). On a QuantStudio 5 (Applied Biosystem Co., Ltd., Foster, CA, USA) using SYBR green (G3328, Servicebio Technology Co., Ltd., Wuhan, Hubei, China), RT-qPCR was conducted. The PCR reaction components included 5 μL SYBR green premix, 1 μL cDNA, 3.6 μL diethyl pyrocarbonate (DEPC) water, 0.2 μL forward primers, and 0.2 μL reverse primers. The PCR reaction procedure was performed as follows: 95 °C for 30 s, followed by 95 °C for 15 s and 60 °C for 34 s, then 95 °C for 15 s, and finally 60 °C for 1 min and 95 °C for 15 s for 40 cycles. Table S3 provides a list of genes and primers. Bata-actin was used as an endogenous reference gene for determining relative expression using the 2−ΔΔCt method.

2.9. Western blot analysis

The proteins from yak muscle were extracted using radio immunoprecipitation assay (RIPA) lysate (P0013B) and quantified using a bicinchoninic acid (BCA) protein quantitative kit (P0010S) from Beyotime Biotechnology Co., Ltd. (Shanghai, China). After loading equal amounts of proteins from each sample onto a 7.5% sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) gel, electrophoresis was conducted, then transferred onto polyvinylidene difluoride (PVDF) membranes. In the next step, the PVDF membrane was blocked with a rapid blocking solution (G2052, Servicebio Technology Co., Ltd., Wuhan, Hubei, China) for 5 min at room temperature. The primary antibody was incubated overnight at 4 °C with the membranes, followed by the secondary antibody for 1.5 h. Target proteins were detected using a highly sensitive enhanced chemiluminescence (ECL) reagent (724D281, Oriscience Biological Technology Co., Ltd., Chengdu, Sichuan, China) and visualized with a chemiluminescence imaging system (AGP2307Y05, eBlot Photoelectric Technology Co., Ltd., Shanghai, China). The reference protein used in this study was β-actin. The antibody information is shown in Table S4.

2.10. Immunofluorescence analysis

After fixing the longissimus thoracis muscle samples in an environmentally friendly GD fixing solution (G1111, Servicebio Technology Co., Ltd., Wuhan, Hubei, China), paraffin embedding was performed, and cut into 4-μm sections. The sections were dewaxed using xylene, dehydrated with graded alcohol, and subjected to antigen retrieval. Then the sections were blocked with 5% bovine serum albumin (BSA), incubated with primary antibodies in the blocking solution at 4 °C overnight followed by incubation with secondary antibodies at room temperature for 2 h. The antibody information is listed in Table S5. To complete the observations, an inverted fluorescence microscope (DMI4000B, Leica Imaging Systems Ltd., Wetzlar, Germany) was used to view the sections directly.

2.11. Transmission electron microscope (TEM) observation

The muscle samples were fixed in 2.5% glutaraldehyde for 24 h and then immersed in 2% osmium tetroxide for 2 h. Saturated uranium acetate and lead citrate were used to stain the epoxy resin after dehydration in ethanol and acetone. Lastly, the sections were observed using a TEM (Jem-1400flash, Japan Electron Optics Laboratory Co., Tokyo, Japan).

2.12. Statistical analysis

Each yak was considered an experimental unit. The experimental data were analyzed using one-way analysis of variance (ANOVA), followed by Tukey's post hoc test using SPSS 27.0 (International Business Machines Corp., Chicago, IL, USA). Graphs were made using GraphPad Prism 8.0 (GraphPad Software LLC., La Jolla, CA, USA). Data were quantified using ImageJ v1.80 (National Institutes of Health, Bethesda, MD, USA). The date was expressed as mean and standard error of the mean (SEM), and differences were considered significant when P < 0.05.

The mathematical model for one-way ANOVA is expressed as:

Yij=μ+Ji+eij,

where Yij is the observation of dependent variables; μ is the overall mean; Ji is the treatment effect; eij is the random error.

3. Results

3.1. Serum biochemical indices

Feed-restricted significantly reduced the TG concentration (P = 0.002) and increased the NEFA concentration (P < 0.001) compared to the Con as shown in Table 1. Furthermore, compared with the FR group, dietary Gln supplementation improved the TG concentration (P = 0.002). While FR and Gln had no significant impact on the concentrations of TC, HDL-C, and LDL-C (P > 0.05).

Table 1.

Effects of dietary Gln supplementation on serum biochemical indices of feed-restricted (FR) yaks (mmol/L).

Items Treatments1
 SEM P-value
Con FR FR + Gln
TG 0.48a 0.30b 0.46a 0.119 0.002
TC 1.62 1.64 1.55 0.320 0.861
NEFA 0.40b 0.94a 0.93a 0.286 <0.001
HDL-C 1.10 0.90 0.94 0.254 0.262
LDL-C 0.62 0.76 0.71 0.165 0.234
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TG = triglyceride; TC = total cholesterol; NEFA = non-esterified fatty acid; HDL-C = high-density lipoprotein-cholesterol; LDL-C = low-density lipoprotein-cholesterol; Con = control; FR + Gln = feed restriction + glutamine; SEM = standard error of the mean.

Within a row, means without a common superscript letter differ at P < 0.05, n = 8.

1

Con, the yaks were fed the basal diet ad libitum during d 0 to 60; FR, the yaks were fed 50% dry matter intake (DMI) of the pre-feeding period during d 0 to 60; FR + Gln, the yaks were fed 50% DMI, of the pre-feeding period during d 0 to 30, and were fed 50% DMI, of the pre-feeding + 1% Gln during d 31 to 60.

3.2. Fatty acid composition

The influence of dietary Gln supplementation on fatty acid composition of FR-induced yaks is presented in Table 2. Compared with the Con group, FR significantly increased the C13:0 level, and reduced the levels of C18:2n6c, polyunsaturated fatty acids (PUFA), and n-6 PUFA in the longissimus thoracis muscle of yaks, and PUFA/saturated fatty acids (SFA) (P < 0.05), while dietary Gln supplementation relieved the above changes of C13:0, n-6 PUFA, and PUFA, and PUFA/SFA (P < 0.05). There was no notable impact (P > 0.05) on other fatty acid composition from FR and Gln supplementation (including C4:0, C10:0, C12:0, C14:0, C15:0, C16:0, C17:0, C18:0, C20:0, C22:0, C23:0, C14:1, C15:1, C16:1, C18:1n9t, C18:1n9c, C18:3n3, C20:3n6, C20:5n3, C22:6n3, SFA, monounsaturated fatty acids [MUFA], and n-3 PUFA).

Table 2.

Effects of dietary Gln supplementation on fatty acid composition in longissimus thoracis muscle of feed-restricted (FR) yaks (% total fatty acid).

Items Treatments1
 SEM P-value
Con FR FR + Gln
C4:0 0.097 0.085 0.064 0.0167 0.740
C10:0 0.066 0.065 0.068 0.0028 0.704
C12:0 0.047 0.048 0.048 0.0017 0.855
C13:0 0.011b 0.016a 0.010b 0.0010 0.010
C14:0 1.64 1.45 1.52 0.057 0.454
C15:0 0.21 0.26 0.19 0.012 0.063
C16:0 20.53 21.12 21.30 0.383 0.721
C17:0 1.58 1.69 1.45 0.048 0.103
C18:0 16.96 19.26 16.58 0.707 0.271
C20:0 0.13 0.15 0.12 0.008 0.198
C22:0 0.03 0.07 0.05 0.008 0.252
C23:0 0.40 0.53 0.60 0.059 0.414
C14:1 0.20 0.14 0.19 0.018 0.427
C15:1 0.04 0.06 0.08 0.010 0.342
C16:1 3.95 3.49 3.92 0.184 0.567
C17:1 0.56 0.14 0.25 0.093 0.182
C18:1n9t 1.09 1.93 1.63 0.177 0.164
C18:1n9c 47.40 46.16 47.88 0.671 0.590
C18:2n6c 4.27a 2.50b 3.26b 0.221 <0.001
C18:3n3 0.22 0.22 0.21 0.007 0.790
C20:3n6 0.07 0.09 0.10 0.008 0.460
C20:5n3 0.04 0.06 0.06 0.005 0.405
C22:6n3 0.02 0.03 0.03 0.003 0.605
SFA2 41.70 44.74 42.01 0.737 0.201
MUFA3 53.25 51.92 53.94 0.719 0.538
PUFA4 4.63a 2.89b 3.65ab 0.231 0.002
n-3 PUFA5 0.28 0.31 0.30 0.013 0.765
n-6 PUFA6 4.35a 2.59b 3.36ab 0.232 <0.001
PUFA/SFA 0.11a 0.06b 0.09ab 0.006 0.001
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SFA = saturated fatty acids; MUFA = monounsaturated fatty acids; PUFA = polyunsaturated fatty acids; n-3 PUFA = polyunsaturated fatty acids; n-6 PUFA = polyunsaturated fatty acids; Con = control; FR + Gln = feed restriction + glutamine; SEM = standard error of the mean.

Within a row, means without a common superscript letter differ at P < 0.05, n = 6.

1

Con, the yaks were fed the basal diet ad libitum during d 0 to 60; FR, the yaks were fed 50% dry matter intake (DMI) of the pre-feeding period during d 0 to 60; FR + Gln, the yaks were fed 50% DMI, of the pre-feeding period during d 0 to 30, and were fed 50% DMI, of the pre-feeding + 1% Gln during d 31 to 60.

2

SFA include C4:0, C10:0, C12:0, C13:0, C14:0, C15:0, C16:0, C17:0, C18:0, C20:0, C22:0, and C23:0.

3

MUFA include C14:1, C15:1, C16:1, C17:1, C18:1n9c, and C18:1n9t.

4

PUFA include C18:2n6c, C18:3n3, C18:3n6, C20:5n3, and C22:6n3.

5

n-3 PUFA include C18:3n3, C20:5n3, and C22:6n3.

6

n-6 PUFA include C18:2n6c and C18:3n6.

3.3. Backfat thickness and IMF content

The meat quality is closely linked to BT and IMF content. As illustrated in Table 3, FR significantly decreased the BT (P = 0.029) and IMF (P = 0.007) content compared to the Con group. However, BT and IMF content in the FR + Gln group had no significant difference compared to Con and FR groups (P > 0.05). Oil red O staining of the longissimus thoracis muscle also confirmed this point, as shown in Fig. 1, compared with the Con group, FR reduced the number of lipid droplet (P = 0.003), while dietary Gln supplementation relieved it (P > 0.05).

Table 3.

Effects of dietary Gln supplementation on backfat thickness (BT) and intramuscular fat content (IMF) in the longissimus thoracis muscle of feed-restricted (FR) yaks.

Items Treatments1
 SEM P-value
Con FR FR + Gln
BT, mm 9.47a 5.27b 6.83ab 0.684 0.029
IMF, % 2.56a 1.71b 1.98ab 0.125 0.007
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Con = control; FR + Gln = feed restriction + glutamine; SEM = standard error of the mean.

Within a row, means without a common superscript letter differ at P < 0.05, n = 6.

1

Con, the yaks were fed the basal diet ad libitum during d 0 to 60; FR, the yaks were fed 50% dry matter intake (DMI) of the pre-feeding period during d 0 to 60; FR + Gln, the yaks were fed 50% DMI, of the pre-feeding period during d 0 to 30, and were fed 50% DMI, of the pre-feeding + 1% Gln during d 31 to 60.

Fig. 1.

Fig. 1

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Effects of dietary Gln supplementation on Oil red O staining in the longissimus thoracis muscle of feed-restricted (FR) yaks. (A, B, and C) Oil red O staining; (D) Oil red O quantification. Con, the yaks were fed the basal diet ad libitum during d 0 to 60; FR, the yaks were fed 50% dry matter intake (DMI) of the pre-feeding period during d 0 to 60; FR + Gln, the yaks were fed 50% DMI of the pre-feeding period during d 0 to 30, and were fed 50% DMI of the pre-feeding + 1% Gln during d 31 to 60. Con = control; FR + Gln = feed restriction + glutamine. Different lowercase letters above columns represent significant differences among treatments at P < 0.05, n = 6.

3.4. Taste properties

The effect of dietary Gln supplementation on taste properties in the longissimus thoracis muscle of FR yaks is shown in Table 4 and Fig. 2. The NMS in the FR group was significantly downregulated compared to the Con group, while dietary Gln supplementation relieved it (P = 0.019). There was no notable effect on other taste properties from FR and Gln supplementation (including AHS, CTS, ANS, and SCS) (P > 0.05).

Table 4.

Effects of dietary Gln supplementation on taste properties in the longissimus thoracis muscle of feed-restricted (FR) yaks.

Items Treatments1
 SEM P-value
Con FR FR + Gln
Sourness intensity (AHS) 6.55 6.27 6.49 0.161 0.770
PKS 5.52 5.65 5.71 0.133 0.862
Saltiness intensity (CTS) 5.71 6.83 5.82 0.408 0.492
Umami intensity (NMS) 6.88a 4.75b 6.96a 0.393 0.019
CPS 5.60 5.88 5.23 0.179 0.346
Sweet intensity (ANS) 5.96 4.82 5.93 0.240 0.079
Bitterness intensity (SCS) 6.28 6.43 6.28 0.037 0.171
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Con = control; FR + Gln = feed restriction + glutamine; PKS = porous potentiometric sensor; CPS = conductive polymer sensor; SEM = standard error of the mean.

Within a row, means without a common superscript letter differ at P < 0.05, n = 6.

1

Con, the yaks were fed the basal diet ad libitum during d 0 to 60; FR, the yaks were fed 50% dry matter intake (DMI) of the pre-feeding period during d 0 to 60; FR + Gln, the yaks were fed 50% DMI, of the pre-feeding period during d 0 to 30, and were fed 50% DMI, of the pre-feeding + 1% Gln during d 31 to 60.

Fig. 2.

Fig. 2

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Effects of dietary Gln supplementation on taste properties (radar chart) in the longissimus thoracis muscle of feed-restricted (FR) yaks. Numbers in the figure refer to taste intensity. Con, the yaks were fed the basal diet ad libitum during d 0 to 60; FR, the yaks were fed 50% dry matter intake (DMI) of the pre-feeding period during d 0 to 60; FR + Gln, the yaks were fed 50% DMI of the pre-feeding period during d 0 to 30, and were fed 50% DMI of the pre-feeding + 1% Gln during d 31 to 60; n = 6. AHS, sourness intensity; CTS, saltiness intensity; NMS, umami intensity; ANS, sweet intensity; SCS, bitterness intensity. PKS = porous potentiometric sensor; CPS = conductive polymer sensor; Con = control; FR + Gln = feed restriction + glutamine.

3.5. Lipid metabolism

The influence of dietary Gln supplementation on lipid metabolism in the longissimus thoracis muscle of FR yaks is shown in Fig. 3. Compared with the Con group, FR significantly downregulated the transcriptional levels of FAS, ACC, SREBP1, and PPARγ (P < 0.001), increased the transcriptional levels of HSL, PPARα, and ATGL in yak muscle (P < 0.05), while dietary Gln supplementation relieved transcriptional levels of ACC, FAS, PPARγ, SREBP1, ATGL, and HSL in yak longissimus thoracis muscle (P < 0.001; Fig. 3A and B). However, FR and FR + Gln did not change the CPT1 transcriptional level (P = 0.326). The protein test results showed that FR decreased PPARγ and p-ACC/ACC protein expression levels, and increased ATGL protein expression level, while dietary Gln supplementation relieved them (P < 0.05; Fig. 3C–F). However, FR and FR + Gln had no effect on PPARα protein expression level in yak muscle (P = 0.833; Fig. 3E and F). Similar to the results of mRNA expression, FR significantly decreased the immunofluorescence intensity of SREBP1 protein in yak muscle, while dietary Gln supplementation alleviated to a certain extent (P = 0.029; Fig. 3G and H).

Fig. 3.

Fig. 3

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Effects of dietary Gln supplementation on lipid metabolism in longissimus thoracis muscle of feed-restricted (FR) yaks. (A) Lipid synthesis-related mRNA expression levels. (B) Lipid degradation-related mRNA expression levels. (C and D) Lipid synthesis-related protein expression levels. (E and F) Lipid degradation-related protein expression levels. (G and H) The immunofluorescence of SREBP1 and its quantification results (scale bars represent 100 μm). Con, the yaks were fed the basal diet ad libitum during d 0 to 60; FR, the yaks were fed 50% dry matter intake (DMI) of the pre-feeding period during d 0 to 60; FR + Gln, the yaks were fed 50% DMI of the pre-feeding period during d 0 to 30, and were fed 50% DMI of the pre-feeding + 1% Gln during d 31 to 60. Con = control; FR + Gln = feed restriction + glutamine. Different lowercase letters above columns represent significant differences among treatments at P < 0.05, n = 6.

3.6. Endoplasmic reticulum stress

The influence of dietary Gln supplementation on ERS in the longissimus thoracis muscle of FR yaks is shown in Fig. 4. The results of TEM displayed that FR induced ERS on yak muscle, and dietary Gln supplementation relieved it (Fig. 4A). Genetic testing results suggested that compared with the Con group, FR significantly upregulated the transcriptional levels of ATF4, IRE1, XBP1, PERK, eIF2α, GRP78, and Chop (P < 0.001), but FR had no significant impact on the transcriptional level of ATF6 in yak longissimus thoracis muscle (P = 0.176) (Fig. 4B). While dietary Gln supplementation significantly downregulated the transcriptional levels of IRE1, XBP1, PERK, eIF2α, ATF4, GRP78, and Chop in yak muscle (P < 0.001). Similarly, dietary Gln supplementation relieved the increase of p-IRE1/IER1 and p-PERK/PERK protein expression levels induced by FR in yak muscle (P < 0.001; Fig. 4C and D). The immunofluorescence results displayed that FR improved GRP78 protein expression level in yak muscle, while dietary Gln supplementation relieved it (P = 0.001; Fig. 4E and F).

Fig. 4.

Fig. 4

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Effects of dietary Gln supplementation on endoplasmic reticulum stress (ERS) in the longissimus thoracis muscle of feed-restricted (FR) yaks. (A) The ultrastructure of yak muscle was observed by transmission electron microscope (TEM) (scale bars represent 5 μm). (B) ERS-related mRNA expression levels. (C and D) The expression and quantification of ERS-related proteins. (E and F) The immunofluorescence of GRP78 and its quantification results (scale bars represent 100 μm). Con, the yaks were fed the basal diet ad libitum during d 0 to 60; FR, the yaks were fed 50% dry matter intake (DMI) of the pre-feeding period during d 0 to 60; FR + Gln, the yaks were fed 50% DMI of the pre-feeding period during d 0 to 30, and were fed 50% DMI of the pre-feeding + 1% Gln during d 31 to 60. Con = control; FR + Gln = feed restriction + glutamine. Different lowercase letters above columns represent significant differences among treatments at P < 0.05, n = 6.

4. Discussion

The yak is one of the economically important species unique to the Qinghai-Tibet Plateau (Yi et al., 2022). Due to the low year-round temperatures in the region and the lack of forage during the cold season, yaks frequently experience hunger, leading to inhibited growth (Gao et al., 2022). Previous study in our laboratory found that dietary Gln supplementation effectively alleviated growth retardation of stunted yaks (Ma et al., 2021). In addition, FR decreased the average daily gain (ADG), pre-slaughter live weight, carcass weight, dressing percentage, net meat percentage, net meat weight, body fat weight, and meat-bone ratio, while dietary Gln supplementation effectively improved ADG, carcass weight, net meat weight, dressing percentage, and net meat percentage (Tables S6 and S7) (Yue et al., 2025a,b). In the yak longissimus thoracis muscle, FR inhibited Gln metabolism and induced oxidative stress, while dietary Gln supplementation effectively relieved them (Table S8 and Fig. S1) (Yue et al., 2025b). However, the influence of Gln on lipid metabolism in the yak longissimus thoracis muscle remains unknown. Yak meat is highly valued for its rich nutritional profile and contributes significantly to the livelihood of local herders (Wang et al., 2022). It has been shown that fat deposition can improve the tenderness and flavor in yak meat, thereby enhancing meat quality and economic value (Hu et al., 2021; Xiong et al., 2021). In beef, the IMF content is one of the important indicators influencing muscle quality (Yu et al., 2020). The ER is a primary site for lipid metabolism (Bartelt et al., 2018). The previous study demonstrated that starvation could lead to ERS and abnormal lipid metabolism (Islam et al., 2021; Yu et al., 2016). Besides, fatty acids are essential components of various lipids (Berman et al., 2015). Therefore, this study established a yak starvation model through FR and explored the effects of dietary Gln supplementation on lipid metabolism, fatty acid composition, and ERS in the longissimus thoracis muscle. The results showed that dietary Gln supplementation effectively alleviated the reduction in lipid deposition and PUFA levels, and ERS in longissimus thoracis muscle induced by FR.

4.1. Dietary Gln supplementation alleviated FR-induced decrease of serum biochemical indices of yaks

Serum biochemical indices can reflect the metabolic status of the organism, especially serum TG, TC, NEFA, HDL-C, and LDL-C levels, which explain the lipid metabolism in the body to a certain extent (Liu et al., 2021). A study in mice found that fasting significantly reduced the serum TG concentration and increased the NEFA concentration (Erickson and Anakk, 2018). In this research, feed restriction brought about similar effects. This indicates fat mobilization from adipose tissue. However, Gln only increased the TG concentration in serum of FR yaks. This may be because Gln inhibited the fat decomposition in the body.

4.2. Dietary Gln supplementation alleviated FR-induced change of fatty acid composition in the longissimus thoracis muscle of yaks

Fatty acids are divided into SFA, MUFA, and PUFA (Bhat and Fayaz, 2011). The PUFAs are beneficial for health, reducing the risk of heart disease, cancer, atherosclerosis, and inflammatory disorders (Pekkoh et al., 2022). It was reported that the fat of the body was decreased in worms fasted for 12 h (Li et al., 2020). In a study on neutrophils, Gln increased the PUFA/SFA and the level of UFA (Lagranha et al., 2008), which is similar to the present results. The present results showed that dietary Gln supplementation relieved the reduction in the levels of n-6 PUFA and PUFA induced by FR in yak muscle. Thus, these results indicate that dietary Gln supplementation can enhance the nutritional value in the longissimus thoracis muscle of starved yaks.

4.3. Dietary Gln supplementation alleviated FR-induced decrease of BT and IMF content in the longissimus thoracis muscle of yaks

Fat accumulation in beef is intimately connected to meat quality, and meat quality is closely linked to BT and IMF content (Wang et al., 2018). During starvation, fat is released from adipose tissue through lipolysis, where TGs are broken down into free fatty acids for energy use in skeletal muscles and other tissues (Huang et al., 2021). A study showed that starvation significantly decreased the BT and IMF content in the longissimus thoracis muscle of yaks (Yu et al., 2016). This experiment aligned with the previous results. In addition, it was also found that Gln could partially alleviate the decrease of BT and IMF content. This may be associated with the role of Gln in promoting lipogenesis (Cheng et al., 2022). This indicates that dietary Gln supplementation can increase the fat content to improve the longissimus thoracis muscle meat quality of starved yaks.

4.4. Dietary Gln supplementation alleviated FR-induced change of taste properties in the longissimus thoracis muscle of yaks

There is a strong relationship between meat quality and its flavor. Research indicated that IMF content could improve the tenderness and umami taste (Kim et al., 2022). The fatty acid composition in IMF could affect the flavor of muscle (Bhat and Fayaz, 2011). In these results, FR significantly decreased the NMS in the longissimus thoracis muscle. The results of changes in fatty acid composition and IMF content supported this finding. Besides, the amount of Gln is closely related to the preferred beef aroma and contributes to the umami flavor (Antonelo et al., 2020). Gln could convert into glutamate and aspartate, contributing to the umami intensity of meat (Kaczmarska et al., 2021). In these results, Gln alleviated the decrease of Gln and glutamate concentrations in yak longissimus thoracis muscle (Fig. S5 A and B). This may be another reason for the increase in NMS. These results indicated that dietary Gln supplementation can improve the edible quality in the longissimus thoracis muscle of starved yaks by enhancing its umami taste.

4.5. Dietary Gln supplementation alleviated FR-induced abnormal lipid metabolism in the longissimus thoracis muscle of yaks

The lipid metabolism pathway involves lipid synthesis for energy storage and cell membrane component creation, while lipid degradation releases stored energy (Yong et al., 2020). A protein related to fat synthesis, FAS, is regulated by the transcription factor SREBP-l (Lu et al., 2019). PPARα is mainly responsible for regulating fatty acid degradation, and PPARγ plays a significant role in regulating lipid storage (Olechnowicz et al., 2018). The present results showed that FR downregulated the transcriptional levels of ACC, FAS, PPARγ, and SREBP mRNA, and upregulated the transcriptional levels of PPARα, GATGL, and HSL mRNA in yak muscle, while dietary Gln supplementation alleviated them. These results indicated that dietary Gln supplementation alleviated the decrease of fat synthesis and the increase of fat degradation in yak muscle induced by FR. Furthermore, Gln provides carbon and nitrogen for lipid biosynthesis (Yu et al., 2023). During starvation, fat production and degradation are imbalanced, resulting in weight loss (Li et al., 2020), while Gln is used by cells as a source of energy or a nutrient substrate (Yu et al., 2023). It is believed that IMF deposition influences meat tenderness and taste in meat animals. Therefore, it is speculated that Gln might improve meat flavor by alleviating the decrease in fat deposition and the change of fatty acid composition in yak muscle induced by FR.

4.6. Dietary Gln supplementation alleviated FR-induced ERS in the longissimus thoracis muscle of yaks

Stress stimuli, such as oxidative stress or nutritional deprivation, usually disrupt cellular homeostasis, leading to unfolded or misfolded proteins that accumulate in the ER cavity (Jiao et al., 2022). During ERS, PERK separates from GRP78 and activates ATF4, which induces the transcription of genes associated with cell survival and pro-apoptotic factors like Chop (Zhou et al., 2019). The results of TEM showed that dietary Gln supplementation alleviated ERS induced by FR in yak muscle. The mRNA and protein results also showed that dietary Gln supplementation alleviated FR-induced ERS through IRE1/XBP1 and PERK/eIF2α/ATF4 pathways in yak muscle. A similar study found that starvation-induced ERS by improving the transcriptional level of XBP1 in dairy cow liver (Islam et al., 2021), and Gln inhibited ERS by decreasing the transcriptional levels of GRP78 and Chop in lung rats (Zhang et al., 2023). It indicated that dietary Gln supplementation alleviated ERS induced by FR in yak muscle. A key function of the ER is the synthesis and storage of lipids (Loi et al., 2019). ERS leads to abnormal lipid metabolism disorders.

5. Conclusion

In conclusion, FR reduced ADG, BT, IMF content, C18:2n6c, n-6 PUFA, total PUFA levels, and the PUFA/SFA ratio in yak longissimus thoracis muscle. Dietary Gln supplementation mitigated these negative effects by restoring ADG, IMF content, and the change of fatty acid composition, thereby improving the umami intensity of the longissimus thoracis muscle. Furthermore, dietary Gln supplementation also alleviated ERS through the IRE1/XBP1 and PERK/eIF2α/ATF4 pathways in yak longissimus thoracis muscle, which in turn alleviated lipid degradation and promoted lipid synthesis. These findings provide theoretical guidance for the use of Gln to enhance beef production and meat quality of yaks in the Qinghai-Tibet Plateau during the cold season.

Credit Author Statement

Ziqi Yue: Writing – original draft, Investigation, Formal analysis. Liyuan Shi: Investigation, Formal analysis. Rui Hu: Writing – review & editing, Project administration, Conceptualization. Zhisheng Wang: Writing – review & editing, Project administration, Conceptualization. Quanhui Peng: Methodology. Huawei Zou: Formal analysis. Jianxin Xiao: Formal analysis. Yahui Jiang: Investigation. Fali Wu: Investigation. Yiping Tang: Investigation.

Declaration of competing interest

We declare that we have no financial and personal relationships with other people or organizations that can inappropriately influence our work, and there is no professional or other personal interest of any nature or kind in any product, service and/or company that could be construed as influencing the content of this paper.

Acknowledgments

This work was supported by the Sichuan Science and Technology Program Grant (2021YFYZ0001) and China Agriculture (Beef Cattle/Yak) Research System of MOF and MARA (CARS-37).

Footnotes

Peer review under the responsibility of Chinese Association of Animal Science and Veterinary Medicine

Appendix A

Supplementary data to this article can be found online at https://doi.org/10.1016/j.aninu.2025.09.011.

Contributor Information

Rui Hu, Email: ruitianhu@yeah.net.

Zhisheng Wang, Email: zswangsicau@126.com.

Appendix A. Supplementary data

The following is the Supplementary data to this article:

Multimedia component 1
mmc1.docx (102.4KB, docx)

References

  1. Antonelo D.S., Cônsolo N.R., Gómez J.F., Beline M., Goulart R.S., RRPDS Corte, et al. Metabolite profile and consumer sensory acceptability of meat from lean Nellore and Angus × Nellore crossbreed cattle fed soybean oil. Food Res Int. 2020;132 doi: 10.1016/j.foodres.2020.109056. [DOI] [PubMed] [Google Scholar]
  2. Bartelt A., Widenmaier S.B., Schlein C., Johann K., Goncalves R.L., Eguchi K., et al. Brown adipose tissue thermogenic adaptation requires Nrf1-mediated proteasomal activity. Nat Med. 2018;24(3):292–303. doi: 10.1038/nm.4481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berman P., Meiri N., Colnago L.A., Moraes T.B., Linder C., Levi O., et al. Study of liquid-phase molecular packing interactions and morphology of fatty acid methyl esters (biodiesel) Biotechnol Biofuels. 2015;8:1–16. doi: 10.1186/s13068-014-0194-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bhat Z.F., Fayaz H. Prospectus of cultured meat–advancing meat alternatives. J Food Sci Technol. 2011;48:125–140. [Google Scholar]
  5. Cheng C., Geng F., Li Z., Zhong Y., Wang H., Cheng X., et al. Ammonia stimulates SCAP/Insig dissociation and SREBP-1 activation to promote lipogenesis and tumour growth. Nat Med. 2022;4(5):575–588. doi: 10.1038/s42255-022-00568-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Ministry of Agriculture of the People’s Republic of China . China Agriculture Press; Beijing, China: 2022. Determination of Acid Detergent Fiber (ADF) in Feeds (NY/T 1459-2022) [Google Scholar]
  7. China National Standard . Standards Press of China; Beijing: 2018. Determination of calcium in feeds. GB/T 6436-2018. [Google Scholar]
  8. China National Standard . Standards Press of China; Beijing: 2018. Determination of crube protein in feeds-Kjeldahl method. GB/T 6432-2018. [Google Scholar]
  9. China National Standard . Standards Press of China; Beijing: 2018. Determination of phosphorus in feeds-spectrophotometry. GB/T 6437-2018. [Google Scholar]
  10. China National Standard . Standards Press of China; Beijing: 2018. Operating procedure of livestock and poultry slaughtering-cattle. GB/T19477-2018. [Google Scholar]
  11. China National Standard . Standards Press of China; Beijing: 2022. Determination of neutral detergent fiber (NDF) in feeds. GB/T 20806-2022. [Google Scholar]
  12. Contreras O., Rossi F.M., Theret M. Origins, potency, and heterogeneity of skeletal muscle fibro-adipogenic progenitors—time for new definitions. Skeletal Muscle. 2021;11(1):16. doi: 10.1186/s13395-021-00265-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cruzat V., Macedo Rogero M., Noel Keane K., Curi R., Newsholme P. Glutamine: metabolism and immune function, supplementation and clinical translation. Nutrients. 2018;10(11):1564. doi: 10.3390/nu10111564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ebadi M., Mazurak V.C. Evidence and mechanisms of fat depletion in cancer. Nutrients. 2014;6(11):5280–5297. doi: 10.3390/nu6115280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Erickson H.L., Anakk S. Identification of IQ motif–containing GTPase-activating protein 1 as a regulator of long-term ketosis. JCI Insight. 2018;3(21) doi: 10.1172/jci.insight.99866. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Freeman M.R., Kim J., Lisanti M.P., Di Vizio D. A metabolic perturbation by U0126 identifies a role for glutamine in resveratrol-induced cell death. Cancer Biol Ther. 2011;12(11):966–977. doi: 10.4161/cbt.12.11.18136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gao J., Yang D., Sun Z., Niu J., Bao Y., Liu S., et al. Changes in blood metabolic profiles reveal the dietary deficiencies of specific nutrients and physiological status of grazing Yaks during the cold season in Qinghai province of China. Metabolites. 2022;12(8):738. doi: 10.3390/metabo12080738. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hu C., Ding L., Jiang C., Ma C., Liu B., Li D., et al. Effects of management, dietary intake, and genotype on rumen morphology, fermentation, and microbiota, and on meat quality in yaks and cattle. Front Nutr. 2021;8 doi: 10.3389/fnut.2021.755255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hu H., Chen L., Dai S., Li J., Bai X. Effect of glutamine on antioxidant capacity and lipid peroxidation in the breast muscle of heat-stressed broilers via antioxidant genes and HSP70 pathway. Animals. 2020;10(3):404. doi: 10.3390/ani10030404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Huang M., Lin Y., Wang L., You X., Wang S., Zhao J., et al. Adipose tissue lipolysis is regulated by PAQR11 via altering protein stability of phosphodiesterase 4D. Mol Metabol. 2021;47 doi: 10.1016/j.molmet.2021.101182. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Huo W., Weng K., Gu T., Luo X., Zhang Y., Zhang Y., et al. Effects of integrated rice-duck farming system on duck carcass traits, meat quality, amino acid, and fatty acid composition. Poult Sci. 2021;100(6) doi: 10.1016/j.psj.2021.101107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Islam M.A., Adachi S., Shiiba Y., Takeda K.-I., Haga S., Yonekura S. Effects of starvation-induced negative energy balance on endoplasmic reticulum stress in the liver of cows. Anim Biosci. 2021;35(1):22. doi: 10.5713/ab.21.0140. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Jiang Q., Chen J., Liu S., Liu G., Yao K., Yin Y. L-glutamine attenuates apoptosis induced by endoplasmic reticulum stress by activating the IRE1α-XBP1 axis in IPEC-J2: a novel mechanism of l-glutamine in promoting intestinal health. Int J Mol Sci. 2017;18(12):2617. doi: 10.3390/ijms18122617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Jiao D., Wang J., Yu W., Zhang K., Zhang N., Cao L., et al. Biocompatible reduced graphene oxide stimulated BMSCs induce acceleration of bone remodeling and orthodontic tooth movement through promotion on osteoclastogenesis and angiogenesis. Bioact Mater. 2022;15:409–425. doi: 10.1016/j.bioactmat.2022.01.021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kaczmarska K., Taylor M., Piyasiri U., Frank D. Flavor and metabolite profiles of meat, meat substitutes, and traditional plant-based high-protein food products available in Australia. Foods. 2021;10(4):801. doi: 10.3390/foods10040801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kim H.C., Baek K.H., Lee Y.E., Kang T., Kim H.J., Lee D., et al. Using 2D qNMR analysis to distinguish between frozen and frozen/thawed chicken meat and evaluate freshness. NPJ Sci Food. 2022;6(1):44. doi: 10.1038/s41538-022-00159-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kong S.-E., Hall J.C., Cooper D., Mccauley R.D. Starvation alters the activity and mRNA level of glutaminase and glutamine synthetase in the rat intestine. J Nutr Biochem. 2000;11(7–8):393–400. doi: 10.1016/s0955-2863(00)00095-4. [DOI] [PubMed] [Google Scholar]
  28. Lagranha C., Alba-Loureiro T., Martins E., Pithon-Curi T., Curi R. Neutrophil fatty acid composition: effect of a single session of exercise and glutamine supplementation. Amino Acids. 2008;35:243–245. doi: 10.1007/s00726-007-0561-9. [DOI] [PubMed] [Google Scholar]
  29. Li X., Yang Y., Zhu Y., Ben A., Qi J. A novel strategy for discriminating different cultivation and screening odor and taste flavor compounds in Xinhui tangerine peel using E-nose, E-tongue, and chemometrics. Food Chem. 2022;384 doi: 10.1016/j.foodchem.2022.132519. [DOI] [PubMed] [Google Scholar]
  30. Li X., Zhou D., Cai Y., Yu X., Zheng X., Chen B., et al. Endoplasmic reticulum stress inhibits AR expression via the PERK/eIF2α/ATF4 pathway in luminal androgen receptor triple-negative breast cancer and prostate cancer. NPJ Breast Cancer. 2022;8(1):2. doi: 10.1038/s41523-021-00370-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Li Y., Ding W., Li C.-Y., Liu Y. HLH-11 modulates lipid metabolism in response to nutrient availability. Nat Commun. 2020;11(1):5959. doi: 10.1038/s41467-020-19754-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Liu J., Song Y., Zhao Q., Wang Y., Li C., Zou L., et al. Effects of tartary buckwheat protein on gut microbiome and plasma metabolite in rats with high-fat diet. Foods. 2021;10(10):2457. doi: 10.3390/foods10102457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Loi M., Raimondi A., Morone D., Molinari M. ESCRT-III-driven piecemeal micro-ER-phagy remodels the ER during recovery from ER stress. Nat Commun. 2019;10(1):5058. doi: 10.1038/s41467-019-12991-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Lu J., Meng Z., Cheng B., Liu M., Tao S., Guan S. Apigenin reduces the excessive accumulation of lipids induced by palmitic acid via the AMPK signaling pathway in HepG2 cells. Exp Ther Med. 2019;18(4):2965–2971. doi: 10.3892/etm.2019.7905. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Ma J., Shah A., Wang Z., Hu R., Zou H., Wang X., et al. Dietary supplementation with glutamine improves gastrointestinal barrier function and promotes compensatory growth of growth-retarded yaks. Animal. 2021;15(2) doi: 10.1016/j.animal.2020.100108. [DOI] [PubMed] [Google Scholar]
  36. Manso H.E.C., Filho H.C.M., De Carvalho L.E., Kutschenko M., Nogueira E.T., Watford M. Glutamine and glutamate supplementation raise milk glutamine concentrations in lactating gilts. J Anim Sci Biotechnol. 2012;3:1–7. doi: 10.1186/2049-1891-3-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. NASEM (National Academy of Sciences) Nutrient requirements of beef cattle. 8th revised ed. National Academic Press; Washington (DC): 2016. [Google Scholar]
  38. Olechnowicz J., Tinkov A., Skalny A., Suliburska J. Zinc status is associated with inflammation, oxidative stress, lipid, and glucose metabolism. J Physiol Sci. 2018;68(1):19–31. doi: 10.1007/s12576-017-0571-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Pekkoh J., Phinyo K., Thurakit T., Lomakool S., Duangjan K., Ruangrit K., et al. Lipid profile, antioxidant and antihypertensive activity, and computational molecular docking of diatom fatty acids as ACE inhibitors. Antioxidants. 2022;11(2):186. doi: 10.3390/antiox11020186. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Qi M., Wang J., Tan B.E., Li J., Liao S., Liu Y., et al. Dietary glutamine, glutamate, and aspartate supplementation improves hepatic lipid metabolism in post-weaning piglets. Anim Nutr. 2020;6(2):124–129. doi: 10.1016/j.aninu.2019.12.002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Scollan N.D., Price E.M., Morgan S.A., Huws S.A., Shingfield K.J. Can we improve the nutritional quality of meat? Proc Nutr Soc. 2017;76(4):603–618. doi: 10.1017/S0029665117001112. [DOI] [PubMed] [Google Scholar]
  42. Tomaszewska E., Domaradzki P., Drabik K., Kasperek K., Puzio I., Burmańczuk A., et al. Long-term dietary glutamine supplementation modulates fatty acid profile and health indices in quail meat. Poult Sci. 2025 doi: 10.1016/j.psj.2025.105290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Wang Q., Dong K., Wu Y., An F., Luo Z., Huang Q., et al. Exploring the formation mechanism of off-flavor of irradiated yak meat based on metabolomics. Food Chem X. 2022;16 doi: 10.1016/j.fochx.2022.100494. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Wang Y., Zhang Y., Su X., Wang H., Yang W., Zan L. Cooperative and independent functions of the mir-23a∼ 27a∼ 24-2 cluster in bovine adipocyte adipogenesis. Int J Mol Sci. 2018;19(12):3957. doi: 10.3390/ijms19123957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Wei Y., Yang H., Wang Z., Zhao J., Qi H., Wang C., et al. Roughage biodegradation by natural co-cultures of rumen fungi and methanogens from Qinghai yaks. AMB Express. 2022;12(1):123. doi: 10.1186/s13568-022-01462-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Wilson M.D., Hunt I.G., Sawyer S.M., Kocharunchitt C., Li Z., Stanley R.A. Electronic tongue measurements as a predictor for sensory properties of vacuum-packed minced beef–A preliminary study. Meat Sci. 2025;220 doi: 10.1016/j.meatsci.2024.109705. [DOI] [PubMed] [Google Scholar]
  47. Xiong L., Pei J., Wang X., Guo S., Guo X., Yan P. Lipidomics and transcriptome reveal the effects of feeding systems on fatty acids in yak's meat. Foods. 2022;11(17):2582. doi: 10.3390/foods11172582. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Xiong L., Pei J., Wu X., Kalwar Q., Yan P., Guo X. Effect of gender to fat deposition in yaks based on transcriptomic and metabolomics analysis. Front Cell Dev Biol. 2021;9 doi: 10.3389/fcell.2021.653188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Yan S., Pei Y., Li J., Tang Z., Yang Y. Recent progress on circular RNAs in the development of skeletal muscle and adipose tissues of farm animals. Biomolecules. 2023;13(2):314. doi: 10.3390/biom13020314. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Yi S., Dai D., Wu H., Chai S., Liu S., Meng Q., et al. Dietary concentrate-to-forage ratio affects rumen bacterial community composition and metabolome of yaks. Front Nutr. 2022;9 doi: 10.3389/fnut.2022.927206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Yong C., Stewart G., Frezza C. Oncometabolites in renal cancer: Warburg's hypothesis re-examined. Nat Rev Nephrol. 2020;16(3):156–172. doi: 10.1038/s41581-019-0210-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Yu C., Wang N., Chen X., Jiang Y., Luan Y., Qin W., et al. A photodynamic-mediated glutamine metabolic intervention nanodrug for triple negative breast cancer therapy. Mater Today Bio. 2023;19 doi: 10.1016/j.mtbio.2023.100577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Yu X., Fang X., Gao M., Mi J., Zhang X., Xia L., et al. Isolation and identification of bovine preadipocytes and screening of MicroRNAs associated with adipogenesis. Animals. 2020;10(5):818. doi: 10.3390/ani10050818. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Yu X., Peng Q., Luo X., An T., Guan J., Wang Z. Effects of starvation on lipid metabolism and gluconeogenesis in yak. Asian-Australas J Anim Sci. 2016;29(11):1593. doi: 10.5713/ajas.15.0868. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Yue Z., Ke S., Shah A.M., Junmei W., Wang Z., Hu R., et al. Glutamine alleviates feed restriction-induced barrier function injury in yak rumen epithelium. Anim Nutr. 2025 doi: 10.1016/j.aninu.2025.09.006. [DOI] [Google Scholar]
  56. Yue Z., Ke S., Shi L., Hu R., Wang Z., Peng Q., et al. Effects of a diet containing glutamine on the slaughter performance, meat quality, and skeletal muscle fiber types of feed-restricted yaks. Meat Sci. 2025 doi: 10.1016/j.meatsci.2025.109945. [DOI] [PubMed] [Google Scholar]
  57. Zhang S., Li X., Yuan T., Guo X., Jin C., Jin Z., et al. Glutamine inhibits inflammation, oxidative stress, and apoptosis and ameliorates hyperoxic lung injury. J Physiol Biochem. 2023;79(3):613–623. doi: 10.1007/s13105-023-00961-5. [DOI] [PubMed] [Google Scholar]
  58. Zhang X., Wu R., Tian C., Wang W., Zhou L., Guo T., et al. GRP78 blockade overcomes intrinsic resistance to UBA1 inhibitor TAK-243 in glioblastoma. Cell Death Discov. 2022;8(1):133. doi: 10.1038/s41420-022-00950-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Zhou X.T., Pu Z.J., Liu L.X., Li G.P., Feng J.L., Zhu H.C., et al. Inhibition of autophagy enhances adenosine-induced apoptosis in human hepatoblastoma HepG2 cells. Oncol Rep. 2019;41(2):829–838. doi: 10.3892/or.2018.6899. [DOI] [PMC free article] [PubMed] [Google Scholar]

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