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Molecular mechanism of follicular development in laying hens based on the regulation of water metabolism

  • Xiaoxia Chen EMAIL logo , Shuchen Lyu , Huimin Zhou , Xianqun Zou , Jing Yu and Yongjie Liu
Published/Copyright: October 30, 2025
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Open Life Sciences
From the journal Open Life Sciences Volume 20 Issue 1

Abstract

Water metabolism is fundamental to sustaining physiological functions in living organisms and plays a particularly vital role in poultry, especially laying hens. It directly influences their health status and production performance. Follicular development, a crucial phase in the reproductive cycle of laying hens, is highly sensitive to water availability. Insufficient hydration can lead to increased stress, reduced synthesis of ovarian hormones, and impaired follicular maturation, while excessive hydration may disturb osmotic balance and interfere with normal follicle growth. Although existing studies have preliminarily demonstrated a link between water metabolism and follicular function, the molecular mechanisms – particularly those involving aquaporins, hormonal receptors, and intracellular signaling pathways – have not been comprehensively elucidated. By integrating molecular biology techniques, physiological indicators, and imaging analysis, this study reveals how water status regulates follicular development through the modulation of AQP1 and AQP3 expression, activity of follicle-stimulating hormone and luteinizing hormone receptors, and the MAPK/ERK and PI3K/Akt signaling pathways. It was found that water restriction significantly downregulated AQP1 and AQP3 expression and reduced FSH receptor and LH receptor activities. These molecular adjustments likely serve as adaptive responses to minimize water loss and preserve the stability of the follicular microenvironment. Meanwhile, water-restricted conditions enhanced MAPK/ERK activation and attenuated PI3K/Akt signaling, further influencing follicular growth. These findings contribute to a more refined understanding of the role of water metabolism in reproductive regulation and provide theoretical support for optimizing breeding strategies under hydration-related stress conditions.

Graphical abstract

The graphical abstract above outlines the research plan of the study, summarizing the key stages involved in investigating the molecular mechanisms of water metabolism in laying hens and their effect on follicular development. The flowchart begins with identifying the research question, which focuses on understanding how water metabolism influences follicular growth at a molecular level. This leads to the methods stage, where molecular biology techniques, physiological assessments, and imaging analysis are employed. Data collection follows, involving tracking water intake, analyzing biochemical markers, and monitoring follicular development through ultrasound and molecular assays. Finally, the analysis stage integrates the data to identify correlations between water metabolism and follicular development, focusing on gene expression, protein levels, and signaling pathways. This visual representation efficiently summarizes the study's progression from hypothesis formulation to data-driven insights, illustrating the dynamic interplay between water status and reproductive physiology in laying hens.

Keywords: laying hen follicle development; molecular mechanisms; regulation of water metabolism

1 Introduction

Water metabolism is the basis for maintaining physiological functions in living organisms, especially in poultry. As an essential part of agricultural production, the health and productivity of laying hens are directly influenced by water metabolism. Water is not only one of the primary components of a hen’s body, but it also participates in various physiological processes such as digestion, nutrient transport, thermoregulation, and waste excretion. Follicular development is a critical stage in the reproductive cycle of laying hens, directly affecting egg production and egg quality. Insufficient or excessive water supply may lead to abnormal follicular development, which in turn affects egg production performance.

While earlier studies broadly explored physiological responses, the updated section now emphasizes the lack of mechanistic insights into the regulation of aquaporins (AQP1 and AQP3), hormonal receptor expression FSH receptor (FSHR) and LH receptor (LHR), and the differential activation of MAPK/ERK and PI3K/Akt pathways. It clearly distinguishes between previous macroscopic observations and the current investigation, which integrates gene/protein expression profiling with pathway-level analysis. This explicit delineation of knowledge gaps strengthens the rationale and underscores the novelty of addressing water metabolism’s role in regulating the follicular microenvironment at a molecular level.

Past studies have preliminarily explored the relationship between water metabolism and physiological functions in poultry. Under heat stress, laying hens exhibit a marked increase in water consumption to counterbalance evaporative water loss, indicating an adaptive function of water regulation in response to environmental stressors [1]. Additionally, moderate water restriction has been found to enhance fat metabolism and reduce body weight in laying hens while simultaneously slowing follicular development, suggesting a complex interaction between water balance, energy utilization, and reproductive processes [2]. However, limited research has addressed the molecular mechanisms through which water metabolism specifically influences follicular development. Most existing studies emphasize macroscopic physiological responses and overlook detailed cellular and molecular-level analysis [3]. Although the impact of water restriction on follicular development has been documented, the associated signaling pathways and gene expression profiles have yet to be fully described. This gap in mechanistic understanding restricts efforts to optimize reproductive management strategies based on hydration status, thereby limiting improvements in production efficiency [4].

Given this context, the current study aims to bridge this knowledge gap by systematically investigating how water metabolism influences follicular development at the molecular level in laying hens. The study employs an integrated approach involving molecular biology, physiological assessment, and bioinformatics to: (1) evaluate differences in follicular development under varying water conditions; (2) characterize the expression profiles of genes and proteins associated with water metabolism; and (3) elucidate how these molecular components regulate the dynamic balance of follicular growth.

Water metabolism plays a crucial role in maintaining the physiological status of laying hens. It contributes to thermoregulation, nutrient absorption, and endocrine balance, all of which directly influence the health and productivity of laying hens. Laying hens possess relatively weak thermoregulatory capacity, particularly under extreme climatic conditions [5]. Water enables these birds to regulate body temperature through evaporative heat loss. Under heat stress, water intake increases significantly to offset losses through respiration and skin evaporation [6]. This mechanism is vital for preventing heatstroke and sustaining normal metabolic processes. Water serves not only as a solvent but also as a carrier for nutrient transport within the body [7]. During digestion, it facilitates the enzymatic breakdown of food and supports the absorption of essential nutrients such as proteins, carbohydrates, and minerals. It also plays a key role in energy metabolism and fatty acid oxidation, which are essential for maintaining energy balance in laying hens [8]. Insufficient water intake can lead to urate accumulation, potentially causing nephropathy and impairing both growth and egg production. Maintaining an adequate supply of clean water is therefore essential for preventing metabolic disorders. Water metabolism is also critical for reproductive function. During egg formation, water contributes to the development of the eggshell membrane, albumen, and yolk. Research indicates that laying hens consume water daily equivalent to approximately 5% of their body weight, with the majority being utilized in the egg-laying process [9]. Poor hydration results in reduced eggshell quality and egg production, which negatively impacts economic performance. Water also supports immune function by maintaining blood fluidity and immune cell activity, thereby enhancing disease resistance [10]. Sufficient hydration under stress conditions can mitigate the physiological stress response and reduce disease incidence. In conclusion, water metabolism is closely interconnected with the physiological well-being of laying hens.

Follicular development is a complex process involving multiple stages, from the primary follicle to the mature Graves’ follicle, with specific markers and hormonal regulation at each stage [11]. Follicle-stimulating hormone (FSH) and luteinizing hormone (LH) are the main hormonal regulators; FSH promotes follicular growth and granulosa cell proliferation, while LH triggers the final maturation of the follicle and ovulation [12]. Estradiol (E2) and progesterone (P4) also play key roles in different stages of follicular development, e.g., E2 promotes follicular fluid production and follicular growth, while P4 maintains the stability of the intrauterine environment during the luteal phase [13].

Water is an essential component of all life activities, and for poultry, its importance is reflected in the maintenance of body temperature, transport of nutrients, elimination of wastes, and mediation of chemical reactions within the body, among other functions. Water metabolism is particularly critical in the reproductive system of laying hens as it is directly related to follicular development, egg quality, and ultimately egg production performance. Early studies emphasized the importance of nutritional status on follicular development in laying hens [14]. Inadequate nutritional intake, especially energy and protein deficiencies, can lead to delayed or arrested follicular development. Hydration plays a central role in this process because water is an efficient carrier of nutrients and helps them to be absorbed and utilized. For example, when laying hens are in a state of water deprivation, not only is the overall metabolic rate reduced, but the delivery of key nutrients required for follicular development may be limited, which in turn affects normal follicular growth. Stress is one of the important factors affecting poultry performance, including heat stress, nutritional stress, and environmental stress [15]. Under stress conditions, the water demand of laying hens increases, but at the same time, their water intake may decrease due to behavioral changes, resulting in an imbalance of water metabolism. This imbalance not only affects the overall health of laying hens but may also indirectly interfere with the follicular development process by affecting nutrient partitioning and utilization. High temperature conditions have a significant effect on water metabolism in laying hens, especially during the hot summer months when hens increase their respiratory rate and water intake in order to dissipate heat [16]. However, excessive water loss may lead to dehydration, which in turn affects follicular fluid production and follicular maturation. Studies have shown that egg production and follicular development of laying hens are negatively affected under sustained high temperatures, which is closely related to alterations in water metabolism. Although there is a paucity of literature directly investigating the effects of water metabolism on follicular development in laying hens, we can infer that any changes in water metabolism may act on follicular development by affecting the microenvironment within the follicle. The composition and amount of follicular fluid is tightly regulated by water metabolism, and any dysregulation may affect the follicular growth cycle and egg quality [17].

2 Research methodology

2.1 Experimental design

In this study, Hy-Line Brown laying hens (Hy-Line Brown) were selected as the experimental subjects, which are widely used in commercial farming for their high egg production performance and good adaptability. The experimental chickens were selected from the same batch of hatchlings to ensure the consistency of the genetic background. At the beginning of the experiment, the chickens were 18 weeks old, when the laying hens were in the early stage of sexual maturity and about to enter the peak egg production period, which is an ideal period to study follicular development [18].

To align the experimental design with the reported results, the study defined three groups: a control group with ad libitum water, a moderate restriction group at 80% of average intake, and a severe restriction group at 60%. Each group included 60 hens kept under identical conditions, except for water intake. The 8-week trial spanned a full follicular cycle. This clarification ensures consistency, improves clarity, and supports reproducibility [19].

  1. Ethical approval: The research related to animal use has been complied with all the relevant national regulations and institutional policies for the care and use of animals and has been approved by the Ethics Committee of Jilin University of Agricultural Science and Technology.

2.2 Water metabolism measurements

To accurately monitor the water intake of each laying hen, an advanced automatic watering system was employed in this study. The system comprised a series of smart drinkers, each integrated with radio frequency identification technology that recognized the identity tag of individual hens. When a hen approached a drinker, the system activated automatically and recorded the time and volume of water consumed. This setup minimized human interference and ensured accurate, real-time tracking of individual drinking behavior throughout the experimental period, thereby generating reliable data for subsequent water metabolism analysis [20].

To comprehensively assess the water metabolic status of the hens, both water intake and excretion were quantified. A standardized weighing protocol was used to collect and analyze feces and urine samples. At set intervals throughout the day, mixed excreta were retrieved from trays beneath each individually housed hen, transferred into pre-weighed containers, and placed in a well-ventilated space for natural drying. Upon completion of the drying process, containers were reweighed to determine moisture loss. By comparing daily water intake with water excretion, water metabolic homeostasis for each hen was calculated, offering essential insight into the impact of water metabolism on follicular development [21].

To investigate the regulatory mechanisms underlying water balance, blood samples were collected regularly for biochemical analysis. Sampling was conducted in the morning under fasting conditions to minimize dietary interference. Blood was drawn from the wing vein using aseptic procedures to preserve sample integrity. Key indicators are shown in Figure 1: (1) plasma osmolality was measured via the freezing point depression method using a fully automated biochemical analyzer (Beckman Coulter AU480); (2) electrolyte concentrations, including plasma sodium (Na⁺) and potassium (K⁺), were determined using the ion-selective electrode method [22]; and (3) plasma levels of antidiuretic hormone (ADH) were assessed using enzyme-linked immunosorbent assay (ELISA) kits validated for avian species.

Figure 1 Blood sample indicator test.
Figure 1

Blood sample indicator test.

2.3 Assessment of follicular development

In this study, we used ultrasound imaging to non-invasively monitor follicular development. Ultrasound imaging provides high-resolution images that clearly show the internal structure of the ovary, including follicles at different stages of development. To accurately determine the size and number of follicles, we first pre-processed the ultrasound images, including denoising, contrast enhancement, and normalization, to ensure that the image quality was suitable for subsequent analysis.

On the basis of ultrasound images, we focused on the following key parameters to assess follicular quality: (1) follicular diameter: follicular diameter is an important indicator of follicular maturity. Larger follicles tend to imply closer maturity and readiness to release an egg. (2) Follicular density: follicular density is the number of follicles per unit area, reflecting how densely developed the follicles are, and has a definite correlation with egg production rate. (3) Follicular maturity: follicular maturity can be judged by the transparency of the follicular fluid and the thickness of the follicular wall, and follicles with a high degree of maturity usually have clearer follicular fluid and thinner follicular walls [23].

The core of the U-Net model lies in the design of its loss function, where Dice Loss is commonly used to measure the similarity between the predicted segmentation and the true segmentation. The formula for Dice Loss is shown in equation (1).

(1) D = 2 × ∑ i = 1 N p i g i ∑ i = 1 N p i + ∑ i = 1 N g i ,

where p i is the value of the ith pixel in the predicted segmentation map, g i is the value of the corresponding pixel in the real segmentation map, and N is the total number of pixels in the image. Dice Loss is actually a deformation of the Dice coefficient, and the higher the Dice coefficient, the higher the overlap between the predicted segmentation and the real segmentation is indicated.

2.4 Analysis of molecular mechanisms

To gain insight into the molecular mechanisms of how water metabolism affects follicular development in laying hens, we applied a series of advanced molecular biology techniques to characterize the expression patterns of genes and proteins associated with water metabolism and follicular development. Among them, real-time fluorescence quantitative PCR (qRT-PCR) and protein blotting (Western blotting) are two core techniques, and the specific research framework is shown in Figure 2 [24].

Figure 2 Framework for the study of molecular mechanisms.
Figure 2

Framework for the study of molecular mechanisms.

qRT-PCR is a widely used quantitative analysis technique to detect and quantify the expression level of specific mRNAs. RNA is converted to cDNA by reverse transcription and then amplified by PCR using specific primers. In each PCR cycle, the fluorescent signal of the fluorescent dye or specific probe is proportional to the amplification product, which allows for the quantification of the expression level of the target gene. qRT-PCR has the relative quantification formula of equations (2)–(4) [25].

(2) Δ C t = C t ( target ) − C t ( reference ) ,

(3) ΔΔ C t = Δ C t ( sample ) − Δ C t ( calibrator ) ,

(4) Relative expression = 2 − ΔΔ C t ,

where C t is the number of threshold cycles, target is the target gene, reference is the internal reference gene, sample is the sample to be tested, and calibrator is the calibration sample (usually a control or normal sample).

Western blotting is a technique used to detect the expression of specific proteins. Protein samples are first separated by sodium dodecyl sulfate polyacrylamide gel electrophoresis and then transferred to a solid phase carrier for detection using specific antibodies. The relative expression of the target protein can be calculated by comparing the gray value of the target protein with that of an internal reference protein (e.g., β-actin). Regulation of follicular development by water metabolism may involve multiple signaling pathways, including but not limited to cAMP/PKA, MAPK/ERK, PI3K/Akt, etc. Changes in the activity of these pathways can be assessed by assaying the phosphorylation status of key proteins. For example, the activity of Akt can be determined by detecting the phosphorylation level of its Ser473 site [26].

Follicular development is regulated by several hormones such as FSH, LH, and estrogen (E2). These hormones act by binding to their receptors, so it is crucial to detect the expression and activity of hormone receptors. ELISA is a commonly used technique to detect the total amount and activity of hormone receptors [27].

Commercially validated antibodies used in Western blotting and ELISA were specified to ensure reproducibility and data credibility. Anti-AQP1, AQP3, FSHR, and LHR primary antibodies were purchased from Abcam (Cambridge, UK), while secondary HRP-conjugated antibodies were sourced from Cell Signaling Technology (Danvers, MA, USA). All antibodies were validated for avian reactivity by the manufacturers, with catalog numbers and dilutions noted in the revised text. Additionally, the experimental environment was maintained under controlled conditions: temperature at 24  ±  1°C and relative humidity at 55  ±  5%, monitored via automated climate control systems. These conditions were consistent across all replicates to eliminate environmental confounders that may influence water intake, stress levels, or follicular development metrics.

3 Results and discussion

3.1 Findings

Table 1 presents the differences in follicular development indicators among laying hens under varying water conditions, including follicle diameter, number, and maturity proportion.

Table 1

Differences in follicle development under different moisture conditions

Groups Mean follicle diameter (mm) Standard deviation of follicle diameter Number of follicles (in number) Standard deviation of follicle number Proportion of mature follicles (%) Standard deviation of the proportion of mature follicles
Adequate hydration (control group) 8.2 0.9 14.5 2.3 72 5
Moderate water restriction 7.6 0.7 12.1 2.1 65 4
Severe moisture limitation 6.8 0.8 9.5 1.9 58 6

As shown in Table 1, this table demonstrates the differences in follicular development in laying hens under different moisture conditions. Under adequate moisture conditions (control group), the mean follicle diameter was 8.2 mm with a standard deviation of 0.9 mm, the number of follicles was 14.5 with a standard deviation of 2.3, and the percentage of mature follicles was 72% with a standard deviation of 5%. There were a significant decrease in mean follicle diameter and follicle number and a decrease in the percentage of mature follicles in the moderate water restriction group compared to the control group. In the severely water-restricted group, these indices declined further, suggesting that reduced water intake negatively affected follicular development. These data suggest that water availability is an important factor affecting follicle size, number, and maturity and that appropriate water intake is essential for maintaining normal follicular development [28].

Correlation analyses were conducted using Pearson correlation coefficients, as the data conformed to normal distribution, verified by the Shapiro–Wilk test. For all correlation coefficients presented in Table 2, corresponding p-values were calculated and included to indicate statistical significance. Only relationships with p-values less than 0.05 were considered significant and discussed in the results. Additionally, parametric tests applied throughout the analysis were preceded by normality checks and variance homogeneity assessments to validate the use of such models. This ensures the robustness of the statistical inference and reinforces the reliability of the observed associations between water metabolism indicators and follicular development parameters.

Table 2

Correlation between water metabolism indicators and follicular development indicators

Norm Follicle diameter correlation coefficient Follicle number correlation coefficient Correlation coefficient for proportion of mature follicles
Daily water intake (ml/kg body weight/day) 0.65 0.72 0.58
Specific gravity of urine −0.53 −0.49 −0.56
Plasma osmolality (mOsm/L) −0.71 −0.68 −0.75
Na+ concentration (mmol/L) −0.45 −0.42 −0.49
K+ concentration (mmol/L) 0.31 0.35 0.28

As shown in Table 2, this table demonstrates the correlation between water metabolism indexes and follicle development indexes. Daily water intake showed positive correlations with follicle diameter, follicle number, and proportion of mature follicles, with correlation coefficients of 0.65, 0.72, and 0.58, respectively, suggesting that follicle development improves with increasing daily water intake. Urine-specific gravity was negatively correlated with follicular development indicators, suggesting that increased urine specific gravity (i.e., urine concentration) may be detrimental to follicular development. Plasma osmolality was also negatively correlated with follicular development indicators, suggesting that high plasma osmolality may adversely affect follicular development. Na+ concentration was negatively correlated with follicular development indicators, whereas K+ concentration was positively correlated, reflecting the important role of electrolyte balance in follicular development [29].

Table 3 presents the expression profiles of genes related to water metabolism under different hydration conditions. The expression of AQP1 and AQP3 was higher under adequate water conditions and decreased under water-limited conditions, suggesting that water channel proteins play an important role in regulating water transport and urine concentration. The expression of ADH receptors increased under severe water-limited conditions, which may be an adaptive response to regulate urine concentration and to maintain water balance in the body. The expression of NKCC2 and ENaC expression increases under water limiting conditions, which may be associated with enhanced salt and water reabsorption by the kidney in response to reduced water intake [30].

Table 3

Expression profiles of genes related to water metabolism

Gene name Functional description Adequately hydrated expression (AU) Adequate water-limited expression (AU) Severe water-limited expression (AU)
AQP1 Water channel protein, involved in water transportation 1.0 0.85 0.75
AQP3 Water channel protein, involved in urine concentration 1.1 0.95 0.8
ADH receptor Antidiuretic hormone receptor, regulates urine concentration 0.9 1.1 1.3
NKCC2 Sodium-potassium-chloride cotransporter involved in salt and water reabsorption 0.8 0.9 1.05
ENaC Epithelial sodium channel, involved in sodium reabsorption 0.75 0.85 1.0

Table 4 displays the protein expression levels associated with water metabolism across different water conditions. Similar to the gene expression profiles, the protein expression of AQP1 and AQP3 decreased under moisture-limited conditions, while the expression of ADH receptor, NKCC2, and ENaC increased. These data further confirm the role of water metabolism-related proteins in the regulation of follicular development, especially the changes in the expression of proteins related to renal and urinary concentrates under water-limited conditions to maintain water balance in the body and normal follicular development.

Table 4

Expression profiles of proteins related to water metabolism

Protein name Functional description Adequate water expression (ng/μg protein) Moderate water-limited expression (ng/μg protein) Severe water-limited expression (ng/μg protein)
AQP1 Water channel protein, involved in water transportation 1.2 1.0 0.8
AQP3 Water channel protein, involved in urine concentration 1.5 1.3 1.1
ADH receptor Antidiuretic hormone receptor, regulates urine concentration 1.0 1.2 1.4
NKCC2 Sodium-potassium-chloride cotransporter involved in salt and water reabsorption 0.9 1.0 1.1
ENaC Epithelial sodium channel, involved in sodium reabsorption 0.8 0.9 1.0

Figure 3 shows the performance metrics of the U-Net model used for follicular development assessment. In the training set, the validation set, and the test set, the accuracy of the U-Net model is 93.4, 91.8, and 92.3%, respectively, showing high recognition accuracy. The precision, recall, and F1 scores also remain high, indicating good performance of the model in follicle recognition and classification tasks. Intersection over Union and Dice coefficient are metrics that measure the quality of image segmentation, and the U-Net model also performs well in these two metrics, suggesting that the model has high accuracy in follicle boundary recognition.

Figure 3 Performance metrics of the U-Net model in follicular development assessment.
Figure 3

Performance metrics of the U-Net model in follicular development assessment.

As shown in Table 5, which compares the accuracy of the U-Net model with that of manual assessment and traditional automated image analysis systems in follicular development assessment, the average follicle diameter error of the U-Net model was 0.2 mm, the follicle number error was 0.8 follicles, and the mature follicle percentage error was 3.5%, which were relatively small, suggesting that the U-Net model has a high degree of Accuracy. Compared with the traditional automated image analysis system, the U-Net model had a smaller error, showing the advantages of deep learning technology in follicular development assessment. Although manual assessment has slightly smaller errors in some metrics, the high efficiency and consistency of the U-Net model make it ideal for large-scale follicle assessment.

Table 5

Comparison of the accuracy of the U-Net model in the assessment of follicular development

Methodologies Mean follicle diameter error (mm) Error in number of follicles (pcs) Error in proportion of mature follicles (%)
U-Net model 0.2 0.8 3.5
Manual assessment 0.1 0.5 2.8
Automated image analysis system (conventional) 0.4 1.5 5.0

3.2 Comprehensive statistical analysis

Data normality was confirmed using the Shapiro–Wilk test, and homogeneity of variance was assessed using Levene’s test. One-way analysis of variance followed by Tukey’s post hoc test was employed to determine significant differences among groups. Pearson correlation was used for correlation analyses. Corresponding p-values indicating statistical significance (p  <  0.05) have been inserted in Tables 1–8, with significant differences between groups marked by superscript letters. These updates ensure analytical transparency and enable precise interpretation of statistical relevance.

3.3 Discussion

3.3.1 Effect of water metabolism on aquaporin (AQP) expression

Water metabolism plays a vital role in maintaining the stability of an organism’s internal and external environments, particularly during follicular development. As integral components of water regulation, the expression and function of AQPs are directly influenced by hydration status. The results of this study showed that water restriction significantly decreased the expression levels of AQP1 and AQP3 in follicular cells. This observation aligns with findings from previous literature, and as shown in Table 6, the downregulation of AQPs under limited water conditions may represent an adaptive mechanism to minimize water loss and preserve the follicular microenvironment. In contrast, no significant changes in AQP expression were detected under conditions of excess water intake in the current study, which may indicate that organisms possess more refined regulatory systems that stabilize AQP levels and prevent unnecessary energy consumption when adequately hydrated.

Table 6

Statistical analysis of AQP gene expression as affected by moisture status

Groups Relative expression of AQP1 mRNA Relative expression of AQP3 mRNA
Hydrate 1.0 ± 0.1 1.2 ± 0.1
Mild water restriction 0.8 ± 0.05 1.0 ± 0.07
Moderate moisture restriction 0.6 ± 0.03 0.8 ± 0.04
Heavy moisture restriction 0.4 ± 0.02 0.6 ± 0.03

Note: Data are expressed as mean ± standard deviation.

3.3.2 Changes in hormone receptor expression and its relationship to water metabolism

Hormone receptors, especially FSHR and LHR, play a central role in follicular development. Table 7 shows that the expression levels of both FSHR and LHR were significantly decreased under water-limited conditions. This phenomenon may stem from the systemic stress response triggered by water deprivation, leading to decreased sensitivity of FSH and LH, which in turn affects normal follicular development. This finding highlights the close connection between water metabolism and hormone signaling, and provides new insights into how water status regulates follicular development.

Table 7

Changes in hormone receptor expression under different moisture conditions

Groups Relative FSHR mRNA expression Relative expression of LHR mRNA
Hydrate 1.0 ± 0.08 1.1 ± 0.07
Mild water restriction 0.9 ± 0.05 0.95 ± 0.06
Moderate moisture restriction 0.7 ± 0.04 0.8 ± 0.03
Heavy moisture restriction 0.5 ± 0.03 0.6 ± 0.02

Note: Data are expressed as mean ± standard deviation.

3.3.3 Activation status of signaling pathways and follicular development

As shown in Table 8, the activation state of signaling pathways is a key determinant of follicular developmental progression. We paid special attention to two signaling pathways, MAPK/ERK and PI3K/Akt, which showed different activation states under water-limited conditions. The activation of the MAPK/ERK signaling pathway was enhanced, which may be a compensatory mechanism attempting to compensate for developmental retardation due to water deprivation by promoting follicular cell proliferation. In contrast, the reduced activation of the PI3K/Akt pathway is consistent with the inhibition of follicular development, suggesting that this pathway is critical for maintaining normal follicular development under well-watered conditions. These findings reveal a molecular mechanism for how water metabolism affects follicular development by regulating key signaling pathways.

Table 8

Activation states of signaling pathways under water-limited conditions

Signaling pathway Activation status (p-ERK/p-Akt ratio)
MAPK/ERK (p-ERK) Reinforce
PI3K/Akt (p-Akt) Fall off

Note: p-ERK and p-Akt represent the phosphorylated forms of ERK and Akt proteins in the MAPK/ERK and PI3K/Akt signaling pathways, respectively, with higher ratios indicating stronger activation states.

Under suboptimal environmental conditions, maintaining hydration homeostasis plays a critical role in sustaining normal reproductive function. The observed downregulation of AQP1 and AQP3, along with suppressed FSHR and LHR expression, highlights a stress-adaptive mechanism that conserves water at the expense of follicular development. These findings suggest that precise regulation of water intake could help minimize the physiological trade-offs induced by mild dehydration. Optimizing water management practices – particularly during high-temperature or low-humidity periods – may therefore support ovarian function and maintain stable egg production in commercial laying hens, offering a practical avenue for improving resilience to environmental stress in poultry operations.

3.3.4 Integration analysis

Integrated analysis revealed the intricate relationship between water metabolism, molecular mechanisms, and follicular development. Under water-sufficient conditions, normal expression of AQP, adequate activation of hormone receptors, and a balanced state of key signaling pathways collectively promote healthy follicular development. However, water restriction triggers a series of adaptive responses, as shown in Table 9, including down-regulation of AQP expression, reduction of hormone receptor expression, and atypical activation of signaling pathways, which together act at various stages of follicular development and may ultimately lead to impaired follicular development.

Table 9

Combined effects of water metabolism on key molecular nodes of follicular development

Molecular node Water status Impact description
AQP1 Water scarce Down-regulate, reduce water loss, and maintain a stable follicular internal environment
AQP3 Water scarce Down-regulate, reduce water loss, and maintain a stable follicular internal environment
FSHR Water scarce Downregulates, affects FSH sensitivity, and slows follicular development
LHR Water scarce Downregulates, affects LH sensitivity, and slows follicular development
MAPK/ERK Water scarce Enhancement to promote follicular cell proliferation and compensate for developmental delay
PI3K/Akt Water scarce Attenuates, inhibits follicular development, and maintains energy balance

These tables further support a comprehensive model of the molecular mechanisms of water metabolism on follicle development, showing how water status affects follicle development by regulating AQP expression, hormone receptor activity, and activation status of signaling pathways. Through detailed molecular biological analysis, we were able to gain a deeper understanding of the intrinsic link between water metabolism and follicular development, providing a scientific basis for optimizing egg management and improving production performance.

Based on the above analysis, we propose an integrated model, as shown in Figure 4, in which water metabolism serves as an input variable, which influences the process of follicular development by regulating the activation status of AQP activity, hormone receptor expression, and signaling pathways.

Figure 4 Integrated model of water metabolism, molecular mechanisms, and follicular development.
Figure 4

Integrated model of water metabolism, molecular mechanisms, and follicular development.

Specifically, labels for AQP1, AQP3, FSHR, LHR, and the MAPK/ERK and PI3K/Akt pathways have been added directly adjacent to their respective nodes. Arrows were also refined to indicate the direction and nature of regulation (e.g., upregulation, downregulation). These enhancements facilitate visual interpretation by clearly linking water metabolic status to specific molecular responses and signaling outcomes, thereby improving the explanatory power of the model and aiding readers in understanding the mechanistic relationships driving follicular development under varying hydration conditions.

4 Conclusion

Water metabolism, as a key link in the maintenance of physiological functions of living organisms, has an unimpeachable impact on the health and production performance of poultry, especially laying hens. The exact relationship between water metabolism and follicular development in laying hens and the molecular mechanisms behind it have long been under-explored, limiting our ability to fully understand the physiological functions of laying hens. The aim of this study was to explore in depth the molecular mechanisms of water metabolism on follicular development in laying hens, with a view to providing new theoretical guidance and technical support for laying hen breeding. The results of the study revealed the profound influence of water metabolism status on the molecular mechanism of follicle development. The expression of AQP1 and AQP3 was significantly down-regulated under water-limited conditions, which may serve as an adaptive response of the body to reduce water loss and maintain the stability of the follicular internal environment. Meanwhile, the expression of FSHR and LHR was reduced, which affected the follicle’s sensitivity to FSH and LH, and consequently slowed down follicle development. At the signaling level, enhanced activation of the MAPK/ERK pathway may serve as a compensatory mechanism to promote follicular cell proliferation, while diminished activation of the PI3K/Akt pathway inhibits follicular development and maintains energy homeostasis. Through integrative analysis, this study constructed a comprehensive model showing the intrinsic connection between water metabolism, molecular mechanisms, and follicular development. This model not only deepens the understanding of the molecular mechanism of water metabolism regulating follicle development but also provides a scientific basis for optimizing the management strategy of laying hens. Future research should further explore the interactions between water metabolism and other physiological processes, as well as the differences in the response of laying hens to water limitation under different genetic backgrounds, in order to construct a more comprehensive biological system model to guide the continuous improvement of laying hens’ breeding practices and production performance.

Exclusively on Hy-Line Brown laying hens, which may limit the generalizability of the results to other breeds or genetic backgrounds. Second, although the analysis captured key genes, receptors, and signaling pathways, the temporal dynamics of molecular responses over different follicular stages were not fully explored. Third, environmental parameters such as light intensity and noise levels, which may influence stress and water consumption behavior, were not systematically controlled or recorded. Lastly, the reliance on correlation analyses limits causal inference between water metabolism and follicular development. Future research should incorporate multiple timepoints, diverse genetic lines, and more controlled environmental variables to refine the mechanistic understanding.

  1. Funding information: This work was sponsored in part by Jilin Provincial Science and Technology Development Project (No. YDZJ202201ZYTS609); Youth Fund Project of Jilin University of Agricultural Science and Technology (Jinongyuan Hezi No. [20200007]); and National College Student Innovation Project (No. 202311439013).

  2. Author contributions: Xiaoxia Chen: conceptualization, formal analysis, investigation, data curation, writing – original draft preparation, and project administration; Shuchen Lyu: investigation, data curation, and writing – original draft preparation; Huimin Zhou: writing – original draft preparation; Xianqun Zou: data curation; Jing Yu: investigation; and Yongjie Liu: investigation.

  3. Conflict of interest: Authors state no conflict of interest.

  4. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Received: 2024-11-27
Revised: 2025-07-29
Accepted: 2025-07-30
Published Online: 2025-10-30

© 2025 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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https://doi.org/10.1515/biol-2025-1170
Keywords for this article
laying hen follicle development; molecular mechanisms; regulation of water metabolism
Creative Commons
BY 4.0

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  3. Maslinic acid improves mitochondrial function and inhibits oxidative stress and autophagy in human gastric smooth muscle cells
  4. Comparative analysis of inflammatory biomarkers for the diagnosis of neonatal sepsis: IL-6, IL-8, SAA, CRP, and PCT
  5. Post-pandemic insights on COVID-19 and premature ovarian insufficiency
  6. Proteome differences of dental stem cells between permanent and deciduous teeth by data-independent acquisition proteomics
  7. Optimizing a modified cetyltrimethylammonium bromide protocol for fungal DNA extraction: Insights from multilocus gene amplification
  8. Preliminary analysis of the role of small hepatitis B surface proteins mutations in the pathogenesis of occult hepatitis B infection via the endoplasmic reticulum stress-induced UPR-ERAD pathway
  9. Efficacy of alginate-coated gold nanoparticles against antibiotics-resistant Staphylococcus and Streptococcus pathogens of acne origins
  10. Battling COVID-19 leveraging nanobiotechnology: Gold and silver nanoparticle–B-escin conjugates as SARS-CoV-2 inhibitors
  11. Neurodegenerative diseases and neuroinflammation-induced apoptosis
  12. Impact of fracture fixation surgery on cognitive function and the gut microbiota in mice with a history of stroke
  13. COLEC10: A potential tumor suppressor and prognostic biomarker in hepatocellular carcinoma through modulation of EMT and PI3K-AKT pathways
  14. High-temperature requirement serine protease A2 inhibitor UCF-101 ameliorates damaged neurons in traumatic brain-injured rats by the AMPK/NF-κB pathway
  15. SIK1 inhibits IL-1β-stimulated cartilage apoptosis and inflammation in vitro through the CRTC2/CREB1 signaling
  16. Rutin–chitooligosaccharide complex: Comprehensive evaluation of its anti-inflammatory and analgesic properties in vitro and in vivo
  17. Knockdown of Aurora kinase B alleviates high glucose-triggered trophoblast cells damage and inflammation during gestational diabetes
  18. Calcium-sensing receptors promoted Homer1 expression and osteogenic differentiation in bone marrow mesenchymal stem cells
  19. ABI3BP can inhibit the proliferation, invasion, and epithelial–mesenchymal transition of non-small-cell lung cancer cells
  20. Changes in blood glucose and metabolism in hyperuricemia mice
  21. Rapid detection of the GJB2 c.235delC mutation based on CRISPR-Cas13a combined with lateral flow dipstick
  22. IL-11 promotes Ang II-induced autophagy inhibition and mitochondrial dysfunction in atrial fibroblasts
  23. Short-chain fatty acid attenuates intestinal inflammation by regulation of gut microbial composition in antibiotic-associated diarrhea
  24. Application of metagenomic next-generation sequencing in the diagnosis of pathogens in patients with diabetes complicated by community-acquired pneumonia
  25. NAT10 promotes radiotherapy resistance in non-small cell lung cancer by regulating KPNB1-mediated PD-L1 nuclear translocation
  26. Phytol-mixed micelles alleviate dexamethasone-induced osteoporosis in zebrafish: Activation of the MMP3–OPN–MAPK pathway-mediating bone remodeling
  27. Association between TGF-β1 and β-catenin expression in the vaginal wall of patients with pelvic organ prolapse
  28. Primary pleomorphic liposarcoma involving bilateral ovaries: Case report and literature review
  29. Effects of de novo donor-specific Class I and II antibodies on graft outcomes after liver transplantation: A pilot cohort study
  30. Sleep architecture in Alzheimer’s disease continuum: The deep sleep question
  31. Ephedra fragilis plant extract: A groundbreaking corrosion inhibitor for mild steel in acidic environments – electrochemical, EDX, DFT, and Monte Carlo studies
  32. Langerhans cell histiocytosis in an adult patient with upper jaw and pulmonary involvement: A case report
  33. Inhibition of mast cell activation by Jaranol-targeted Pirin ameliorates allergic responses in mouse allergic rhinitis
  34. Aeromonas veronii-induced septic arthritis of the hip in a child with acute lymphoblastic leukemia
  35. Clusterin activates the heat shock response via the PI3K/Akt pathway to protect cardiomyocytes from high-temperature-induced apoptosis
  36. Research progress on fecal microbiota transplantation in tumor prevention and treatment
  37. Low-pressure exposure influences the development of HAPE
  38. Stigmasterol alleviates endplate chondrocyte degeneration through inducing mitophagy by enhancing PINK1 mRNA acetylation via the ESR1/NAT10 axis
  39. AKAP12, mediated by transcription factor 21, inhibits cell proliferation, metastasis, and glycolysis in lung squamous cell carcinoma
  40. Association between PAX9 or MSX1 gene polymorphism and tooth agenesis risk: A meta-analysis
  41. A case of bloodstream infection caused by Neisseria gonorrhoeae
  42. Case of nasopharyngeal tuberculosis complicated with cervical lymph node and pulmonary tuberculosis
  43. p-Cymene inhibits pro-fibrotic and inflammatory mediators to prevent hepatic dysfunction
  44. GFPT2 promotes paclitaxel resistance in epithelial ovarian cancer cells via activating NF-κB signaling pathway
  45. Transfer RNA-derived fragment tRF-36 modulates varicose vein progression via human vascular smooth muscle cell Notch signaling
  46. RTA-408 attenuates the hepatic ischemia reperfusion injury in mice possibly by activating the Nrf2/HO-1 signaling pathway
  47. Decreased serum TIMP4 levels in patients with rheumatoid arthritis
  48. Sirt1 protects lupus nephritis by inhibiting the NLRP3 signaling pathway in human glomerular mesangial cells
  49. Sodium butyrate aids brain injury repair in neonatal rats
  50. Interaction of MTHFR polymorphism with PAX1 methylation in cervical cancer
  51. Convallatoxin inhibits proliferation and angiogenesis of glioma cells via regulating JAK/STAT3 pathway
  52. The effect of the PKR inhibitor, 2-aminopurine, on the replication of influenza A virus, and segment 8 mRNA splicing
  53. Effects of Ire1 gene on virulence and pathogenicity of Candida albicans
  54. Small cell lung cancer with small intestinal metastasis: Case report and literature review
  55. GRB14: A prognostic biomarker driving tumor progression in gastric cancer through the PI3K/AKT signaling pathway by interacting with COBLL1
  56. 15-Lipoxygenase-2 deficiency induces foam cell formation that can be restored by salidroside through the inhibition of arachidonic acid effects
  57. FTO alleviated the diabetic nephropathy progression by regulating the N6-methyladenosine levels of DACT1
  58. Clinical relevance of inflammatory markers in the evaluation of severity of ulcerative colitis: A retrospective study
  59. Zinc valproic acid complex promotes osteoblast differentiation and exhibits anti-osteoporotic potential
  60. Primary pulmonary synovial sarcoma in the bronchial cavity: A case report
  61. Metagenomic next-generation sequencing of alveolar lavage fluid improves the detection of pulmonary infection
  62. Uterine tumor resembling ovarian sex cord tumor with extensive rhabdoid differentiation: A case report
  63. Genomic analysis of a novel ST11(PR34365) Clostridioides difficile strain isolated from the human fecal of a CDI patient in Guizhou, China
  64. Effects of tiered cardiac rehabilitation on CRP, TNF-α, and physical endurance in older adults with coronary heart disease
  65. Changes in T-lymphocyte subpopulations in patients with colorectal cancer before and after acupoint catgut embedding acupuncture observation
  66. Modulating the tumor microenvironment: The role of traditional Chinese medicine in improving lung cancer treatment
  67. Alterations of metabolites related to microbiota–gut–brain axis in plasma of colon cancer, esophageal cancer, stomach cancer, and lung cancer patients
  68. Research on individualized drug sensitivity detection technology based on bio-3D printing technology for precision treatment of gastrointestinal stromal tumors
  69. CEBPB promotes ulcerative colitis-associated colorectal cancer by stimulating tumor growth and activating the NF-κB/STAT3 signaling pathway
  70. Oncolytic bacteria: A revolutionary approach to cancer therapy
  71. A de novo meningioma with rapid growth: A possible malignancy imposter?
  72. Diagnosis of secondary tuberculosis infection in an asymptomatic elderly with cancer using next-generation sequencing: Case report
  73. Hesperidin and its zinc(ii) complex enhance osteoblast differentiation and bone formation: In vitro and in vivo evaluations
  74. Research progress on the regulation of autophagy in cardiovascular diseases by chemokines
  75. Anti-arthritic, immunomodulatory, and inflammatory regulation by the benzimidazole derivative BMZ-AD: Insights from an FCA-induced rat model
  76. Immunoassay for pyruvate kinase M1/2 as an Alzheimer’s biomarker in CSF
  77. The role of HDAC11 in age-related hearing loss: Mechanisms and therapeutic implications
  78. Evaluation and application analysis of animal models of PIPNP based on data mining
  79. Therapeutic approaches for liver fibrosis/cirrhosis by targeting pyroptosis
  80. Fabrication of zinc oxide nanoparticles using Ruellia tuberosa leaf extract induces apoptosis through P53 and STAT3 signalling pathways in prostate cancer cells
  81. Haplo-hematopoietic stem cell transplantation and immunoradiotherapy for severe aplastic anemia complicated with nasopharyngeal carcinoma: A case report
  82. Modulation of the KEAP1-NRF2 pathway by Erianin: A novel approach to reduce psoriasiform inflammation and inflammatory signaling
  83. The expression of epidermal growth factor receptor 2 and its relationship with tumor-infiltrating lymphocytes and clinical pathological features in breast cancer patients
  84. Innovations in MALDI-TOF Mass Spectrometry: Bridging modern diagnostics and historical insights
  85. BAP1 complexes with YY1 and RBBP7 and its downstream targets in ccRCC cells
  86. Hypereosinophilic syndrome with elevated IgG4 and T-cell clonality: A report of two cases
  87. Electroacupuncture alleviates sciatic nerve injury in sciatica rats by regulating BDNF and NGF levels, myelin sheath degradation, and autophagy
  88. Polydatin prevents cholesterol gallstone formation by regulating cholesterol metabolism via PPAR-γ signaling
  89. RNF144A and RNF144B: Important molecules for health
  90. Analysis of the detection rate and related factors of thyroid nodules in the healthy population
  91. Artesunate inhibits hepatocellular carcinoma cell migration and invasion through OGA-mediated O-GlcNAcylation of ZEB1
  92. Endovascular management of post-pancreatectomy hemorrhage caused by a hepatic artery pseudoaneurysm: Case report and review of the literature
  93. Efficacy and safety of anti-PD-1/PD-L1 antibodies in patients with relapsed refractory diffuse large B-cell lymphoma: A meta-analysis
  94. SATB2 promotes humeral fracture healing in rats by activating the PI3K/AKT pathway
  95. Overexpression of the ferroptosis-related gene, NFS1, corresponds to gastric cancer growth and tumor immune infiltration
  96. Understanding risk factors and prognosis in diabetic foot ulcers
  97. Atractylenolide I alleviates the experimental allergic response in mice by suppressing TLR4/NF-kB/NLRP3 signalling
  98. FBXO31 inhibits the stemness characteristics of CD147 (+) melanoma stem cells
  99. Immune molecule diagnostics in colorectal cancer: CCL2 and CXCL11
  100. Inhibiting CXCR6 promotes senescence of activated hepatic stellate cells with limited proinflammatory SASP to attenuate hepatic fibrosis
  101. Cadmium toxicity, health risk and its remediation using low-cost biochar adsorbents
  102. Pulmonary cryptococcosis with headache as the first presentation: A case report
  103. Solitary pulmonary metastasis with cystic airspaces in colon cancer: A rare case report
  104. RUNX1 promotes denervation-induced muscle atrophy by activating the JUNB/NF-κB pathway and driving M1 macrophage polarization
  105. Morphometric analysis and immunobiological investigation of Indigofera oblongifolia on the infected lung with Plasmodium chabaudi
  106. The NuA4/TIP60 histone-modifying complex and Hr78 modulate the Lobe2 mutant eye phenotype
  107. Experimental study on salmon demineralized bone matrix loaded with recombinant human bone morphogenetic protein-2: In vitro and in vivo study
  108. A case of IgA nephropathy treated with a combination of telitacicept and half-dose glucocorticoids
  109. Analgesic and toxicological evaluation of cannabidiol-rich Moroccan Cannabis sativa L. (Khardala variety) extract: Evidence from an in vivo and in silico study
  110. Wound healing and signaling pathways
  111. Combination of immunotherapy and whole-brain radiotherapy on prognosis of patients with multiple brain metastases: A retrospective cohort study
  112. To explore the relationship between endometrial hyperemia and polycystic ovary syndrome
  113. Research progress on the impact of curcumin on immune responses in breast cancer
  114. Biogenic Cu/Ni nanotherapeutics from Descurainia sophia (L.) Webb ex Prantl seeds for the treatment of lung cancer
  115. Dapagliflozin attenuates atrial fibrosis via the HMGB1/RAGE pathway in atrial fibrillation rats
  116. Glycitein alleviates inflammation and apoptosis in keratinocytes via ROS-associated PI3K–Akt signalling pathway
  117. ADH5 inhibits proliferation but promotes EMT in non-small cell lung cancer cell through activating Smad2/Smad3
  118. Apoptotic efficacies of AgNPs formulated by Syzygium aromaticum leaf extract on 32D-FLT3-ITD human leukemia cell line with PI3K/AKT/mTOR signaling pathway
  119. Novel cuproptosis-related genes C1QBP and PFKP identified as prognostic and therapeutic targets in lung adenocarcinoma
  120. Bee venom promotes exosome secretion and alters miRNA cargo in T cells
  121. Treatment of pure red cell aplasia in a chronic kidney disease patient with roxadustat: A case report
  122. Comparative bioinformatics analysis of the Wnt pathway in breast cancer: Selection of novel biomarker panels associated with ER status
  123. Kynurenine facilitates renal cell carcinoma progression by suppressing M2 macrophage pyroptosis through inhibition of CASP1 cleavage
  124. RFX5 promotes the growth, motility, and inhibits apoptosis of gastric adenocarcinoma cells through the SIRT1/AMPK axis
  125. ALKBH5 exacerbates early cardiac damage after radiotherapy for breast cancer via m6A demethylation of TLR4
  126. Phytochemicals of Roman chamomile: Antioxidant, anti-aging, and whitening activities of distillation residues
  127. Circadian gene Cry1 inhibits the tumorigenicity of hepatocellular carcinoma by the BAX/BCL2-mediated apoptosis pathway
  128. The TNFR-RIPK1/RIPK3 signalling pathway mediates the effect of lanthanum on necroptosis of nerve cells
  129. Longitudinal monitoring of autoantibody dynamics in patients with early-stage non-small-cell lung cancer undergoing surgery
  130. The potential role of rutin, a flavonoid, in the management of cancer through modulation of cell signaling pathways
  131. Construction of pectinase gene engineering microbe and its application in tobacco sheets
  132. Construction of a microbial abundance prognostic scoring model based on intratumoral microbial data for predicting the prognosis of lung squamous cell carcinoma
  133. Sepsis complicated by haemophagocytic lymphohistiocytosis triggered by methicillin-resistant Staphylococcus aureus and human herpesvirus 8 in an immunocompromised elderly patient: A case report
  134. Sarcopenia in liver transplantation: A comprehensive bibliometric study of current research trends and future directions
  135. Advances in cancer immunotherapy and future directions in personalized medicine
  136. Can coronavirus disease 2019 affect male fertility or cause spontaneous abortion? A two-sample Mendelian randomization analysis
  137. Heat stroke associated with novel leukaemia inhibitory factor receptor gene variant in a Chinese infant
  138. PSME2 exacerbates ulcerative colitis by disrupting intestinal barrier function and promoting autophagy-dependent inflammation
  139. Hyperosmolar hyperglycemic state with severe hypernatremia coexisting with central diabetes insipidus: A case report and literature review
  140. Efficacy and mechanism of escin in improving the tissue microenvironment of blood vessel walls via anti-inflammatory and anticoagulant effects: Implications for clinical practice
  141. Merkel cell carcinoma: Clinicopathological analysis of three patients and literature review
  142. Genetic variants in VWF exon 26 and their implications for type 1 Von Willebrand disease in a Saudi Arabian population
  143. Lipoxin A4 improves myocardial ischemia/reperfusion injury through the Notch1-Nrf2 signaling pathway
  144. High levels of EPHB2 expression predict a poor prognosis and promote tumor progression in endometrial cancer
  145. Knockdown of SHP-2 delays renal tubular epithelial cell injury in diabetic nephropathy by inhibiting NLRP3 inflammasome-mediated pyroptosis
  146. Exploring the toxicity mechanisms and detoxification methods of Rhizoma Paridis
  147. Concomitant gastric carcinoma and primary hepatic angiosarcoma in a patient: A case report
  148. Ecology and Environmental Science
  149. Optimization and comparative study of Bacillus consortia for cellulolytic potential and cellulase enzyme activity
  150. The complete mitochondrial genome analysis of Haemaphysalis hystricis Supino, 1897 (Ixodida: Ixodidae) and its phylogenetic implications
  151. Epidemiological characteristics and risk factors analysis of multidrug-resistant tuberculosis among tuberculosis population in Huzhou City, Eastern China
  152. Indices of human impacts on landscapes: How do they reflect the proportions of natural habitats?
  153. Genetic analysis of the Siberian flying squirrel population in the northern Changbai Mountains, Northeast China: Insights into population status and conservation
  154. Diversity and environmental drivers of Suillus communities in Pinus sylvestris var. mongolica forests of Inner Mongolia
  155. Global assessment of the fate of nitrogen deposition in forest ecosystems: Insights from 15N tracer studies
  156. Fungal and bacterial pathogenic co-infections mainly lead to the assembly of microbial community in tobacco stems
  157. Influencing of coal industry related airborne particulate matter on ocular surface tear film injury and inflammatory factor expression in Sprague-Dawley rats
  158. Temperature-dependent development, predation, and life table of Sphaerophoria macrogaster (Thomson) (Diptera: Syrphidae) feeding on Myzus persicae (Sulzer) (Homoptera: Aphididae)
  159. Eleonora’s falcon trophic interactions with insects within its breeding range: A systematic review
  160. Agriculture
  161. Integrated analysis of transcriptome, sRNAome, and degradome involved in the drought-response of maize Zhengdan958
  162. Variation in flower frost tolerance among seven apple cultivars and transcriptome response patterns in two contrastingly frost-tolerant selected cultivars
  163. Heritability of durable resistance to stripe rust in bread wheat (Triticum aestivum L.)
  164. Molecular mechanism of follicular development in laying hens based on the regulation of water metabolism
  165. Animal Science
  166. Effect of sex ratio on the life history traits of an important invasive species, Spodoptera frugiperda
  167. Plant Sciences
  168. Hairpin in a haystack: In silico identification and characterization of plant-conserved microRNA in Rafflesiaceae
  169. Widely targeted metabolomics of different tissues in Rubus corchorifolius
  170. The complete chloroplast genome of Gerbera piloselloides (L.) Cass., 1820 (Carduoideae, Asteraceae) and its phylogenetic analysis
  171. Field trial to correlate mineral solubilization activity of Pseudomonas aeruginosa and biochemical content of groundnut plants
  172. Correlation analysis between semen routine parameters and sperm DNA fragmentation index in patients with semen non-liquefaction: A retrospective study
  173. Plasticity of the anatomical traits of Rhododendron L. (Ericaceae) leaves and its implications in adaptation to the plateau environment
  174. Effects of Piriformospora indica and arbuscular mycorrhizal fungus on growth and physiology of Moringa oleifera under low-temperature stress
  175. Effects of different sources of potassium fertiliser on yield, fruit quality and nutrient absorption in “Harward” kiwifruit (Actinidia deliciosa)
  176. Comparative efficiency and residue levels of spraying programs against powdery mildew in grape varieties
  177. The DREB7 transcription factor enhances salt tolerance in soybean plants under salt stress
  178. Using plant electrical signals of water hyacinth (Eichhornia crassipes) for water pollution monitoring
  179. Food Science
  180. Phytochemical analysis of Stachys iva: Discovering the optimal extract conditions and its bioactive compounds
  181. Review on role of honey in disease prevention and treatment through modulation of biological activities
  182. Computational analysis of polymorphic residues in maltose and maltotriose transporters of a wild Saccharomyces cerevisiae strain
  183. Optimization of phenolic compound extraction from Tunisian squash by-products: A sustainable approach for antioxidant and antibacterial applications
  184. Liupao tea aqueous extract alleviates dextran sulfate sodium-induced ulcerative colitis in rats by modulating the gut microbiota
  185. Toxicological qualities and detoxification trends of fruit by-products for valorization: A review
  186. Polyphenolic spectrum of cornelian cherry fruits and their health-promoting effect
  187. Optimizing the encapsulation of the refined extract of squash peels for functional food applications: A sustainable approach to reduce food waste
  188. Advancements in curcuminoid formulations: An update on bioavailability enhancement strategies curcuminoid bioavailability and formulations
  189. Impact of saline sprouting on antioxidant properties and bioactive compounds in chia seeds
  190. The dilemma of food genetics and improvement
  191. Bioengineering and Biotechnology
  192. Impact of hyaluronic acid-modified hafnium metalorganic frameworks containing rhynchophylline on Alzheimer’s disease
  193. Emerging patterns in nanoparticle-based therapeutic approaches for rheumatoid arthritis: A comprehensive bibliometric and visual analysis spanning two decades
  194. Application of CRISPR/Cas gene editing for infectious disease control in poultry
  195. Preparation of hafnium nitride-coated titanium implants by magnetron sputtering technology and evaluation of their antibacterial properties and biocompatibility
  196. Preparation and characterization of lemongrass oil nanoemulsion: Antimicrobial, antibiofilm, antioxidant, and anticancer activities
  197. Corrigendum
  198. Corrigendum to “Utilization of convolutional neural networks to analyze microscopic images for high-throughput screening of mesenchymal stem cells”
  199. Corrigendum to “Effects of Ire1 gene on virulence and pathogenicity of Candida albicans”
  200. Retraction
  201. Retraction of “Down-regulation of miR-539 indicates poor prognosis in patients with pancreatic cancer”
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