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Article

Accumulation Characteristics of Trace Elements in Leafy Vegetables with Different Heavy Metal Tolerances Under Cd and as Stress

by
Yuan Meng
1,2,*,
Liang Zhang
1,
Liping Li
3,
Linquan Wang
4,
Yongfu Wu
1,
Tao Zeng
1,
Haiqing Shi
5,
Zeli Chang
1,
Qian Shi
1 and
Jian Ma
1
1
School of Agriculture and Bioengineering, Longdong University, Qingyang 745000, China
2
Gansu Key Laboratory of Conservation and Utilization of Biological Resources and Ecological Restoration in Longdong, Qingyang 745000, China
3
School of Environmental Engineering, Henan University of Technology, Zhengzhou 450001, China
4
College of Natural Resources and Environment, Northwest A&F University, Yangling 712100, China
5
School of Resources and Environment, Northeast Agricultural University, Harbin 150030, China
*
Author to whom correspondence should be addressed.
Agronomy 2025, 15(8), 1790; https://doi.org/10.3390/agronomy15081790
Submission received: 25 May 2025 / Revised: 7 July 2025 / Accepted: 18 July 2025 / Published: 25 July 2025
(This article belongs to the Special Issue Heavy Metal Pollution and Prevention in Agricultural Soils)
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Abstract

This study investigates growth responses, heavy metal (Cd, As) uptake, translocation, and mineral nutrient regulation in leafy vegetables with varying heavy metal tolerance, addressing the threat posed by combined Cd and As pollution. Three high-tolerance, four moderate-tolerance, and one sensitive leafy vegetable were grown in Cd+As-contaminated hydroponics. Post-harvest yields and concentrations of Cd, As, and trace elements were assessed. Results showed that (1) compared with single heavy metal treatments, the combination of Cd and As significantly increased the translocation factor of Cd in black bean sprouts and white radish sprouts by up to 83.83% and 503.2%; (2) changes in mineral nutrient concentrations in leafy vegetables were similar between single and combined heavy metal stresses, but the regulatory patterns varied among different leafy vegetable species; (3) under Cd/As exposure, high-tolerance leafy vegetables (e.g., pak choi) had strong heavy metal accumulation abilities, and heavy metal stress positively regulated mineral elements in their roots; In contrast, sensitive leafy vegetables (e.g., pea sprouts) often exhibited suppressed mineral element content in their roots, which was a result of their strategy to reduce heavy metal uptake. These results offer key insights into resistance mechanisms against combined heavy metal pollution in leafy vegetables, supporting phytoremediation efforts and safe production.

1. Introduction

The acceleration of the global industrialization process and frequent agricultural activities have led to heavy metal pollution becoming a significant issue in soil and water environments, which urgently needs to be addressed. It is reported that approximately 14% to 17% of farmland soil globally, encompassing nearly 242 million hectares, is contaminated with heavy metals, and there exists the issue of multi-metal co-contamination [1]. Especially in industrial and agricultural regions of China, rapid industrialization and urbanization have exacerbated the problem of soil heavy metal pollution [2,3]. Cadmium (Cd) and arsenic (As), as representative heavy metal pollutants, pose severe challenges to crop growth and food safety due to their high toxicity, ease of accumulation, and difficulty in degradation [4]. Leafy vegetables are a crucial component of the human daily diet. Studying their heavy metal accumulation characteristics and intrinsic regulatory mechanisms is not only relevant to vegetable quality and safety but also crucial for safeguarding public health and preventing the risk of heavy metal exposure. In recent years, research on heavy metal pollution in leafy vegetables has gradually increased, revealing differences in heavy metal accumulation in different vegetables and their potential risks to human health. Studies have shown that the levels of heavy metal accumulation in some vegetables sold in the market have exceeded the safety limits set by the WHO and FAO [5,6]. This exceeding phenomenon not only affects the edibility and safety of vegetables but may also pose significant health risks to consumers.
Currently, some progress has been made in research on the response and regulatory mechanisms of leafy vegetables to heavy metal stress. Plants typically cope with the toxicity of single heavy metal stress through complex physiological and molecular mechanisms. For instance, plants can mitigate heavy metal toxicity by chelating and sequestering heavy metal ions, regulating metal uptake and transport, and enhancing antioxidant mechanisms [7,8]. However, combined pollution with Cd and As may lead to increased levels of reactive oxygen species (ROS) in plants, causing greater damage to cell membranes and other cellular structures. Meanwhile, it may affect plant metabolism and signaling through different pathways. Therefore, there is an urgent need for in-depth research to reveal the interactions of these heavy metals under combined pollution conditions and their comprehensive effects on plants.
This paper delves into the following scientific question: “Are there differences in the mineral nutrition regulation mechanisms of leafy vegetable crops under single and combined pollution conditions of cadmium (Cd) and arsenic (As) and their correlation with heavy metal tolerance?” Based on this core question, we have constructed the following scientific hypothetical framework: When leafy vegetable crops are subjected to single and combined stresses of Cd and As, their mineral nutrition regulation mechanisms are similar and significantly correlated with heavy metal tolerance. High-tolerance varieties may maintain physiological homeostasis by enhancing mineral nutrition regulation, whereas sensitive varieties may reduce mineral nutrition absorption to decrease heavy metal uptake. Through meticulous experimental design and data analysis, this study aims to validate the aforementioned hypotheses and deepen our understanding of the response mechanisms of leafy vegetable crops to heavy metal stress.
Given the above background, this study selected three high-tolerance leafy vegetable species (pak choi, snow cabbage, Takaicai), four moderately tolerant species (Youmaicai, water spinach, black bean sprouts, and white radish sprouts), and one sensitive species (pea sprouts) as research objects. A hydroponic experiment was conducted to simulate environmental conditions of combined Cd and As pollution, systematically studying the growth response, heavy metal uptake and transport characteristics, and mineral nutrition regulatory mechanisms of these leafy vegetables under heavy metal stress. This study achieved breakthroughs and innovations in the following aspects. Based on the tolerance and transport characteristics of leafy vegetables to Cd and As, it revealed different nutrient regulation patterns exhibited by different types of leafy vegetables under heavy metal stress, further elucidating the core role of mineral nutrition in regulating heavy metal accumulation in leafy vegetables. This provides a new perspective for a deeper understanding of the response mechanisms of different leafy vegetable varieties to heavy metal stress.

2. Materials and Methods

2.1. Vegetables

The experiment was conducted between March and May 2023 in the Heavy Metal Pollution Prevention and Remediation Laboratory of the School of Agriculture and Bioengineering, Longdong University. The tested materials included three high-tolerance leafy vegetable species (pak choi, snow cabbage, Takaicai), four moderately tolerant species (Youmaicai, water spinach, black bean sprouts, and white radish sprouts), and one sensitive species (pea sprouts). All seeds (Table 1) were purchased from Longdong Agricultural Materials Mall in Qingyang City, Gansu Province, China.

2.2. Hydroponic Experiment

Hydroponic solution [9,10]: The modified 1/2 Hoagland’s nutrient solution contained 0.1 mM NH4H2PO4, 0.505 mM KNO3, 0.15 mM Ca(NO3)2, 0.1 mM MgSO4, 1.0 µM FeSO4, 0.91 µM MnCl2, 0.03 µM CuSO4, 0.16 µM ZnSO4, 4.63 µM H3BO3, 0.06 µM H2MoO4, and 0.81 µM Na2EDTA.
Heavy metal solution: CdCl2 and NaAsO2 were used to provide Cd and As elements.
EDTA-Na2 (ethylenediaminetetraacetic acid disodium salt) solution (concentration of 20 mmol/L): EDTA-Na2 was used to wash the roots to remove surface-attached metal ions.
Management of the hydroponic experiment: Depending on the thickness of the seed coat, seeds were soaked in water for 5–12 h before being sown in covered seedling trays. After 7–14 days of germination, when the seeds had developed four leaves, they were transplanted into hydroponic tanks. The hydroponic tanks had dimensions of 53.3 cm in length, 34.3 cm in width, and a volume of 9 L, with a nutrient solution depth of approximately 5 cm. The tanks were covered with a 2 cm thick foam board as a planting board, with 24 evenly spaced planting holes. The nutrient solution level in the tanks was controlled to be approximately 3 cm below the planting board, allowing part of the roots to be exposed to the air. During the entire growth period, the pH of the solution was maintained within the range of 6.0–6.5, and a small oxygen supply device was used to oxygenate the hydroponic nutrient solution for 1 h each day. The hydroponic experimental conditions were set to a photoperiod of 16 h/8 h (light/dark) with a light intensity of 20,000 lx.
Experimental treatment plan: After the leafy vegetables matured (approximately 60 days), each plant was transferred to a 300 mL black conical flask. A total of 14 treatments were set up, as shown in Table 2. Each treatment had 6 to 8 replicates. According to the Chinese soil standard (GB 15618-2018) [11], when the pH value exceeds 7.5, the concentration of cadmium (Cd) should not exceed 0.6 ppm, and the concentration of arsenic (As) should not exceed 25 ppm. In this hydroponic study, we selected a Cd concentration range of 1–20 ppm and a broader As concentration range of 10–200 ppm, aiming to evaluate the tolerance of leafy vegetables to heavy metal stress across a wider concentration spectrum, up to the level where a 50% reduction in fresh weight was observed. In this endeavor, we sought to provide new insights into the underlying mechanisms of stress tolerance.
The exact time of heavy metal addition was recorded, and the experiment was terminated 96 h after stress exposure. The plants were harvested for measurement. After heavy metal stress treatment, the roots of the leafy vegetables were first soaked in a 20 mM Na2-EDTA root-washing solution for 30 min to remove residual heavy metals from the roots [12]. Then, they were soaked and rinsed in distilled water twice for 30 min each. After drying with paper towels, the plants were cut at the stem base using plastic scissors and divided into shoot and root parts. The samples were placed in envelopes and dried in an oven at 65 °C.

2.3. Data Processing

The translocation factor (TF-X) for an element was the ratio between shoot concentration and root concentration of this element in one vegetable. A one-way ANOVA and multiple comparisons were utilized to assess the significance of differences between the measured data. GraphPad Prism 9.5.1 was used for graphical representation. Treatments 1–14 involved measuring the fresh weight, dry weight, and water content of leafy vegetables, which were used for the analysis of fresh weight (Section 3.1) and water content of leafy vegetables under Cd/As treatments (Section 3.2). Treatments 1, 3, 5, 8, 10, and 12 involved measuring the Cd, As, Ca, Mg, Fe, Mn, Cu, and Zn contents of leafy vegetables, which were used to analyze the heavy metal content of leafy vegetables under Cd/As treatments, the translocation factor of heavy metals from roots to shoots (Section 3.3), mineral nutrition regulation, and the interactions between mineral nutrients (Section 3.4).

2.4. Sample Element Analysis

To determine the concentrations of Cd, As, calcium (Ca), magnesium (Mg), iron (Fe), manganese (Mn), copper (Cu), and zinc (Zn) in the samples, an acid digestion method using HNO3-HClO4 was employed, followed by measurements using an atomic absorption spectrophotometer (Hitachi Z2000, Tokyo, Japan) and an atomic fluorescence spectrophotometer (AFS-930 dual-channel atomic fluorescence spectrophotometer, Beijing, China) [13,14]

3. Results

3.1. Yield

Tolerant and Sensitive Leafy Vegetables: Vegetable yields are presented in Figure 1. There were no significant differences in the fresh weights of the shoots and roots of pak choi, snow cabbage, and Takaicai under various treatments. Figure 1D, with p < 0.05 (n = 6), indicates that the shoot fresh weight of pea sprouts was significantly higher under the CK treatment than under Cd4As2, Cd2As4, Cd2As2, As5, As4, and As1 treatments; it was also significantly higher under the Cd1 treatment than under Cd4As2, Cd2As4, Cd2As2, As5, As4, and As1 treatments; and under the Cd2 treatment, it was significantly higher than under Cd4As2 and Cd2As4 treatments. However, there were no significant differences in the root fresh weight of pea sprouts among the treatments.
Moderately Tolerant Leafy Vegetables: As can be seen from Figure 2, except for black soybean sprouts, the water content in the roots of the other tested leafy vegetables did not change with heavy metal treatment. Figure 2A, with p < 0.05 (n = 6), shows that the shoot fresh weight of water spinach was significantly higher under the As1 treatment than under Cd4As2, Cd2As4, Cd2As2, As5, As4, As3, Cd5, and Cd4 treatments; it was significantly lower under the As4 treatment than under Cd1 and CK treatments; and under the Cd2As4 treatment, it was significantly lower than under the CK treatment. According to Figure 2B, with p < 0.05 (n = 6), the shoot fresh weight of Black Bean Sprouts was significantly higher under the Cd2 treatment than under Cd4As2, Cd2As4, Cd2As2, As5, As4, As3, As2, and Cd5 treatments. It was significantly lower under the As3 treatment than under Cd3 and CK treatments; under the As3 treatment, the root fresh weight was significantly higher than under Cd4As2, Cd2As4, As5, and As4 treatments. Figure 2C, with p < 0.05 (n = 6), reveals that the shoot fresh weight of white radish sprouts was significantly higher under the Cd2 treatment than under Cd2As4, As5, As4, As2, and Cd5 treatments; it was significantly higher under the CK treatment than under As5, As4, and Cd5 treatments; and under the As5 treatment, it was significantly lower than under the Cd1 treatment. Figure 2D, with p < 0.05 (n = 6), indicates that the shoot fresh weight of Youmaicai was significantly higher under the Cd3 treatment than under the As5 treatment.
Summary: Pak choi, snow cabbage, and Takaicai exhibited no significant differences in shoot and root fresh weights under Cd and As treatments, demonstrating high tolerance and belonging to the high-tolerance leafy vegetable category; The fresh weight of pea sprouts was significantly lower than that of the control or other treatments under multiple conditions, showing relatively low tolerance and belonging to the low-tolerance leafy vegetable category. The remaining leafy vegetables (Youmaicai, water spinach, black bean sprouts, and white radish sprouts) belonged to the medium-tolerance category.

3.2. Moisture Content of Leafy Vegetables Under Cd/as Treatments

Tolerant and Sensitive Leafy Vegetables: From Figure 3 and Figure 4, it can be observed that the moisture content of the tested leafy vegetables was not affected by the experimental treatments. As indicated by Figure 3A, where p < 0.05 (n = 3), under As4 treatment, the water content in the aerial parts of pak choi was significantly lower than that under Cd2As2, Cd3, Cd2, Cd1, and CK treatments. According to Figure 3B, where p < 0.05 (n = 3), under As5 treatment, the water content in the aerial parts of snow cabbage was significantly lower than that under Cd3, Cd2, and Cd1 treatments. Figure 3C shows no significant difference in the water content of both aerial parts and roots of Takaicai under different treatments. From Figure 3D, where p < 0.05 (n = 3), under Cd3 treatment, the water content in the aerial parts of pea sprouts was significantly higher than that under Cd4As2, As4, As3, As2, and As1 treatments; under As4 treatment, its aerial water content was significantly lower than that under Cd4, Cd5, and As5 treatments.
Moderately Tolerant Leafy Vegetables: Figure 4A indicates no significant difference in the water content of both aerial parts and roots of water spinach under various treatments. As per Figure 4B, where p < 0.05 (n = 3), under Cd4As2 treatment, the water content in the aerial parts of black bean sprouts was significantly lower than that under As5, Cd3, Cd2, Cd1, and CK treatments; under Cd2As4 treatment, its aerial water content was significantly lower than that under Cd3, Cd2, Cd1, and CK treatments; and under As2 treatment, its aerial water content was also significantly lower than that under CK treatment. Figure 4C, where p < 0.05 (n = 3), shows that under Cd2As4 treatment, the aerial water content of white radish sprouts was significantly lower than that under Cd3, Cd2, Cd1, and CK treatments; under As5 treatment, its aerial water content was significantly lower than that under Cd2 and Cd1 treatments; and under Cd4As2 treatment, its aerial water content was significantly lower than that under Cd2 treatment. Figure 4D, where p < 0.05 (n = 3), reveals that under Cd4As2 treatment, the water content in the aerial parts of Youmaicai was significantly lower than that under Cd2, Cd1, and CK treatments; under Cd2As4 treatment, its aerial water content was significantly lower than that under Cd2 and Cd3 treatments; and under As5 treatment, its aerial water content was significantly lower than that under Cd3, Cd2, Cd1, and CK treatments.
Summary: The water content in the aerial parts of tolerant leafy vegetables (pak choi, snow cabbage) showed a decreasing trend only under arsenic (As) treatment. For Takaicai and water spinach, its aerial parts and roots showed no significant difference in water content under Cd and As treatments. Moderately tolerant leafy vegetables (Youmaicai, black bean sprouts, and white radish sprouts) were more sensitive to Cd and As treatments, with their aerial water content significantly decreased under specific treatments. Meanwhile, sensitive leafy vegetable (pea sprouts) exhibited a positive response to Cd treatment (increased water content) and a negative response to As treatment (decreased water content). However, the root water content of these tested leafy vegetables generally remained stable.

3.3. Accumulation and Translocation of Heavy Metals in Leafy Vegetables

As shown in Table 3, the shoot and root Cd concentrations of four-season creamy pak choi and white radish sprouts were higher than those of other leafy vegetables. Willow-leaf water spinach had the lowest shoot Cd and As concentrations, while pea sprouts and black bean sprouts had the lowest root Cd and As concentrations. The shoot and root As concentrations of white radish sprouts were higher than those of other leafy vegetables. Thai fragrant Youmaicai had the lowest TF-Cd, while black bean sprouts had the highest TF-Cd. Pea sprouts had the highest TF-As, while small eight-leaf Takaicai and willow-leaf water spinach had the lowest TF-As.
Based on the experimental results and the summarized characteristics of heavy metal absorption and translocation, the leafy vegetables can be classified as follows. (1) Accumulation Type: four-season creamy pak choi belongs to the Cd accumulation type (high Cd concentrations in both shoots and roots), while white radish sprouts are the Cd-As accumulation type. (2) Avoidance Type: pea sprouts and willow-leaf water spinach are Cd-As avoidance types (low Cd and As concentrations in both shoots and roots). (3) Translocation Type: pea sprouts and black bean sprouts belong to the Cd-As translocation type (high translocation coefficients from roots to shoots), while white radish sprouts are the Cd translocation type. (4) Root Accumulation Type: small eight-leaf Takaicai belongs to the As root accumulation type, and Thai fragrant Youmaicai belongs to the Cd root accumulation type (low shoot Cd concentration but high root concentration, with poor translocation ability from roots to shoots).

3.3.1. Vegetable Cd Contents

As shown in Figure 5A,C, with p < 0.05 (n = 3), under Cd4 treatment, the Cd content in the aboveground parts of white radish sprouts was significantly higher than that in willow-leaf water spinach and Thai fragrant Youmaicai. However, under Cd2 and combined Cd and As exposure, there were no significant differences among these eight leafy vegetables. This indicates that under high Cd concentration treatment, white radish sprouts exhibited stronger Cd absorption capacity in their aboveground parts, whereas under combined pollution or low Cd concentration treatment, the differences among leafy vegetables were insignificant. According to Figure 5B,D, with p < 0.05 (n = 3), under Cd2 treatment, the Cd content in the roots of four-season creamy pak choi was significantly higher than that in Jiutouniao snow cabbage and pea sprouts. Under Cd4 treatment, there were no significant differences among these eight leafy vegetables. Under combined Cd and As exposure, the Cd content in the roots of four-season creamy pak choi was significantly higher than that in Jiutouniao snow cabbage, small eight-leaf Takaicai, and pea sprouts. This suggests that under combined pollution conditions, four-season creamy pak choi exhibits enhanced Cd accumulation capacity in its roots, with a specific increase rate of 55.02%.

3.3.2. Vegetable as Contents

As illustrated in Figure 6A,C, with p < 0.05 (n = 3), under As2 and As4 treatments, the As content in the aboveground parts of white radish sprouts was significantly higher than that in willow-leaf water spinach, black bean sprouts, and Thai fragrant Youmaicai. Under As2 treatment, the aboveground As content of Thai fragrant Youmaicai and black bean sprouts was significantly higher than that of willow-leaf water spinach. Under As4 treatment, the aboveground As content of black bean sprouts was significantly higher than that of willow-leaf water spinach, and the aboveground As content of Jiutouniao snow cabbage was significantly higher than that of pea sprouts. Under combined Cd and As exposure, the aboveground As content of white radish sprouts was significantly higher than that of willow-leaf water spinach and Thai fragrant Youmaicai, while the aboveground As content of black bean sprouts was higher than that of willow-leaf water spinach. This indicates that white radish sprouts exhibit strong As absorption capacity in their aboveground parts, regardless of whether the pollution is from As alone or from combined Cd-As pollution.
From Figure 6B,D, with p < 0.05 (n = 3), under As4 treatment, the As content in the roots of four-season creamy pak choi was significantly higher than that in pea sprouts, and the As content in the roots of white radish sprouts was significantly higher than that in the other seven leafy vegetables. Under combined Cd and As exposure, the As content in the roots of white radish sprouts was significantly higher than that in willow-leaf water spinach and black bean sprouts, while the As content in the roots of four-season creamy pak choi and small eight-leaf Takaicai was significantly higher than that in pea sprouts. Under As2 treatment, there were no significant differences among these eight leafy vegetables. This demonstrates that under combined pollution conditions, the As accumulation capacity in the roots of four-season creamy pak choi (with an increase rate of 34.96%), white radish sprouts (with an increase rate of 117.73%), and small eight-leaf Takaicai (with an increase rate of 129.52%) is enhanced.

3.3.3. Heavy Metal Translocation Factor

As shown in Figure 7A,C, where p < 0.05 (n = 3), under Cd4 treatment, the TF-Cd (translocation factor for Cd) of small eight-leaf Takaicai was significantly higher than that of Jiutouniao snow cabbage and pea sprouts. For the combined Cd and As treatment, the TF-Cd of black bean sprouts and white radish sprouts was significantly higher than that of willow-leaf water spinach and Thai fragrant Youmaicai. However, under Cd2 treatment, there were no significant differences in TF-Cd among different leafy vegetables. This indicates that under combined pollution conditions, the Cd translocation ability of black bean sprouts and white radish sprouts was enhanced, with an increase ratio of 83.83% and 503.2%, respectively.
As illustrated in Figure 7B,D, where p < 0.05 (n = 3), under As2 treatment, the TF-As (translocation factor for As) of pea sprouts was significantly higher than that of four-season creamy pak choi, Jiutouniao snow cabbage, and small eight-leaf Takaicai. The TF-As of black bean sprouts was also significantly higher than that of willow-leaf water spinach and Thai fragrant Youmaicai. Under As4 treatment, the TF-As of pea sprouts was significantly higher than that of four-season creamy pak choi and small eight-leaf Takaicai, while the TF-As of black bean sprouts was significantly higher than that of white radish sprouts and Thai fragrant Youmaicai. For the combined Cd and As treatment, the TF-As of pea sprouts was significantly higher than that of four-season creamy pak choi, Jiutouniao snow cabbage, and small eight-leaf Takaicai, and the TF-As of black bean sprouts was significantly higher than that of willow-leaf water spinach, white radish sprouts, and Thai fragrant Youmaicai. This suggests that both pea sprouts and black bean sprouts exhibit strong As translocation ability, regardless of whether the pollution is solely As or a combination of Cd and As.

3.4. Mineral Nutrient Regulation Under Cd/as Stress

3.4.1. Mineral Nutrient Concentration

The concentration range of Mg in the whole plants of the eight tested leafy vegetables was 1.060 to 72.079 g kg−1, with an average of 22.020 g kg−1; the concentration range of Ca was 4.502 to 49.358 g kg−1, with an average of 20.186 g kg−1; the concentration range of Fe was 0.045 to 2.034 g kg−1, with an average of 0.350 g kg−1; the concentration range of Mn was 9.631 to 301.577 mg kg−1, with an average of 87.401 mg kg−1; the concentration range of Zn was 11.364 to 227.124 mg kg−1, with an average of 45.839 mg kg−1; and the concentration range of Cu was 1.770 to 48.657 mg kg−1, with an average of 8.649 mg kg−1.
Under single Cd, single As, and combined Cd-As stress treatments, we illustrated the effects of heavy metal stress on the absorption and distribution of mineral nutrients in leafy vegetables (Figure 8). The results are analyzed as follows.
Compared with the control group (CK), under single Cd, single As, and combined Cd-As stress treatments, the same leafy vegetable species exhibited consistent trends in their response to heavy metal stress, as reflected in changes in mineral element concentrations and translocation factors (see Figure 8, note 3). This indicates that the regulatory mechanisms of mineral nutrient ions in the same leafy vegetable species are similar when facing both single and combined heavy metal stresses; however, different leafy vegetable species display distinct nutrient regulation patterns. This provides important clues for exploring the mechanisms of leafy vegetable resistance to combined heavy metal pollution stress, suggesting that the regulatory mechanisms of leafy vegetables’ resistance to heavy metal stress are variety-specific.
Single heavy metal stress and combined pollution stress had a promoting effect on the mineral element content in the roots of four-season creamy pak choi (Cd-accumulator; tolerant type) but exhibited an inhibitory effect on pea sprouts (Cd-excluder; sensitive type). This discovery reveals a certain pattern between the ability of leafy vegetables to absorb Cd and the regulation of mineral elements in their roots: namely, the stronger the Cd-accumulation ability, the stronger the positive regulatory effect on mineral elements in the roots of leafy vegetables.
The mineral nutrition level of white radish sprouts (Cd-As accumulator; Cd translocator) was least affected under different heavy metal treatments, with the exception of inhibited Zn concentration absorption in the aboveground parts; no significant effects were observed for other elements. This strong mineral nutrition stabilization ability may be one of the reasons for white radish sprouts’ high cadmium/arsenic accumulation and translocation capabilities.

3.4.2. Translocation Factors of Mineral Elements

The calculated TF-Ca range for the eight tested leafy vegetables was 0.410 to 4.590, with an average of 1.761; the TF-Mg range was 0.503 to 7.582, with an average of 1.984; the TF-Fe range was 0.069 to 3.483, with an average of 0.383; the TF-Mn range was 0.523 to 10.574, with an average of 3.352; the TF-Cu range was 0.180 to 4.068, with an average of 0.709; and the TF-Zn range was 0.391 to 3.710, with an average of 1.298. Correlation analysis revealed a significant positive correlation between TF-Cd and TF-Cu in leafy vegetables (r = 0.29 *, p < 0.05). Simultaneously, significant positive correlations were also observed between TF-As and TF-Mg (r = 0.35 *, p < 0.05), TF-Fe (r = 0.51 *, p < 0.05), and TF-Zn (r = 0.42 *, p < 0.05). This suggests that the translocation ability of Cd from roots to shoots in leafy vegetables is closely related to the translocation of Cu. In contrast, the translocation of As is influenced by the complex translocation abilities of multiple mineral elements, particularly positively influenced by Mg, Fe, and Zn. Higher TF-Cu may be one of the reasons for transporter-type leafy vegetables (such as pea sprouts and black bean sprouts) to have higher TF-Cd.

3.4.3. Interactions Between Mineral Nutrients

This experiment summarized changes in the interaction patterns between mineral nutrients in leafy vegetables under heavy metal stress (Table 4). The results showed that under control conditions, only a synergistic effect between Fe and Ca in the roots and an antagonistic relationship between Zn and Ca in the aboveground parts existed within the leafy vegetables. Compared with the control, heavy metal stress significantly increased the complexity of the interactions between mineral elements. Specifically, single Cd, single As, and combined pollution treatments not only increased the synergistic effects between elements in both the roots and aboveground parts of leafy vegetables (e.g., Mg-Ca, Mg-Mn, Mg-Zn, and Fe-Cu relationships changed from non-significant correlations to synergistic) but also increased antagonistic effects (e.g., the Cu-Ca relationship changed from non-significant correlation to antagonism). These findings provide an important basis for further understanding the interactions between mineral nutrients in leafy vegetables under heavy metal stress.

4. Discussion

4.1. Safety Standards for Vegetable Intake and Tolerance Differences

Globally, approximately 900 million to 1.4 billion people reside in high-risk areas affected by soil heavy metal contamination, making food safety a paramount concern [1]. The Joint Expert Committee on Food Additives (JECFA), established jointly by the Food and Agriculture Organization of the United Nations (FAO) and the World Health Organization (WHO), has set the Provisional Tolerable Weekly Intake (PTWI) for inorganic arsenic in humans at 15 μg/(kgbw) [15]. This article evaluates based on total arsenic exposure. Additionally, the JECFA has established a Provisional Tolerable Monthly Intake (PTMI) for cadmium of 25 μg/(kgbw). According to this standard, a 60-kg adult should consume less than 128.4 μg of arsenic (As) and no more than 50 μg of cadmium (Cd) per day. Under conditions of combined Cd2As2 contamination, the cadmium content in the aerial parts of four-season creamy pak choi reached as high as 156.5 mg/kg, while the lowest cadmium content was found in Thai fragrant Youmaicai aerial parts, at 4.9 mg/kg. For arsenic, the highest content was observed in the aerial parts of white radish sprouts, reaching 928.1 mg/kg, and the lowest in willow-leaf water spinach aerial parts, at 171.6 mg/kg. Considering these factors comprehensively, to ensure safe cadmium intake, a 60-kg adult should consume no more than 31.95 g (fresh weight: 394.44 g) of four-season creamy pak choi or no more than 10.20 g (fresh weight: 65.81 g) of Thai fragrant Youmaicai per day. To control arsenic intake, daily consumption of white radish sprouts should be limited to 0.1383 g (fresh weight: 0.4461 g), and willow-leaf water spinach should not exceed 0.7485 g (fresh weight: 3.4178 g).
High-tolerance leafy vegetables (such as four-season creamy pak choi, Jiutouniao snow cabbage, small eight-leaf Takaicai) exhibited no significant changes in fresh weight of their shoots and roots when exposed to Cd and As treatments compared to the control, demonstrating good adaptability to heavy metal stress. The water content in the shoots and roots of these leafy vegetables also remained relatively stable (see Figure 3 and Figure 4), similar to the findings in studies on tobacco and chickpeas, which dilute heavy metal concentrations by regulating water balance [16,17]. In contrast, moderate-tolerance leafy vegetables (such as Thai fragrant Youmaicai, willow-leaf water spinach, black bean sprouts and white radish sprouts) showed more pronounced changes in fresh weight under heavy metal stress, although the fluctuations were still less than those observed in low-tolerance leafy vegetables (such as pea sprouts). The differences in heavy metal tolerance among leafy vegetables may be attributed to variations in phytochelatin (PC) concentrations. Our previous research has shown that the ranking of PC concentrations in the roots of leafy vegetables exhibits consistency with the tolerance index (TI) of the plants [18].

4.2. Heavy Metal Accumulation and Translocation Abilities

Leafy vegetables generally exhibit a higher propensity for heavy metal accumulation compared to other vegetable types due to their leafy structure and growth traits [19]. Their species-dependent response to heavy metal stress is intricately linked to physiological attributes and gene expression patterns, dictating variations in absorption, translocation, immobilization, and sequestration mechanisms [20]. In combined pollution contexts, these mechanisms undergo significant alterations, with moderately tolerant species like black bean sprouts and white radish sprouts showing enhanced Cd translocation, while highly tolerant species such as four-season creamy pak choi and small eight-leaf Takaicai accumulate As and Cd predominantly in their roots, attributed to their unique physiological adaptations and root-based immobilization mechanisms [19,20].
High-tolerance leafy vegetables (such as small eight-leaf Takaicai and four-season creamy pak choi) exhibit distinct heavy metal coping strategies. Although small eight-leaf Takaicai accumulated high levels of As in its roots (Table 3), its shoots did not show significant heavy metal accumulation, which may be related to its robust root-based heavy metal immobilization or sequestration mechanisms. This phenomenon has been observed in many studies, such as those on wetland plants, which usually avoid shoot accumulation by sequestering heavy metals in underground tissues [21]. Spinach and lettuce reduce shoot heavy metal accumulation by limiting the movement of As within the plant [10]. The cell walls and intercellular spaces in plant roots may immobilize heavy metals through chemical binding and physical barriers, reducing their movement within the plant [22,23]. In contrast, four-season creamy pak choi showed high Cd absorption and accumulation abilities, which may be related to its cell wall characteristics, root exudates, and efficient expression of heavy metal transporter proteins.
Moderate-tolerance leafy vegetables exhibit diversity in heavy metal translocation. For example, black bean sprouts enhanced Cd translocation under combined pollution conditions, which may be related to the activation of their xylem Cd loading mechanism by combined pollution. White radish sprouts showed prominent Cd and As absorption and translocation abilities under both single and combined pollution conditions. It may possess a mechanism that makes the rapid export or storage of the heavy metals transported to the shoots in cell structures less likely to cause damage, such as through chelation, compartmentalization, or vacuolar sequestration of heavy metals [22,24,25]. Willow-leaf water spinach and low-tolerance leafy vegetables (such as pea sprouts) belong to the avoidance type, with low heavy metal content in both shoots and roots. This may stem from their efficient heavy metal efflux mechanisms or lower heavy metal absorption capacities, which may be related to their root structure, root exudates, or other physiological characteristics.

4.3. Mineral Nutrition Regulation Mechanisms

Significant cultivar-specific responses to heavy metal stress were observed among different varieties of leafy vegetables. When subjected to either single or combined heavy metal stress, similar patterns of mineral nutrient ion regulation were noted within the same cultivar, but these patterns differed among different types of leafy vegetables (see Figure 8). Highly tolerant leafy vegetables (such as four-season creamy pak choi) exhibited increased mineral element content in their roots under heavy metal stress, which is associated with their strong heavy metal accumulation capacity and effective nutrient regulation strategies, contributing to enhanced stress resistance and growth performance. In contrast, sensitive leafy vegetables (such as pea sprouts) showed suppressed mineral element content in their roots, potentially a result of their strategy to reduce heavy metal absorption. Moderately tolerant leafy vegetables (such as white radish sprouts) demonstrated robust mineral nutrition stability, maintaining a relatively stable nutrient status under heavy metal stress.
As shown in Section 3.4.2, there was a significant positive correlation between the translocation ability of Cd from roots to shoots in leafy vegetables and the translocation of Cu elements (r = 0.29 *), suggesting that Cu may be involved in the Cd translocation process, potentially through regulating the activity of related transporter proteins. Studies have indicated that transporter proteins such as TcOPT3 can simultaneously transport Fe, Zn, Cd, and Cu, playing a crucial role in the long-distance transport of metals in plants [26]. Therefore, higher TF-Cu can explain why Cd-translocating leafy vegetables (such as pea sprouts and black bean sprouts) also exhibit higher TF-Cd. Regarding As translocation, it is positively influenced by the translocation abilities of various mineral elements such as Mg, Fe, and Zn, further revealing the complex interaction network among elements within plants.
Heavy metal stress significantly altered the interaction patterns among mineral elements in leafy vegetables, manifesting as synergistic or antagonistic effects [27,28,29]. This may be related to the interference of heavy metals with metabolic pathways in leafy vegetables [29,30,31]. Compared to the control, single Cd, single As, and combined pollution treatments induced an antagonistic relationship between Cu and Ca (Table 4), potentially leading to reduced absorption of these nutrients and exerting greater impacts on sensitive leafy vegetables. Simultaneously, these treatments promoted the synergistic absorption or translocation of Mg-Ca, Mg-Mn, Mg-Zn and Fe-Cu (Table 4), aiding the plants in maintaining normal physiological functions and mitigating heavy metal toxicity.

5. Conclusions

In summary, this study conducted an in-depth analysis of the mineral nutrient regulation mechanisms in tolerant and sensitive leafy vegetable crops under cadmium (Cd)/arsenic (As) stress conditions, thereby revealing the complex characteristics of leafy vegetable crops in response to heavy metal stress and the specific differences among varieties. This study robustly validated the preset scientific hypothesis: when leafy vegetable crops encounter single or combined Cd or As stress, they exhibit similar mineral nutrient regulation mechanisms, and there is a significant correlation between these mechanisms and heavy metal tolerance.
Specifically, high-tolerance varieties (e.g., pak choi) tend to maintain physiological homeostasis by enhancing mineral nutrient regulation mechanisms; in contrast, sensitive varieties (e.g., pea sprouts) may adopt strategies to reduce mineral nutrient uptake, thereby decreasing heavy metal absorption. Moderate-tolerance leafy vegetables (e.g., white radish sprouts), which were Cd-As accumulators with strong Cd translocation abilities, exhibited robust mineral nutrient homeostasis. These research findings not only deepen our understanding of the physiological and nutritional regulation mechanisms of plants under complex and variable environmental stress conditions but also provide novel perspectives and insights for research in this field.

Author Contributions

Conceptualization, Y.M. and L.Z.; methodology, L.Z.; software, L.Z.; validation, L.Z. and Z.C.; formal analysis, L.Z.; investigation, L.Z.; resources, Y.M. and L.Z.; data curation, L.Z.; writing—original draft preparation, Y.M., H.S., Z.C. and Q.S.; writing—review and editing, Y.M., L.L., L.W., Y.W., T.Z. and J.M.; visualization, L.Z.; supervision, Y.M.; project administration, Y.M.; funding acquisition, Y.M., L.Z., Y.W. and J.M. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by National Natural Science Foundation of China (32001200), Gansu Provincial Science and Technology Fund Plan (22JR11RM171), and Longdong University Doctoral Fund Project (Y.M., L.Z. and XYBYZK2204). The Qingyang City Science and Technology Plan Project (QY-STK-2022A-079), Natural Science Foundation of Gansu Province (25JRRM003), Science and Technology Plan Project of Xifeng District and Qingyang city (XK2024-14) also provided financial support for the conduct of this research work.

Data Availability Statement

Regarding the data availability for this study, we hereby state that a series of raw data were indeed generated during the analysis phase of our research. However, currently, these data have not been organized into a publicly archived dataset format. This decision is primarily made out of concerns for data security and privacy protection. Nonetheless, we are more than willing to share these raw data with researchers who have legitimate research needs, provided that all data privacy and ethical requirements are strictly adhered to. Scholars who wish to obtain the raw data from this study may submit their requests by contacting the corresponding.

Conflicts of Interest

The authors declare no conflicts of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

Abbreviations

The following abbreviations are used in this manuscript:
CdCadmium
AsArsenic
CaCalcium
MgMagnesium
FeIron
MnManganese
CuCopper
ZnZinc

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Figure 1. Yields (FW) of tolerant (A–C) and sensitive (D) leafy vegetables under different heavy metal treatments. Note: *** and **** on connecting lines indicate significant differences at the 0.001, and 0.0001 levels, respectively (n = 6).
Figure 1. Yields (FW) of tolerant (A–C) and sensitive (D) leafy vegetables under different heavy metal treatments. Note: *** and **** on connecting lines indicate significant differences at the 0.001, and 0.0001 levels, respectively (n = 6).
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Figure 2. Yields (FW) of moderately tolerant leafy vegetables (A–D) under different heavy metal treatments. Note: *, **, *** and **** on connecting lines indicate significant differences at the 0.05, 0.01, 0.001 and 0.0001 levels, respectively (n = 6). (A–D) represent water spinach, black bean sprouts, and white radish sprouts, and Youmaicai, respectively.
Figure 2. Yields (FW) of moderately tolerant leafy vegetables (A–D) under different heavy metal treatments. Note: *, **, *** and **** on connecting lines indicate significant differences at the 0.05, 0.01, 0.001 and 0.0001 levels, respectively (n = 6). (A–D) represent water spinach, black bean sprouts, and white radish sprouts, and Youmaicai, respectively.
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Figure 3. Trends in water content of tolerant (A–C) and sensitive (D) leafy vegetables under different heavy metal treatments. Note: * and **on connecting lines indicate significant differences at the 0.05 and 0.01 levels, respectively (n = 3).
Figure 3. Trends in water content of tolerant (A–C) and sensitive (D) leafy vegetables under different heavy metal treatments. Note: * and **on connecting lines indicate significant differences at the 0.05 and 0.01 levels, respectively (n = 3).
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Figure 4. Trends in the water content of moderately tolerant leafy vegetables (A–D) under different heavy metal treatments. Note: *, **, *** and **** denote statistical significance at the 0.05, 0.01, 0.001 and 0.0001 levels, respectively (n = 3). (A–D) represent water spinach, black bean sprouts, and white radish sprouts, and Youmaicai, respectively.
Figure 4. Trends in the water content of moderately tolerant leafy vegetables (A–D) under different heavy metal treatments. Note: *, **, *** and **** denote statistical significance at the 0.05, 0.01, 0.001 and 0.0001 levels, respectively (n = 3). (A–D) represent water spinach, black bean sprouts, and white radish sprouts, and Youmaicai, respectively.
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Figure 5. Cd content in tolerant, sensitive (A,B), and moderately tolerant (C,D) leafy vegetables. Note: *, **, and *** denote statistical significance at the 0.05, 0.01, and 0.001 levels, respectively (n = 3).
Figure 5. Cd content in tolerant, sensitive (A,B), and moderately tolerant (C,D) leafy vegetables. Note: *, **, and *** denote statistical significance at the 0.05, 0.01, and 0.001 levels, respectively (n = 3).
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Figure 6. As content in tolerant, sensitive (A,B), and moderately tolerant (C,D) leafy vegetables. Note: *, **, *** and **** denote statistical significance at the 0.05, 0.01, 0.001and 0.0001 levels, respectively (n = 3).
Figure 6. As content in tolerant, sensitive (A,B), and moderately tolerant (C,D) leafy vegetables. Note: *, **, *** and **** denote statistical significance at the 0.05, 0.01, 0.001and 0.0001 levels, respectively (n = 3).
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Figure 7. Translocation factors (TFs) for Cd/As from root to shoot in tolerant, sensitive (A,B), and moderately tolerant (C,D) leafy vegetables. Note: *, **, and *** denote statistical significance at the 0.05, 0.01, and 0.001 levels, respectively (n = 3).
Figure 7. Translocation factors (TFs) for Cd/As from root to shoot in tolerant, sensitive (A,B), and moderately tolerant (C,D) leafy vegetables. Note: *, **, and *** denote statistical significance at the 0.05, 0.01, and 0.001 levels, respectively (n = 3).
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Figure 8. Mineral nutrient regulation in leafy vegetables under Cd/As stress. Note: 1. The symbols (+) and (−) indicate significant increases and decreases, respectively, in ion concentration or translocation factor (TF) from root to shoot compared to the CK control under Cd/As stress. 2. “None” indicates no significant change in ion concentration or TF in the shoot or root of leafy vegetables compared to the CK control under Cd/As stress. 3. The trends in the figure refer to changes under single Cd, single As, and combined Cd-As stress treatments (experimental results showed consistent trends in mineral nutrient content and translocation in the same leafy vegetable species in response to single Cd, single As, and combined Cd-As pollution stress treatments).
Figure 8. Mineral nutrient regulation in leafy vegetables under Cd/As stress. Note: 1. The symbols (+) and (−) indicate significant increases and decreases, respectively, in ion concentration or translocation factor (TF) from root to shoot compared to the CK control under Cd/As stress. 2. “None” indicates no significant change in ion concentration or TF in the shoot or root of leafy vegetables compared to the CK control under Cd/As stress. 3. The trends in the figure refer to changes under single Cd, single As, and combined Cd-As stress treatments (experimental results showed consistent trends in mineral nutrient content and translocation in the same leafy vegetable species in response to single Cd, single As, and combined Cd-As pollution stress treatments).
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Table 1. Leaf vegetables for testing.
Table 1. Leaf vegetables for testing.
ToleranceChinese NameEnglish NameLatin Name
Tolerant四季奶油小白菜Four-Season Creamy Pak ChoiBrassica rapa subsp. pekinensis
九头鸟雪里蕻Jiutouniao Snow CabbageBrassica juncea var. crispifolia
小八叶榻菜Small Eight-Leaf TakaicaiBrassica rapa subsp. narinosa
Moderately Tolerant泰国香油麦菜Thai Fragrant YoumaicaiLactuca sativa var. longifolia
柳叶空心菜Willow-Leaf Water SpinachIpomoea aquatica
黑豆苗Black Bean SproutsVigna mungo (L.) Hepper
白萝卜苗White Radish SproutsRaphanus sativus L.
Sensitive麻豌豆苗Pea SproutsPisum sativum
Table 2. Treatments in the experiment.
Table 2. Treatments in the experiment.
NumberTreatmentCd Content (mg L−1)As Content (mg L−1)
1CK00
2Cd110
3Cd220
4Cd340
5Cd4100
6Cd5200
7As1010
8As2020
9As3040
10As40100
11As50200
12Cd2As2220
13Cd2As42100
14Cd4As21020
Table 3. Average heavy metal contents and translocation factors in different leafy vegetables.
Table 3. Average heavy metal contents and translocation factors in different leafy vegetables.
Tolerance TypeLeafy Vegetable SpeciesAverage Cd Content in Shoot (mg kg−1)Average Cd Content in Root (mg kg−1)Average As Content in Shoot (mg kg−1)Average As Content in Root (mg kg−1)Average TF-CdAverage TF-AsHeavy Metal Accumulation Characteristics
TolerantPak Choi163.81270.06426.16149.020.542.97Cd Accumulation Type
Snow
Cabbage		80.90108.62431.8995.280.675.02/
Takaicai97.7797.86360.20137.751.112.12As Root Accumulation Type
SensitivePea Sprouts50.6169.85244.2814.201.9724.61Avoidance Type-Translocation Type
Moderately TolerantWater Spinach39.2692.11180.5773.890.422.12Avoidance Type
Black Bean Sprouts73.7163.08683.0751.012.3813.09Translocation Type
White Radish Sprouts132.80227.531038.31459.761.784.01Accumulation Type-Translocation Type
Youmaicai47.64137.62441.42116.390.303.76Cd Root Accumulation Type
Note: The data in the table represent the average heavy metal content in the leafy vegetable plants under test, encompassing a total of five treatments, including single Cd exposure, single As exposure, and combined Cd-As contamination.
Table 4. Synergistic and antagonistic relationships between mineral elements in leafy vegetables under Cd/As stress.
Table 4. Synergistic and antagonistic relationships between mineral elements in leafy vegetables under Cd/As stress.
Mineral ElementRootShoot
CKSingle CdSingle AsCombined Cd-AsCKSingle CdSingle AsCombined Cd-As
Mg-Ca/0.41
Synergistic		0.61 Synergistic0.54
Synergistic		////
Fe-Ca0.71 *
Synergistic		//−0.46 *
Antagonistic		////
Mn-Ca//0.46 Synergistic//−0.38 *
Antagonistic		−0.39 *
Antagonistic		/
Cu-Ca/−0.32 *
Antagonistic		///−0.50
Antagonistic		−0.49
Antagonistic		−0.49 *
Antagonistic
Zn-Ca///0.76
Synergistic		−0.73 *
Antagonistic		−0.42 Antagonistic−0.36 *
Antagonistic		/
Mg-Fe//////−0.45 Antagonistic−0.56 Antagonistic
Mg-Mn/0.40 *
Synergistic		0.50
Synergistic		0.49 *
Synergistic		//0.34 *
Synergistic		/
Mg-Cu/−0.57 Antagonistic/////−0.41 *
Antagonistic
Mg-Zn/0.42
Synergistic		0.34 *
Synergistic		0.54
Synergistic		/0.39 *
Synergistic		0.50
Synergistic		0.44 *
Synergistic
Fe-Mn//////−0.39 *
Antagonistic		−0.48 *
Antagonistic
Fe-Cu/////0.45
Synergistic		0.63
Synergistic		0.50 *
Synergistic
Fe-Zn/////0.64
Synergistic		//
Mn-Cu//////−0.33 *
Antagonistic		/
Mn-Zn////////
Cu-Zn//0.33 *
Synergistic		//0.51
Synergistic		//
Note: Under CK control, single Cd, single As, and combined Cd-As pollution treatments, pairwise correlation analysis was conducted between mineral element concentrations in leafy vegetables. A significant positive correlation was judged as “synergistic”; a significant negative correlation was judged as “antagonistic”; and no significant correlation between two ion concentrations was judged as having no relationship. * Indicates a significant correlation between the concentrations of the two nutrients.
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Meng, Y.; Zhang, L.; Li, L.; Wang, L.; Wu, Y.; Zeng, T.; Shi, H.; Chang, Z.; Shi, Q.; Ma, J. Accumulation Characteristics of Trace Elements in Leafy Vegetables with Different Heavy Metal Tolerances Under Cd and as Stress. Agronomy 2025, 15, 1790. https://doi.org/10.3390/agronomy15081790

AMA Style

Meng Y, Zhang L, Li L, Wang L, Wu Y, Zeng T, Shi H, Chang Z, Shi Q, Ma J. Accumulation Characteristics of Trace Elements in Leafy Vegetables with Different Heavy Metal Tolerances Under Cd and as Stress. Agronomy. 2025; 15(8):1790. https://doi.org/10.3390/agronomy15081790

Chicago/Turabian Style

Meng, Yuan, Liang Zhang, Liping Li, Linquan Wang, Yongfu Wu, Tao Zeng, Haiqing Shi, Zeli Chang, Qian Shi, and Jian Ma. 2025. "Accumulation Characteristics of Trace Elements in Leafy Vegetables with Different Heavy Metal Tolerances Under Cd and as Stress" Agronomy 15, no. 8: 1790. https://doi.org/10.3390/agronomy15081790

APA Style

Meng, Y., Zhang, L., Li, L., Wang, L., Wu, Y., Zeng, T., Shi, H., Chang, Z., Shi, Q., & Ma, J. (2025). Accumulation Characteristics of Trace Elements in Leafy Vegetables with Different Heavy Metal Tolerances Under Cd and as Stress. Agronomy, 15(8), 1790. https://doi.org/10.3390/agronomy15081790

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