Download

ORIGINAL ARTICLE

Effects of pot simulated heavy metal stress on growth and heavy metal accumulation of Brassica chinensis L. in greenhouse

Genxin Nie1, Ling Wu2, Tianhua Tu1, Lifang Hu1,2, Yaomin Zhou1*

1Institute of Quality Safety and Standards of Agricultural Products, Jiangxi Academy of Agricultural Sciences, Nanchang, China;

2Institute of Animal Husbandry and Veterinary Medicine, Jiangxi Academy of Agricultural Sciences, Nanchang, China

Abstract

The effect of heavy metal migration, accumulation, and growth of Brassica chinensis L. were studied by the pot experiment. The results had shown that cadmium (Cd), lead (Pb), copper (Cu), zinc (Zn), and nickel (Ni) had inhibitory effects on the growth of Brassica chinensis L., but chromium (Cr) did not. The highest inhibitory degree was observed for Ni and Cu, relative growth rate was 0.21–0.35 and 0.32–0.42 g d−1, stress tolerance index was 22.44–31.77 and 29.88–36.55%, and leaf area and root length were the lowest. The main accumulation organs of Cd, Cu, and Zn are edible parts, and Pb, Cr, and Ni are in the roots. The bioconcentration factor of Cd (0.212–7.064) is the highest and that of Ni and Cr are the lowest. The accumulation of Cd and Pb, Cd and Zn, and Cd and Ni in Brassica chinensis L. showed mutual inhibition effects, and the accumulation of Pb and Cr in Brassica chinensis L. showed synergistic effects. In the production of leaf vegetables, attention should be given to the pollution of Cd in soil. Brassica chinensis L. has a high cumulative capacity for Cd, which has a certain application prospect in the implementation of green technology remediation of Cd-contaminated soil.

Key words: red soil, greenhouse, Brassica chinensis L, heavy metals, accumulation

*Corresponding Author: Yaomin Zhou, Institute of Quality Safety and Standards of Agricultural Products, Jiangxi Academy of Agricultural Sciences, Nanchang, China. Email: zhouyaomin666@163.com

Academic Editor: Aziz A. Fallah, PhD, Department of Food Hygiene and Quality Control, Faculty of Veterinary Medicine, Shahrekord University, Shahrekord, Iran

Received: 15 March 2024; Accepted: 21 November 2024; Published: 1 April 2025

DOI: 10.15586/qas.v17i2.1511

© 2025 Codon Publications
This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0). License (http://creativecommons.org/licenses/by-nc-sa/4.0/)

Introduction

Vegetables can provide vitamins, proteins, and other essential nutrients and are one of the main sources of food for humans (Wang et al., 2022). China is a major producer and consumer of vegetables. With the continuous improvement of living standards, vegetable safety has attracted extensive attention. Greenhouse vegetables can balance the supply of vegetables, as it is an efficient production mode. In recent years, with the rapid development of greenhouse vegetables, there have also been problems of environmental pollution and ecological risk, such as a high multiple cropping index, excess pesticides and chemical fertilization, and heavy metals continuously accumulating in greenhouse vegetable fields (Gao et al., 2019; Wang et al., 2021; Wen et al., 2020). Heavy metals cannot be naturally degraded, resulting in their accumulation and pollution (Tariq et al., 2019). Contamination of food by heavy metals has a series of toxic and lethal effects on human health. The major symptoms of heavy metals toxicity in humans are intellectual disability in children, central nervous system disease, dementia and depression in adults, insomnia, kidney and liver diseases, emotional instability, and vision disturbances (Jan et al., 2010). Intake of metals through contaminated vegetables may cause various chronic diseases, such as malnutritional disablities, immunological deficiencies, impaired psychosocial faculties, intrauterine growth retardation, and a high risk of upper gastrointestinal cancer in rats (Türkdogan et al., 2003). Cd can cause diseases such as bronchiolitis, emphysema, and alveolitis. Symptoms of lead poisoning are primarily associated with the central nervous system and gastrointestinal tract, and its poisoning can be either acute or chronic. Zn can cause impairment of growth and reproduction (Nolan, 2003). Cr is toxic to plants and animals including humans (Mohanty et al., 2013). Exposure of vegetables to As can cause abnormal heartbeat, low level of erythrocytes and leukocytes, nausea and vomiting, pricking sensation in the hands and legs, and severe blood vessel damage, cardiovascular disease, hypertension, internal cancers, neurological problems, peripheral vascular disease, pulmonary disease, skin lesions, and diabetes mellitus (Smith et al., 2000). Hg can cause defects such as fetal changes, spontaneous miscarriage, sexual impotency, and low sperm quality. Cu can cause defects such as severe mucosal irritation and corrosion and necrotic changes in the liver and kidney. Ni can affect the pulmonary system and skin, potential carcinogen for lung, and cause skin allergies. Plants absorb heavy metal from the soil in response to concentration gradient and selective uptake of ions or by diffusion. Roots play a significant role in the uptake of heavy metals. The adsorption of heavy metals on the root surface occurs in the cationic form with negative cell wall (Arif et al., 2016). The cations are available at the root surface from the dissociation of their complex forms and accumulated into the apoplast (Krzesłowska, 2011). Once accumulated in the root apoplast, the cations are either retained in the root cells or translocated radially to root stele and subsequently loaded into the xylem and phloem tissues through two ways known as apoplastic passive transportation and symplastic active transportation. The passive transportation occurs through the intercellular spaces by the diffusion of metal ions in the root cell through the soil solution, while the active transportation of heavy metal ions takes place through the plasma membrane mediated by different carriers or transporters (Barberon and Geldner, 2014). The transpiration stream derives the xylem sap upward, where heavy metals are distributed to the part of above ground. Heavy metals are accumulated in photosynthetically active leaves. Many studies have shown that greenhouse vegetable fields in China are polluted by heavy metals. There is a trend of heavy metal accumulation in greenhouse vegetable fields. The migration ability of heavy metals in greenhouse vegetable bases was decreased in the order of Cd>Hg>Cr>As>Pb (Xu et al., 2017). Cd, Cu, and Cr concentrations in greenhouse vegetable fields in the Huang Huai Hai and Bohai Rim regions have exceeded local maximum limit levels (Hu et al, 2017). Hu et al. (2018) found that Cd concentrations in 17.9% of sampled soils from five greenhouse vegetable production areas exceeded local maximum limit levels, and leafy vegetables have relatively higher concentrations and transfer factors of Cd. Soil under long-term greenhouse planting has seriously accumulated Cd and other heavy metals (Li et al., 2018). The concentrations of Pb and Cr of vegetables in Yunnan, China, have reached two times the region’s maximum limit levels (Wang et al., 2021). The concentration of Cd in the greenhouse soil in Xi’an city has exceeded 0.4 mg kg−1 (Guo et al., 2022). Liu et al. (2021) found that the concentration of Cd in greenhouse soil was 0.84 mg kg−1. The mean concentrations of all eight heavy metals in plastic-shed soils were greater than those in open-field agricultural soils, Zn, Cr, Cd, Hg, and Pb cause heavy pollution in the vegetable fields of the suburb Urumqi in Xinjiang, China (Sawut et al., 2018). Chen et al. (2021) found that Cd and As seriously exceeded the maximum limit levels, and the transfer capacity of Cd and Zn in leafy vegetables was the strongest. Yuan et al. (2008) and Meng et al. (2021) have found that the pollution of Cd, Pb, and Cr in North China greenhouse vegetable fields is relatively serious; transfer factors of As, Cr, Ni, and Pb were higher in leaf vegetables than in tuber and fruit vegetables; and Cd showed relatively higher transfer factors in vegetables than other metals. Leafy vegetables can accumulate higher amount of trace elements (Gupta et al., 2019), and they have a relatively high potential for Cd uptake and translocation (Baldantoni et al., 2016). Yuan et al. (2008) used the bioconcentration factor (BCF) to evaluate heavy metal transport ability in greenhouse vegetables in northern China and found that the transport coefficients of As, Cr, and Pb were higher in leafy and fruit vegetables than in tuber vegetables. Study of Gupta et al. (2019) showed that the heavy metal transport factor of leafy vegetables was higher. Jalali and Meyari (2022) evaluated the heavy metal transfer factor in the soil–vegetable system, the transfer factor of Cd is the highest, and iron is the lowest. Birghila et al. (2023) evaluated the heavy metal transfer factor of tomato; the transfer factor was less than 1. The soil–vegetable system of historical wastewater irrigation in Kaifeng city, central China, was evaluated by BCF, and the transfer factor of Cd was the highest (Cao et al., 2024; Ruan et al., 2023). The heavy metal translocation factor was higher in spinach (Ahmed et al., 2022). Some heavy metals are essential elements for plant growth; however, numerous studies (Chin et al., 2022; Zubair et al., 2024) have shown that when heavy metals reach a certain threshold, they have a significant impact on plant growth, resulting in a reduction in biomass. The Brassica species are known as metal accumulators (Neilson and Rajakaruna, 2012), which have shown high tolerance to heavy metals’ concentrations in soils (Mourato et al., 2015). Studies have demonstrated the accumulation of metals in the Brassica species (Purakayastha et al., 2008). Brassica chinensis accumulated higher levels of Cd, Cr, and Pb in all plant parts than Brassica rapa (Zunaidi et al., 2023). Heavy metals not only stunted plant and crop production growth but also posed a significant threat to ecosystems and food chains. Even at trace levels, plants tend to absorb toxic elements, leading to a growing concern within the community (Ningombam, 2024). There is an urgent need to identify plant species with hyper accumulation capabilities for heavy metals. Simultaneously, further research is needed to explore heavy metals’ accumulation, transport, and tolerance in the Brassica species.

Red soil is characteristic of a strong biological enrichment for heavy metals. The soil is polluted by heavy metals, which can easily result in excessive heavy metals in vegetables, especially leafy vegetables (Nie et al., 2023; Singh et al., 2024; Yvette et al., 2024). Therefore, in the case of heavy metal pollution, it is of great significance to explore the migration rule, pollution status, and level of heavy metals in greenhouse vegetables and assess whether vegetable planting activities can continue to ensure the quality and safety of greenhouse vegetables, especially to control heavy metal pollution in leafy vegetables. In this study, greenhouse fields were taken as the research object to simulate soil polluted by Cd, Pb, Cr, Cu, Zn, and Ni at different levels. The purpose of this study was to determine the tolerance and accumulation of six heavy metals, including Cd and Pb, in Brassica plants, which were selected because this vegetable is commonly grown locally and has a high accumulation rate of heavy metals. The objectives of this study were: (1) To observe the growth of brassica under heavy metal pollution; (2) to study the accumulation rate of heavy metals in Brassica and the interaction between heavy metal accumulation; (3) to evaluate its remediation potential for soil heavy metal pollution. This study can provide a reference for the quality and safety assurance of the development of protected vegetables in red soil areas.

Materials and Methods

Experimental materials

The experimental soil is red soil, which was collected from the land (0–20 cm) in the greenhouse of Fuzhou Agricultural Research Institute in Jiangxi Province, China. The physical and chemical properties of the collected red soil are as follows: texture classification: alfisol, sand (0.05–2.00 mm) 30.4%, silt (0.002–0.05 mm) 53.2%, clay (<0.002 mm) 16.4%, electrical conductivity 0.32 dS m−1, moisture 32.5%, total organic carbon 1.82%, organic matter 2.76%, total N 0.14%, total P 0.05%, total K 1.61%, total Ca 1.13%, total Mg 0.85%, total Na 0.11%, cation exchange capacity 13.2 cmol kg−1, total Cd 0.12 mg kg−1, total Pb 37.9 mg kg−1, total Cr 45.9 mg kg−1, total Cu 20.8 mg kg−1, total Zn 49.1 mg kg−1, total Ni 19.3 mg kg−1, and pH 5.42. According to HJ 333-2006, the soil is not polluted. The experimental crop was Brassica chinensis L., produced by the Degao Vegetable Seed Research Institute of Dezhou City, Shangdong Province, China.

Experimental design

The surface soil (0–20 cm, 930 kg) was collected from the vegetable experimental field of Fuzhou Agricultural Science and Technology Institute. The soil was crushed, air-dried, and passed through a 10-mesh nylon sieve. The sifted soil was divided into 93 plastic pots (60×20×15 centimeter), each containing 10 kg of soil. With no heavy metals added as the control and with heavy metals added to the soil reaching the maximum limit levels of HJ 333-2006 as the starting point, in order to simulate the soil by different degrees of heavy metal pollution, heavy metals were added according to Table 1. The amount of added heavy metals was increased according to the gradient to simulate the impact of heavy metals on vegetable growth under different levels of pollution. HJ 333-2006 stipulates that the limited values of Cd, Pb, Cr, Cu, Zn, and Ni are, respectively, 0.3, 50, 150, 50, 200, and 40 mg kg−1. After addition, the content of heavy metals in the soil reached the limit value as the starting point, and then gradually increased according to the multiple of the first addition amount to simulate different soil pollution degrees. At the same time, the pollution degree and migration rule of heavy metals in vegetables were analyzed when the heavy metals exceeded the maximum limit levels. The experimental design is shown in Table 1. Six treatments were set up for fixed planting soil. At the same time, a control group was set up without additives, and each treatment was repeated three times. The heavy metals were applied to the soil in the form of salt solution, fully mixed with the soil, and then sprayed with deionized water to maintain an appropriate amount of water in the soil. After 45 days of balanced cultivation, they will be used as standby.

Table 1. Heavy metal addition scheme.

Addition group Control group Heavy metal addition concentration (mg kg−1)
Cd 0 0.2 0.3 0.5 1 2
Pb 0 10 20 30 50 100
Cr 0 100 200 300 400 600
Cu 0 30 50 100 200 400
Zn 0 100 200 300 500 800
Ni 0 20 40 100 200 300

The pot experiment was conducted in the experimental greenhouse of Fuzhou Agricultural Science Research Institute in Jiangxi Province. The pot experiment began at the end of October and ended in December 2022, and the time from sowing to harvesting lasted 65 days.

Sample collection

The soil samples were collected before grinding, mixing, and sieving. Samples were taken from four corner sites around the soil pile and point site in the center, and finally mixed into a single soil sample, and taken back to the lab in a cloth bag. Soil samples were dried at room temperature, finely ground, and passed through a 10-mesh sieve, which was used to determine physicochemical properties. A portion of the soil that was passed through a 100-mesh sieve was used to determine the concentrations of heavy metals. Each pot of Brassica chinensis L. was collected as a sample and placed into a ziplock bag when they were ripe and brought back to the laboratory under cold storage conditions. Distilled water was used to wash vegetable samples, and they were dried at room temperature. The Brassica chinensis L. samples were divided into leaf, stem, and root parts for weighing. The fresh weight of each part was recorded, in which the leaves and stems were included in the weight of the above ground part, and the root was included in the underground part. Each part was placed into a paper bag for baking for 30 minutes at 100°C and dried at 70°C to a constant weight, and then the water content was calculated (Dong et al., 2022; Shuai et al., 2022). The final test results are converted to fresh samples.

Sample analysis and determination method

HMs content of soil and vegetable samples was determined according to the methods by Nie et al. (2023) and Chen et al. (2021).

The soil analyses included texture classification, pH, cation exchange capacity, organic matter (NY/T 1121-2006), moisture content (NY/T 52-1987), electrical conductivity (HJ 802-2016), total organic carbon content (HJ 658-2013), total N (LY/T 1228-2015), P (LY/T 1232-2015), K (LY/T 1234-2015), Ca, Mg, and Na (NY/T 296-1995).

Data analysis

Edible rate

The edible rate was calculated to assess the edibility of the plants grown in various metal-spiked soil treatments. This calculation involved measuring the total fresh biomass of the species and the fresh biomass of the edible plant parts (leaves and stems). It was calculated as shown in the equation (Eq).1 (Zunaidi et al., 2024).

Ediblerate=fresh biomass of the edible plant partstotal fresh biomass of plant×100% 1

Relative growth rate

The relative growth rate of a plant was assessed by measuring the plant height under metal-spiked soil treatments over a 65-day period. It was calculated as shown in Equation 2 (Hunt et al., 2002).

Relative growth rate=final heightinitial heightgroth day after transplant 2

where the final height is the height of the plant on the day of harvesting, and the initial height is the height of the treated plant during the initial measurement. The growth day after transplant is 65 day.

The stress tolerance index

The stress tolerance index was evaluated for plant height by comparing the mean height of treated plants to that of control plants under various heavy metal treatments. It was calculated as shown in Equation 3 (Mi et al., 2019).

Stress tolerance index=height of treated plantheight of control plant×100% 3

Leaf area and root length

Leaf areas and root lengths are a crucial aspect in examining how heavy metals affect the growth of vegetables and their ability to adapt in polluted environments. Leaf areas were determined by multiplying the maximum length and width of a leaf. It was calculated as shown in Equation 4 (Zunaidi et al., 2024).

Leaf area = Maximum leaf length × Maximum leaf width (4)

The root length was estimated by measuring the maximum length of the main root, from the base to the root tip using a vernier caliper.

BCF

The BCF is used to describe the transfer of heavy metals from the soil to vegetables (Tariq, 2019; Zunaidi et al., 2023). It was calculated as shown in the following equation.

BCF=CC0T 5

where C is the content of heavy metals in the corresponding parts of the addition group, C0 is the content of heavy metals in the corresponding parts of the control group, and T is the concentration of heavy metals added to the soil.

SPSS 17.0 was used to process raw data and perform statistical analyses of survey results. Part of the figure was drawn by Origin Pro 8.

Results and Discussion

Effects of the addition of heavy metals on the growth of Brassica chinensis L.

The effects of different Cd, Pb, Cr, Cu, Zn, and Ni additions on the growth of Brassica chinensis L. are shown in Table 2. The effects of the different amounts of added Cd, Pb, Cr, Cu, Zn, and Ni on the growth biomass of Brassica chinensis L. are shown in Table 1. The edible rate at each addition level of Cd, Pb, Cr, Cu, Zn, and Ni was 88.66–90.33%, 91.95–93.98%, 94.28–95.86%, 86.68–89.87%, 87.66–96.73%, and 87.34–91.04%, respectively. The relative growth rate at each addition level of Cd, Pb, Cr, Cu, Zn, and Ni was 0.52–0.56, 0.89–1.08, 1.36–1.42, 0.32–0.42, 0.28–1.41, and 0.21–0.35 g d−1, respectively. The stress tolerance index at each addition level of Cd, Pb, Cr, Cu, Zn, and Ni was 43.44–45.84%, 68.34–81.13%, 100.58–104.39%, 29.88–36.55%, 26.64–103.96%, and 22.44–31.77%, respectively. The leaf area at each addition level of Cd, Pb, Cr, Cu, Zn, and Ni was 115.47–127.51, 165.11–212.33, 268.44–281.2, 32.24–49.25, 21.36–282.68, and 19.31–39.7 cm2. The root length at each addition level of Cd, Pb, Cr, Cu, Zn, and Ni was 15.35–16.23, 17.44–21.62, 27.62–29.16, 14.33–16.62, 14.67–28.66, and 12.27–15.81 cm. Except for the Cr addition group, the biomass of other addition groups was significantly different from that of the control group.

Table 2. Effects of different amounts of added Cd, Pb, Cr, Cu, Zn, and Ni on the growth biomass of Brassica chinensis L.

Different added substances and added concentrations Number of planted plants in each group (Number of plantings per parallel×Number of parallel) Above ground fresh weight (g/plant) Whole plant fresh weight (g/plant) Edible rate (%) Relative growth rate (g d−1) Stress tolerance index (%) Leaf areas (cm2) Root lengths (cm)
Control group n=6×3 92.18±4.47a 95.62±3.86a 96.75±1.16a 1.36±0.02a 100.00a 260.26±3.56a 24.37±0.94a
Cd (0.2 mg kg−1) n=6×3 39.06±1.04b 43.83±0.97b 89.08±1.07b 0.56±0.01b 45.84±0.25b 121.14±2.11d 15.35±0.86c
Cd (0.3mg kg−1) n=6×3 38.51±1.83b 42.67±1.77b 90.33±1.03b 0.54±0.01b 44.62±0.46b 122.38±1.62c 16.18±0.57b
Cd (0.5mg kg−1) n=6×3 39.27±2.17b 43.91±1.96b 89.42±1.11b 0.56±0.01b 45.92±0.51b 127.51±2.36b 16.23±0.62b
Cd (1.0 mg kg−1) n=6×3 37.54±1.59b 42.03±1.52b 89.28±1.05b 0.53±0.01b 43.96±0.39b 116.22±1.54e 14.51±0.73d
Cd (2.0 mg kg−1) n=6×3 36.82±1.65b 41.54±1.61b 88.66±1.02b 0.52±0.01b 43.44±0.42b 115.47±1.33f 15.37±0.55c
Pb (10mg kg−1) n=6×3 72.94±3.36be 77.58±3.07be 93.98±1.09be 1.08±0.02be 81.13±0.80be 212.33±2.08b 21.62±0.77b
Pb (20mg kg−1) n=6×3 61.83±2.94bcdf 65.92±2.55bcdf 93.74±1.15bcdf 0.90±0.01bcdf 68.94±0.66bcdf 169.61±1.13e 18.71±0.69d
Pb (30 mg kg−1) n=6×3 69.15±1.81be 73.69±1.72be 93.86±1.05be 1.02±0.02be 77.07±0.45be 173.81±1.25c 19.34±0.61c
Pb (50 mg kg−1) n=6×3 70.43±2.24be 75.08±2.19be 93.83±1.02be 1.04±0.02be 78.52±0.57be 171.53±2.04d 18.27±0.54d
Pb (100 mg kg−1) n=6×3 60.11±2.03bcdf 65.35±1.97bcdf 91.95±1.03bcdf 0.89±0.01bcdf 68.34±0.51bcdf 165.11±1.69f 17.44±0.46e
Cr (100 mg kg−1) n=6×3 94.37±4.71a 98.49±4.35a 95.86±1.08a 1.40±0.02a 103.00±1.13a 270.72±3.88e 27.62±1.03d
Cr (200 mg kg−1) n=6×3 91.04±5.09a 96.17±4.76a 94.65±1.07a 1.36±0.02a 100.58±1.23a 268.44±3.16f 27.71±1.28d
Cr (300 mg kg−1) n=6×3 92.29±4.43a 97.25±4.08a 94.98±1.09a 1.38±0.02a 101.70±1.06a 275.69±2.89d 28.46±1.12c
Cr (400 mg kg−1) n=6×3 93.88±6.22a 99.24±5.84a 94.55±1.07a 1.41±0.02 a 103.79±1.51a 281.20±3.74b 28.55±2.05c
Cr (600 mg kg−1) n=6×3 94.13±5.94a 99.82±5.42a 94.28±1.10a 1.42±0.02a 104.39±1.40a 279.17±2.64c 29.16±1.96b
Cu (30 mg kg−1) n=6×3 28.17±3.16bcdef 31.33±2.94bcdef 89.82±1.07bcdef 0.37±0.01bcdef 32.77±0.76bcdef 45.26±1.05c 15.31±0.65c
Cu (50 mg kg−1) n=6×3 31.44±3.23bcd 34.95±2.88bcd 89.87±1.12bcd 0.42±0.01bcd 36.55±0.75bcd 49.25±1.16b 16.28±0.85b
Cu (100 mg kg−1) n=6×3 30.67±3.07bcde 34.57±2.71bcde 88.63±1.13bcde 0.42±0.01bcde 36.15±0.70bcde 41.34±1.24e 16.62±0.75b
Cu (200 mg kg−1) n=6×3 25.71±2.55bdef 29.64±2.23bdef 86.68±1.14bdef 0.34±0.01bdef 31.00±0.58bdef 42.16±1.67d 14.33±0.45d
Cu (400 mg kg−1) n=6×3 25.02±2.68bef 28.57±2.51bef 87.46±1.07bef 0.32±0.01bef 29.88±0.65bef 32.24±1.52f 15.19±0.66c
Zn (100 mg kg−1) n=6×3 96.01±6.65ab 99.41±6.53ab 96.56±1.02ab 1.41±0.02ab 103.96±1.69ab 282.68±2.44b 28.66±0.95b
Zn (200 mg kg−1) n=6×3 90.49±6.04ab 93.53±5.82ab 96.73±1.04ab 1.32±0.02ab 97.81±1.51ab 264.53±3.08c 28.50±1.08b
Zn (300 mg kg−1) n=6×3 44.08±3.91c 46.72±3.03c 94.25±1.29c 0.60±0.01c 48.86±0.78c 103.19±1.13d 20.25±0.58c
Zn (500 mg kg−1) n=6×3 34.15±2.76d 36.90±2.44d 92.67±1.13d 0.45±0.01d 38.59±0.63d 60.22±1.09e 19.14±0.64d
Zn (800 mg kg−1) n=6×3 22.34±2.51e 25.47±2.38e 87.66±1.05e 0.28±0.01e 26.64±0.62e 21.36±1.17f 14.67±0.33e
Ni (20 mg kg−1) n=6×3 27.54±1.99bd 30.38±1.25bd 90.60±1.59bd 0.35±0.01bd 31.77±0.32bd 39.70±1.21b 15.81±0.41b
Ni (40 mg kg−1) n=6×3 22.08±2.06cdef 24.92±2.11cdef 88.55±0.98cdef 0.27±0.01cdef 26.06±0.55cdef 22.48±1.01d 14.29±0.52c
Ni (100 mg kg−1) n=6×3 25.36±1.82bcd 27.85±1.69bcd 91.04±1.08bcd 0.31±0.01bcd 29.13±0.44bcd 25.21±1.49c 14.35±0.31c
Ni (200 mg kg−1) n=6×3 18.77±1.79cef 21.46±1.85cef 87.38±0.97cef 0.21±0.01cef 22.44±0.48cef 19.31±0.55f 12.27±0.25e
Ni (300 mg kg−1) n=6×3 20.21±2.26cef 23.13±2.14cef 87.34±1.06cef 0.24±0.01cef 24.19±0.55cef 21.64±0.82e 13.34±0.54d

Each value represents the mean of three replicates ± standard error, and the different letters within a column for the same cultivar are significantly different at p < 0.05.

Cd can significantly inhibit the growth of Brassica chinensis L., which is consistent with the results of previous studies (Han et al., 2017; Wei, 2019). There was no significant difference in the inhibition degree of different Cd addition levels on the growth of Brassica chinensis L., and it did not increase significantly due to the increase in the added level. Excess Pb has a certain inhibitory effect on the production of Brassica chinensis L., and its inhibition degree presents different degrees of inhibition with increasing addition level. When the addition level was 20 and 100 mg kg−1, the inhibition degree was the largest; when the addition level was 10, 30, and 50 mg kg−1, there was no significant difference in the inhibition degree, and the inhibition degree was far lower than that at addition levels of 20 and 100 mg kg−1. Cr not only has no inhibitory effect on the growth of Brassica chinensis L. but also has a certain growth-promoting effect. Different Cr addition levels had no significant effect on the growth of Brassica chinensis L.. The result is different from the research results of Dong et al. (2022), who believe that Brassica chinensis L. is vulnerable to Cr stress. Excess Cu can significantly inhibit the growth of Brassica chinensis L. and reduce plant biomass (Naveed et al., 2023). The inhibition degree first decreases and then increases, and the inhibition degree is the lowest when 50 mg kg−1 Cu is added. Adding a small amount of Zn can promote the growth of Brassica chinensis L., but when adding too much Zn, it will have a significant inhibitory effect on the growth of Brassica chinensis L., and with the increase in the level of addition, the inhibitory effect will continue to increase. The inhibition effect of exogenous Ni on the growth of Brassica chinensis L. was the most significant among the six heavy metals, and the inhibition degree basically increased according to the increase in the addition level.

Effects of different Cd additions on heavy metal accumulation in different parts of Brassica chinensis L.

The results of the Cd addition are shown in Figure 1. The Cd content in leaves of the control group and from low to high concentrations of heavy metals added was 0.141, 1.413, 1.464, 3.681, 4.339, and 7.664 mg kg−1, respectively. The Cd content in the stems from low to high concentrations of heavy metals added was 0.075, 1.170, 1.129, 1.299, 3.786, and 4.353 mg kg−1, respectively. The Cd content in roots from low to high concentrations of heavy metals added was 0.077, 0.135, 0.141, 0.200, 0.286, and 0.424 mg kg−1, respectively. The BCF of Cd in leaves from low to high concentrations of heavy metals added was 7.064, 4.882, 7.362, 4.339, and 3.832, respectively. The BCF of Cd in the stem from low to high concentrations of heavy metals added was 5.851, 3.764, 2.598, 3.786, and 2.176, respectively. The BCF of Cd in roots from low to high concentrations of heavy metals added was 0.675, 0.471, 0.399, 0.286, and 0.212, respectively.

Figure 1. Effects of different concentrations of exogenous Cd on heavy metal accumulation in Brassica chinensis L. (A) Cd accumulation of different parts, (B) BCF of Cd in different parts, and (C) accumulation of other heavy metals in different parts.

As shown in Figure 1A, different parts of Brassica chinensis L. have different degrees of Cd accumulation. The leaf has the highest degree of Cd accumulation, the root has the lowest degree of Cd accumulation, and the stem has the middle degree of Cd accumulation. This indicates that Cd enters the root system of Brassica chinensis L. from the soil but does not accumulate in the root system. After the root system absorbs Cd, it is transported to the stem quickly, and part of the Cd accumulates in the stem, but most of the Cd is transported to the leaf. As a result, a large amount of Cd accumulates in the leaves. The order of the degree of Cd accumulation and migration ability of each part of Brassica chinensis L. was leaf > stem > root. With the increase in the Cd content in soil, its migration ability generally declined. The leaf is the main organ of Cd accumulation in Brassica chinensis L.. Some studies (Han et al., 2017; Wei, 2019) show that the Cd content in the above ground part of Brassica chinensis L. is always lower than that in the underground part, which is different from the results of this study. The reason may be that the soil properties are different. The pH and cation exchange capacity of the soil in southern China are lower than those in northern China, leading to a higher proportion of available Cd in the soil and lower ion exchange capacity. The Cd accumulation in each part of Brassica chinensis L. was positively correlated with the Cd addition, indicating that the Cd accumulation in each part of Brassica chinensis L. increased with the increase in Cd in the soil. When the concentration of added Cd in the leaves of Brassica chinensis L. was less than 0.3 mg kg−1, the accumulation capacity of Cd did not change significantly. When the concentration of added Cd reached 0.5 mg kg−1, the accumulation capacity of Cd was greatly enhanced. When the concentration of Cd in the stems of Brassica chinensis L. was less than 0.5 mg kg−1, the Cd accumulation capacity did not change significantly. When the concentration of Cd was more than 0.5 mg kg−1, the Cd accumulation capacity was also greatly enhanced. The Cd accumulation ability of roots did not increase significantly with increasing exogenous concentration. Many studies (Ahmed et al., 2022; Cao et al., 2024; Huang et al., 2020; Kalkhajeh et al., 2020) show that leafy vegetables have a strong Cd accumulation capacity. This test shows that after adding exogenous Cd, the Cd content in the leaves and stems of Brassica chinensis L. exceeds 1 mg kg−1, seriously exceeding the limit value (0.2 mg kg−1) specified in the national food safety standard GB2762-2017. The comparison between Table 1 and Figure 1A shows that the growth inhibition degree of Brassica chinensis L. does not change significantly with the increase in Cd accumulation in each part. Figure 1B shows that the order of the migration coefficient of Cd in various parts of Brassica chinensis L. is leaf>stem>root. This is different from the observation by Zunaidi et al. (2024) that the distribution of Cd in Brassica chinensis L. is root>leaf>stem. With increasing concentration, the migration coefficient of Cd in all parts of Brassica chinensis L. was the highest at an addition amount of 0.5 mg kg−1, and the overall migration coefficient of Cd in all parts of Brassica chinensis L. gradually decreased. The effect of different amounts of Cd additions on the accumulation of other heavy metals is shown in Figure 1C. The accumulation of Pb and Ni, Cr in leaves and stems, and Cu in roots was not obvious but significantly affected the accumulation of Cr in roots, Cu in leaves and stems, and Zn in all parts. With the increase in Cd content, the accumulation of Cr in roots and Cu in leaves also increased correspondingly. The accumulation of Cu in stems first increased and then decreased, while the accumulation of Zn in all parts of Brassica chinensis L. showed a trend of first decreasing, then increasing, and then decreasing. The bioaccumulation coefficient of Cd in vegetables is higher than that of other heavy metals, which may be closely related to Cd bioavailability in the environment, soil pH, and gene expression in plant cells (Lin et al., 2024).

Effects of different Pb additions on heavy metal accumulation

Effects of different Pb additions on heavy metal accumulation in different parts of Brassica chinensis L. The different letters within a column for the same cultivar are significantly different at p < 0.05.

The results of the Pb addition are shown in Figure 2. The Pb content in leaves from low to high concentrations of heavy metals added was 0.029, 0.050, 0.062, 0.130, 0.118, and 0.167 mg kg−1, respectively. The Pb content in the stems from low to high concentrations of heavy metals added was 0.036, 0.112, 0.348, 0.641, 0.531, and 0.359 mg kg−1, respectively. The Pb content in roots from low to high concentrations of heavy metals added was 0.011, 0.503, 1.892, 2.450, 4.073, and 3.957 mg kg−1, respectively. The BCF of Pb in leaves from low to high concentrations of heavy metals added was 0.005, 0.003, 0.004, 0.002, and 0.002, respectively. The BCF of Pb in the stem from low to high concentrations of heavy metals added was 0.011, 0.017, 0.021, 0.011, and 0.004, respectively. The BCF of Pb in roots from low to high concentrations of heavy metals added was 0.050, 0.095, 0.083, 0.082, and 0.040, respectively.

Figure 2. Effects of different concentrations of exogenous Pb on heavy metal accumulation in Brassica chinensis L. (A) Pb accumulation of different parts, (B) BCF of Pb in different parts, and (C) accumulation of other heavy metals in different parts.

Figure 2A shows that different parts of Brassica chinensis L. have different levels of Pb accumulation. In addition, the accumulation in roots was much higher than that in leaves and stems, the accumulation in stems was in the middle, and the accumulation in leaves was the lowest. Some studies (Zunaidi et al., 2023) show that the Pb content in the above ground part of Brassica chinensis L. is higher than that in the underground part, which is different from the results of this study. This shows that roots are the main organ for Pb accumulation in Brassica chinensis L., and the accumulation of Pb in stems and leaves is much lower than that in roots. This finding is consistent with Mi et al. (2024). When the level of Pb addition was close to 50 mg kg−1, the accumulation of Pb in roots and stems showed a downward trend. When the concentration of added Pb reached 20 mg kg−1, the Pb content in the stems of Brassica chinensis L. was higher than 0.3 mg kg−1 (the limit value in GB2762-2017). When the concentration of added Pb reached 30 mg kg−1, the Pb accumulation in the stems of Brassica chinensis L. reached the highest level. When the concentration of Pb addition was 30–70 mg kg−1, the Pb accumulation in the stems was more than 0.5 mg kg−1, while the cumulative amount in the leaves did not exceed 0.2 mg kg−1. Figure 2B shows that the transfer coefficient of Pb in different parts of Brassica chinensis L. was in the order of root > stem > leaf. This is different from the observation by Zunaidi et al. (2024) that the distribution of Cd in Brassica chinensis L. is root > leaf > stem, and the transfer coefficient of Pb in roots was much higher than that in stems and leaves. When the level of Pb addition was 20 mg kg−1, the migration coefficient of roots to Pb reached the highest level, and with the increase in the level of Pb addition, the migration coefficient of roots to Pb decreased gradually. The migration coefficient of the stem to Pb showed a trend of first increasing and then decreasing. When the addition level was 30 mg kg−1, the migration coefficient reached the maximum. The migration coefficient of leaves showed a decreasing trend as the concentration increased. The effect of different amounts of Pb additions on the accumulation of other heavy metals is shown in Figure 2C. With the increase in Pb content, the accumulation capacity of Cd and Zn in each part of the plant was inhibited, and the accumulation capacity of Cu in the root was also inhibited. However, the accumulation capacity of Cr in the root was greatly enhanced, while the accumulation capacity of Cu in the leaves and stems showed a trend of first increasing and then decreasing.

Effects of different Cr additions on heavy metal accumulation

Effects of different Cr additions on heavy metal accumulation in different parts of Brassica chinensis L. The different letters within a column for the same cultivar are significantly different at p < 0.05.

The results of Cr addition are shown in Figure 3. The Cr content in leaves from the control group and from low to high concentrations of heavy metals added was 0.018, 0.026, 0.044, 0.071, 0.143, and 0.224 mg kg−1, respectively. The Cr content in the stems from low to high concentrations of heavy metals added was 0.029, 0.038, 0.059, 0.090, 0.200, and 0.240 mg kg−1, respectively. The Cr content in roots from low to high concentrations of heavy metals added was 0.158, 1.503, 2.793, 3.061, 4.924, and 9.416 mg kg−1, respectively. The BCF of Cr in leaves from low to high concentrations of heavy metals added was 0.0003, 0.0002, 0.0002, 0.0004, and 0.0004, respectively. The BCF of Cr in stems from low to high concentrations of heavy metals added was 0.0004, 0.0003, 0.0003, 0.0005, and 0.0004, respectively. The BCF of Cr in roots from low to high concentrations of heavy metals added was 0.015, 0.014, 0.010, 0.012, and 0.016, respectively.

Figure 3. Effects of different concentrations of exogenous Cr on heavy metal accumulation in Brassica chinensis L. (A) Cr accumulation of different parts, (B) BCF of Cr in different parts, and (C) accumulation of other heavy metals in different parts. The different letters within a column for the same cultivar are significantly different at p < 0.05.

Figure 3A shows that within the range of added concentrations, the Cr content in each part of Brassica chinensis L. was positively correlated with the Cr content in the soil. With the increase in the Cr content in soil, the Cr accumulation in the roots of Brassica chinensis L. increased significantly, while the accumulation in the leaves and stems did not show a significant upward trend with the increase in exogenous Cr concentration. The accumulative amount of Cr in leaves and stems was equivalent and lower than that in roots, which could be attributed to the sequestration of Cr in the vacuoles of root cells as a protective mechanism, thereby naturally enhancing the tolerance of the two species to Cr toxicity (Liu, 2010; Zunaidi et al., 2024). This is consistent with the conclusion that the accumulation of Cr in Brassica chinensis L. occurs mainly in roots (Liu, 2010; Yu et al., 2023; Zunaidi et al., 2023). Within the range of addition, the accumulative amount of Cr does not exceed 0.25 mg kg−1, which is far below the limit of 0.5 mg kg−1 in the local food safety standard GB2762-2017. Figure 3B shows that the transfer coefficient of Cr in various parts of Brassica chinensis L. was in the order of root > stem > leaf, and the transfer coefficient of Cr in roots was much higher than that in stems and leaves. The removal coefficient of Cr in stems and leaves was similar, but the change was not significant with increasing Cr concentration. The effect of different amounts of Pb additions on the accumulation of other heavy metals is shown in Figure 3C. With the increase in Cr addition, the accumulation of Pb in leaves and roots and Zn in each part showed an increasing trend; the accumulation of Cd and Cu in leaves and Pb in stems first increased and then decreased; and the accumulation of Cd and Pb in roots, Cu in stems, and Ni in each part showed a decreasing trend.

Effects of different Cu additions on heavy metal accumulation in different parts of Brassica chinensis L

The results of Cu addition are shown in Figure 4. The Cu contents in leaves from low to high concentrations of heavy metals added were 0.300, 0.608, 0.890, 2.719, 3.030, and 5.070 mg kg−1, respectively. The Cu content in the stems from low to high concentrations of heavy metals added was 0.090, 0.092, 0.197, 0.450, 0.646, and 0.751 mg kg−1, respectively. The Cu content in roots from low to high concentrations of heavy metals added was 0.193, 0.111, 0.103, 0.351, 1.153, and 2.167 mg kg−1, respectively. The BCF of Cu in leaves from low to high concentrations of heavy metals added was 0.020, 0.018, 0.027, 0.015, and 0.013, respectively. The BCF of Cu in the stem from low to high concentrations of heavy metals added was 0.003, 0.004, 0.005, 0.003, and 0.002, respectively. The BCF of Cu in roots from low to high concentrations of heavy metals added was 0.004, 0.002, 0.004, 0.006, and 0.005, respectively.

Figure 4. Effects of different concentrations of exogenous Cu on heavy metal accumulation in Brassica chinensis L. (A) Cu accumulation of different parts, (B) BCF of Cu in different parts, and (C) accumulation of other heavy metals in different parts.

Cu plays a vital role in many physiological activities, such as photosynthesis, respiration, and the regulation of the antioxidant system of plants, as well as in the growth and development of plants. However, Cu is considered to be one of the most toxic heavy metals. When plants are exposed to very high concentrations of Cu, it will Pb to the disorder of plant physiological functions and growth retardation (Kumar et al., 2021). Figure 4 shows that within the range of addition concentrations, the Cu content in Brassica chinensis L. is positively correlated with the Cu content added to the soil, but the Cu accumulation effect in each part of Brassica chinensis L. is different. The Cu accumulation ability in the leaf part is much higher than that in the stem and root. Zunaidi et al. (2023) concluded that the roots of Brassica chinensis L. had a stronger Cu accumulation capacity than the leaves and stems, which was different from the results of this study. The Cu accumulation ability in the stem part was the lowest, and the Cu accumulation amount in the leaf part was much higher than that in other parts. The reason is that the leaf is the main organ for photosynthesis, and photosynthesis requires the participation of Cu. It can be seen from the curve trend in Figure 4A that the cumulative amount of Cu in leaves and stems will show a downward trend after reaching a certain degree. With increasing Cu concentration in the environment, the Cu accumulation rate in the roots of Brassica chinensis L. increased steadily, and its accumulation capacity exceeded that in the leaves and stems. This result is consistent with the research results of Yuan et al. (2008). Figure 4B shows that the migration coefficient of Cu at the leaf position is the highest. With the continuous increase in Cu addition concentration, the migration coefficient of the leaf presents a trend of first decreasing, then increasing, and then decreasing. At a concentration of 100 mg kg−1, the migration coefficient reaches the highest value. The Cu transport coefficient of stems and roots was much lower than that of leaves. The effect of different amounts of Pb additions on the accumulation of other heavy metals is shown in Figure 4C. With the increase in Cu content, the accumulation of Cd in the stem and Pb and Cr in the root showed an increasing trend, the accumulation of Pb in the leaf and stem showed an increasing trend and then a decreasing trend, and the accumulation of Cd in the leaf and root and Zn and Ni in each part showed a decreasing trend.

Effects of different Zn additions on heavy metal accumulation

Effects of different Zn additions on heavy metal accumulation in different parts of Brassica chinensis L.. The different letters within a column for the same cultivar are significantly different at p < 0.05.

The results of the Zn addition are shown in Figure 5. The Zn content in leaves from the control group and from low to high concentrations of heavy metals added was 1.172, 5.093, 7.209, 14.570, 16.202, and 47.911 mg kg−1, respectively. The Zn contents in the stems from low to high concentrations of heavy metals added were 1.452, 5.401, 11.888, 25.510, 47.407, and 91.721 mg kg−1, respectively. The Zn content in roots from low to high concentrations of heavy metals added was 0.531, 2.741, 4.012, 12.415, 18.088, and 32.928 mg kg−1, respectively. The BCF of Zn in leaves from low to high concentrations of heavy metals added was 0.051, 0.036, 0.049, 0.032, and 0.060, respectively. The BCF of Zn in the stems from low to high concentrations of heavy metals added was 0.054, 0.059, 0.085, 0.095, and 0.115, respectively. The BCF of Zn in roots from low to high concentrations of heavy metals added was 0.027, 0.020, 0.041, 0.036, and 0.041, respectively.

Figure 5. Effects of different concentrations of exogenous Zn on heavy metal accumulation in Brassica chinensis L. (A) Zn accumulation of different parts, (B) BCF of Zn in different parts, and (C) accumulation of other heavy metals in different parts.

Figure 5A shows that within the range of added concentrations, the Zn content in Brassica chinensis L. is positively correlated with the Zn content in the soil. Among them, the stem has the strongest cumulative capacity, and the root has the lowest cumulative capacity. When the Zn addition concentration in the soil reached 300 mg kg−1, the cumulative capacity of the stem and leaf to Zn was enhanced, but the cumulative capacity of the root to Zn did not show rapid growth. An appropriate amount of Zn application can alleviate the toxicity of Cd and other heavy metals and promote plant growth. When Zn is applied excessively, the ability to mitigate the toxicity of other heavy metals decreases significantly, which in turn inhibits plant growth, thereby decreasing the above ground biomass of plants (Shuai et al., 2022). Combined with the results in Table 1, when the Zn accumulation in Brassica chinensis L. increased by 10 mg kg−1, Zn did not play a role in toxicity mitigation but inhibited the growth of Brassica chinensis L.. The higher the Zn accumulation in Brassica chinensis L. was, the higher the growth inhibition degree of Brassica chinensis L.. At the same time, Figure 5B shows that the migration coefficient of each part of Brassica chinensis L. is stem > leaf > root, and the migration coefficient of Zn from the stem increases with increasing Zn concentration. The effect of different amounts of Pb additions on the accumulation of other heavy metals is shown in Figure 5C. With the increase in Zn addition, the accumulation of Cd and Ni in all parts showed an inhibitory effect, the accumulation of Pb in stems showed a synergistic effect, the accumulation of Pb, Cr, and Cu in leaves showed a trend of first increasing and then decreasing, the accumulation of Cr in stems showed a trend of first increasing and then decreasing, and the accumulation of Pb and Cr in roots also showed a trend of first increasing and then decreasing. The accumulation of Cu in stems and roots was inhibited first and then synergistically.

Effects of different Ni additions on heavy metal accumulation

Effects of different Ni additions on heavy metal accumulation in different parts of Brassica chinensis L.. The different letters within a column for the same cultivar are significantly different at p < 0.05.

The results of the Ni addition are shown in Figure 3. The Ni content in leaves from low to high concentrations of heavy metals added was 0.006, 0.014, 0.036, 0.059, 0.091, and 0.142 mg kg−1, respectively. The Ni content in the stems from low to high concentrations of heavy metals added was 0.005, 0.009, 0.025, 0.049, 0.090, and 0.158 mg kg−1, respectively. The Ni content in roots from low to high concentrations of heavy metals added was 0.007, 0.016, 0.061, 0.374, 0.552, and 0.114 mg kg−1, respectively. The BCF of Ni in leaves from low to high concentrations of heavy metals added was 0.0007, 0.0009, 0.0006, 0.0005, and 0.0005, respectively. The BCF of Ni in the stem from low to high concentrations of heavy metals added was 0.0004, 0.0006, 0.0005, 0.0004, and 0.0005, respectively. The BCF of Ni in roots from low to high concentrations of heavy metals added was 0.0008, 0.0015, 0.0037, 0.0028, and 0.0004, respectively.

Figure 6A shows that within the range of addition concentrations, the Ni accumulation capacity of the leaves and stems of the above ground part of Brassica chinensis L. was positively correlated with the Ni content in the soil, and there was no significant difference in the Ni accumulation capacity of the leaves and stems. When the addition concentration was less than 200 mg kg−1, the Ni accumulation capacity of the leaves and stems did not exceed 0.1 mg kg−1, but the accumulation capacity of the stems was lower than that of the leaves at a lower concentration, and at a higher concentration, Ni accumulation in stems was higher than that in leaves. The Ni accumulation capacity of roots first increased and then decreased with increasing concentration. When the amount of Ni added reached 200 mg kg−1, the Ni accumulation capacity of roots reached a maximum and then showed a downward trend. Within the range of experimental additions, the Ni accumulation organ was mainly roots. Some studies have shown that some vegetables are highly sensitive to Ni. When the accumulation of Ni in plants is greater, the toxicity of Ni is stronger, and the degree of inhibition of vegetable growth is higher (Bai et al., 2018). Combined with the results in Table 1, these results show that Brassica chinensis L. is highly sensitive to Ni, and the higher the Ni accumulation in vegetables, the stronger is the growth inhibition. Compared with other heavy metals, Ni has the lowest migration capacity, which is consistent with the findings of Singh et al. (2024). Figure 6B shows that the order of the Ni transfer coefficient in each part of Brassica chinensis L. is root > leaf > stem. With increasing Ni concentration, the Ni transfer coefficient in each part of Brassica chinensis L. first increased and then decreased. When the Ni concentration reaches 100 mg kg−1, the Ni transfer coefficient in roots reaches the highest value. The effect of different amounts of Pb additions on the accumulation of other heavy metals is shown in Figure 6C. With increasing Ni content, the stem and root had a synergistic effect on Pb and Cr accumulation, and the leaves and stem had an inhibitory effect on Cd and Zn accumulation.

Figure 6. Effects of different concentrations of exogenous Ni on heavy metal accumulation in Brassica chinensis L. (A) Ni accumulation of different parts, (B) BCF of Ni in different parts, and (C) accumulation of other heavy metals in different parts. The different letters within a column for the same cultivar are significantly different at p < 0.05.

There are still some shortcomings in this study; for example, only a single vegetable variety was studied, but there are differences in the corresponding and cumulative ability of heavy metal stress among different varieties. At the same time, multiple heavy metal combined pollution is often encountered in reality, and this study only simulates the situation of a single heavy metal pollution. There is a lack of comparative studies on the effects of heavy metal pollution on crop growth and heavy metal accumulation under different production modes in greenhouses and open fields.

Conclusions

Excessive Cd, Pb, Cu, Zn, and Ni all have inhibitory effects on the growth of Brassica chinensis L., with Ni and Cu having the highest inhibitory degree, followed by Cd. Cr had no inhibitory effect on the growth of Brassica chinensis L.. The main accumulation organs of Cd, Cu, and Zn are the edible parts of stems and leaves, and the main accumulation organs of Pb, Cr, and Ni are mainly in the roots. The BCF of Cd is much higher than that of the five heavy metals, and the BCF of Ni and Cr are the lowest. Compared with other heavy metals, Brassica chinensis L. has a high cumulative capacity for Cd, which has a certain application prospect in the implementation of green technology remediation of Cd-contaminated soil. The accumulation of Cd and Pb, Cd and Zn, and Cd and Ni in Brassica chinensis L. showed mutual inhibition effects, and the accumulation of Pb and Cr in Brassica chinensis L. showed synergistic effects. In the production of leaf vegetables, attention should be given to the pollution of Cd in soil. In the future, it is necessary to further study the accumulation and growth of heavy metals in vegetables under different vegetable varieties, heavy metal composite pollution, and different production modes.

Statements and Declarations

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgment

This study was financially supported by the Jiangxi Vegetable Industry Technical System (Grant No.: JXARS-06).

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Author Contributions

Genxin Nie was in charge of conceptualization, methodology, investigation, editing, writing, and original draft. Yaomin Zhou was responsible for resources, supervision, and review & editing. Tianhua Tu did analysis and data collection. Lifang Hu performed sample collection. Ling Wu was concerned with methodology and review & editing. All authors have read and agreed to the published version of the manuscript.

Funding

This work had received a grant from the Jiangxi Provincial Department of Agriculture and Rural Affairs, China.

REFERENCES

Ahmed, S., Fatema, T.Z., Mahdi, M.M., Md, N., Md., Z.A., and Choudhury T.R. 2022. Health risk assessment for heavy metal accumulation in leafy vegetables grown on tannery effluent contaminated soil. Toxicology Reports 9:346–355. 10.1016/j.toxrep.2022.03.009

Arif N., Yadav, V., Singh, S., Ahmad, P., Mishra, R.K., Sharma, S., Tripathi, D.K., Dubey, N.K., and Chauhan, D.K. 2016. Influence of high and low levels of plant-beneficial heavy metal ions on plant growth and development. Frontiers in Environmental Science 4: 69.

Bai, Y., Shen, G., Chen, X., Guo, C., Qian, X., Zhao, X., and Zhou, Z. 2018. Accumulation and transport of nickel in three vegetable crops and their edible safety. Journal of Agro-Environment Science 37(8): 1619–1625. https://kns.cnki.net/kcms2/article/abstract?v=j6HAoO1nZAxXFt9nKCGnvDyKYejYEkhCgdT6thD4y8ooSQeobu46Z_zJY5uUIE4KZvoHiNmNFZjVj3Up5RNyBLgDJ6S8W8YHZ5Ga_J65_jgXOybsmVxjcN3dIsfk8eQgLbTYMbKG0QhWRhnY7wEZGA==&uniplatform=NZKPT&language=CHS.

Baldantoni, D., Morra, L., Zaccardelli, M., and Alfani, A. 2016. Cadmium accumulation in leaves of leafy vegetables. Ecotoxicology and Environmental Safety 123:89–94. 10.1016/j.ecoenv.2015.05.019

Barberon M., and Geldner N. 2014. Radial transport of nutrients: the plant root as a polarized epithelium. Plant Physiology 166:528–537.

Birghila, S., Matei, N., Dobrinas, S., Popescu, V., Soceanu, A., and Niculescu, A. 2023. Assessment of heavy metal content in soil and lycopersicon esculentum (tomato) and their health implications. Biological Trace Element Research 201:1547–1556. 10.1007/s12011-022-03257-9

Cao, C., Liang, B.Y., Yang, Y., Ren, D., Tang, Q.H., Wang, C.W., Li Z., and Wang, J.J. 2024. Temporal variations in absorption and translocation of heavy metal(loid)s in pak choi (Brassica rapa L.) under open-field and greenhouse cultivation. Ecotoxicology and Environmental Safety, Volume 281, 116667. 10.1016/j.ecoenv.2024.116667

Chen, Z., Muhammad, I., Zhang, Y., Hu, W., Lu, Q., Wang, W., Huang, B., and Hao, M. 2021.Transfer of heavy metals in fruits and vegetables grown in greenhouse cultivation systems and their health risks in northwest China. Science of the Total Environment 766:142663. 10.1016/j.scitotenv.2020.142663

Chin, J.M., Lim, Y.Y., and Ting, A.S.Y. 2022. Biopriming vegetable seeds with metal-tolerant biocontrol agents to enhance tolerance to biotic and abiotic stress. Biological Control 174:105035. 10.1016/j.biocontrol.2022.105035

China National Environmental Protection Agency (CNEPA). 2006. Environmental quality evaluation standard for farmland of greenhouse vegetables production (HJ333–2006). Beijing, China: China Environment Press.

Chinese Ministry of Health (CMH). 2017. National standards for food safety limit of contaminants in food (GB2762-2017). Beijing, China: China Standards Press.

Chinese Ministry of Agriculture. 2006. Soil test (NY/T 1121-2006). Beijing, China: China Agricultural Press.

Chinese Ministry of Agriculture. 1995. Determination of total calcium, magnesium, and sodium in soil (NY/T 296-1995). Beijing, China: China Agricultural Press.

Chinese Ministry of Agriculture.1987. Method for the determination of soil water content (NY/T 52-1987). Beijing, China: China Agricultural Press.

Chinese Ministry of Environmental. 2016. Protection soil quality-determination of conductivity-electrode method (HJ 802-2016). Beijing, China: China Standards Press.

Chinese Ministry of Environmental. 2013. Soil-determination of organic carbon-combustion oxidation-titration method (HJ 658-2013). Beijing, China: China Standards Press.

Chinese Forestry Administration. 2015. Phosphorus determination methods of forest soils (LY/T 1232-2015). Beijing, China: China Standards Press.

Chinese Forestry Administration. 2015. Potassium determination methods of forest soils (LY/T 1234-2015). Beijing, China: China Standards Press.

Chinese Forestry Administration. 2015. Nitrogen determination methods of forest soils (LY/T 1228-2015). Beijing, China: China Standards Press.

Dong, J., Gao, P., Sun, H., Zhou, C., Zhang, X., Xue, P., and Liu, W. 2022. Characteristics and health risk assessment of cadmium, lead, and arsenic accumulation in leafy vegetables planted in a greenhouse. Environmental Science (in Chinese) 43(1):481–489. 10.13227/j.hjkx.202106002

Gao, X., Peng, Y., Zhou, Y., Muhammad, A., and Chen, Q. 2019. Effects of magnesium ferrite biochar on the cadmium passivation in acidic soil and bioavailability for pak choi (Brassica chinensis L.). Journal of Environmental Management 251:109610. 10.1016/j.jenvman.2019.109610.

Guo, J., Zhang, Y., Liu, W., Zhao, J., Yu, S., Jia, H., Zhang, C., and Li, Y. 2022. Incorporating in vitro bioaccessibility into human health risk assessment of heavy metals and metalloid (As) in soil and pak choi (Brassica chinensis L.) from greenhouse vegetable production fields in a megacity in northwest China. Food Chemistry 373:131488. 10.1016/j.foodchem.2021.131488

Gupta, N., Yadav, K.K., Kumar, V., Kumar, S., Chadd, R.P., and Kumar, A. 2019. Trace elements in soil-vegetables interface: translocation, bioaccumulation, toxicity and amelioration—a review. Science of the Total Environment 651:2927–2942. 10.1016/j.scitotenv.2018.10.047

Han, C., Shen, H., and Zhang, H. 2017. Effects of simulated-Cd-pollution on growth, cadmium accumulation and its subcellular distribution in Brasica chinensis L. Northern Horticulture 22: 6–11. https://kns.cnki.net/kcms2/article/abstract?v=j6HAoO1nZAy5Rov9jpwn5-MlNe37Wc1V668XW0DkVHwIFORsZBd97JKdbYktNLujdCOuVwM9CLLutBGYOE0sJEY6I-h7dDPz5yAgXsJh9oUZ0MFAcA_1rwe2loPHOZGZ2wcxnqsuKydkVoi_ZDIT0A==&uniplatform=NZKPT&language=CHS.

Hu, W., Huang, B., Borggaard, O.K., Ye, M., Tian, K., Zhang, H., and Holm, P.E. 2018. Soil threshold values for cadmium based on paired soil-vegetable content analyses of greenhouse vegetable production systems in China: implications for safe food production. Environmental Pollution 241:922–929. 10.1016/j.envpol.2018.06.034.0

Hu, W., Huang, B., Tian, K., Holm, P.E., and Zhang, Y. 2017. Heavy metals in intensive greenhouse vegetable production systems along Yellow Sea of China: levels, transfer and health risk. Chemosphere 167:82–90. 10.1016/j.chemosphere.2016.09.122

Huang, L, Wang, Q., Zhou, Q., Ma, L., Wu, Y., Liu, Q., Wang, S., and Feng, Y. 2020. Cadmium uptake from soil and transport by leafy vegetables: a meta-analysis. Environmental Pollution 264:114677. 10.1016/j.envpol.2020.114677

Hunt, R., Causton, D.R., Shipley, B., and Askew, A.P. 2002. A modern tool for classical plant growth analysis. Annals of Botany 90(2002):485–488. 10.1093/aob/mcf214

Jalali, M., and Meyari, A. 2022. Heavy metal contents, soil-to-plant transfer factors, and associated health risks in vegetables grown in western Iran. Journal of Food Composition and Analysis 106:104316. 10.1016/j.jfca.2021.104316

Jan, F.A., Ishaq, M., Ihsanullah, I., and Asim, S.M. 2010. Multivariate statistical analysis of heavy metals pollution in industrial area and its comparison with relatively less polluted area: a case study from the city of Peshawar and district Dir Lower. Journal of Hazardous Materials 176: 609–616.

Kalkhajeh, Y.K.Y., Huang, B., Hu, W., Ma, C., Gao, H., Thompson, M.L., and Hansen, H.C.B. 2020. Environmental soil quality and vegetable safety under current greenhouse vegetable production management in China. Agriculture, Ecosystems & Environment 307:107230. 10.1016/j.agee.2020.107230

Kumar, V., Pandita, S., Sidhu, G.P.S., Sharma, A., Khanna, K., Kaur, P., Bali, A.S., and Setiaet, R. 2021. Copper bioavailability, uptake, toxicity and tolerance in plants: a comprehensive review. Chemosphere 262:127810. 10.1016/j.chemosphere.2020.127810

Krzesłowska, M. 2011. The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy. Acta Physiologiae Plantarum 33:35–51.

Li, J., Zhu, L., Tong, L., Lu, Y., and Li, J. 2018. Risk assessment of heavy metals accumulation in soils under long-term greenhouse vegetable cultivation conditions. Journal of Agro-Environment Science 37(10):2159–2165. https://kns.cnki.net/kcms2/article/abstract?v=j6HAoO1nZAxQgu_78yfT4Bdf4RJtXa_E7-UyQSBEAWZ5dW84H1dzwR97PfjrFnu8CpFN4MktJ1uyX-nZfM9bfPctiFDV-Z_na1IQuZ0GbWwkn69MrP03LknrmYjLtx9KIssY6PK1R3C0z4mXSQ6Ocw==&uniplatform=NZKPT&language=CHS.

Lin L., Wu, X., Deng, X., Lin, Z., Liu, C., Zhang, J., He, T., Yi, Y., Liu, H., Wang, Y., Sun, W., and Xu, Z. 2024. Mechanisms of low cadmium accumulation in crops: a comprehensive overview from rhizosphere soil to edible parts. Mechanisms of low cadmium accumulation in crops: a comprehensive overview from rhizosphere soil to edible parts. Environmental Research, Volume 245:118054, 10.1016/j.envres.2023.118054

Liu, J., Wang, Y., Liu, X., and Xu, J. 2021. Occurrence and health risks of heavy metals in plastic-shed soils and vegetables across China. Agriculture, Ecosystems and Environmen 21:107632. 10.1016/j.agee.2021.107632

Liu, L. 2010. Changes of heavy metal’s content in greenhouse and the absorption and accumulation of Cr6+ in celery. PhD diss., Northwest Agriculture and Forestry University. https://kns.cnki.net/kcms2/article/abstract?v=jDUTNXVfqCp9BPe5fpmNfVz5qRsQpb7ME0iFsWUS0z1yXs9oxWi_0f7WSYLayZHDCHN7h5c7Ghew_OYDceEk4piNIcKQ1Lg7b4FBiYty5lJ7x-cihmRpa8ItBbxDg1edlGLkfvmnWayCHiq_F4Xh9w==&uniplatform=NZKPT&language=CHS.

Meng, M., Yang, L., Wei, B., Cao, Z., Yu, J., and Liao, X. 2021. Plastic shed production systems: the migration of heavy metals from soil to vegetables and human health risk assessment. Ecotoxicology and Environmental Safety 215:112106. 10.1016/j.ecoenv.2021.112106

Mi, B., Liu, F., Xie, L., Zhou, H., Wu, F., and Dai, X. 2019. Evaluation of the uptake capacities of heavy metals in Chinese cabbage. Ecotoxicology and Environmental Safety 171: 511–517. 10.1016/j.ecoenv.2019.01.022

Mohanty M., and Kumar P.H. 2013. Effect of ionic and chelate assisted hexavalent chromium on mung bean seedlings (Vigna Radiata l. Wilczek. Var k-851) during seedling growth. Journal of Stress Physiology & Biochemistry 9:232–241.

Mourato, M.P., Moreira, I.N., Leitao, I., Pinto, F.R., Sales, J.R., and Martins, L.L. 2015. Effect of heavy metals in plants of the genus Brassica. International Journal of Molecular Sciences 16: 17975–17998. 10.3390/ijms160817975

Mi, B., Xiao, W., Tu, N., and Wu, F. 2024. Selection of pollution-safe head cabbage: interaction of multiple heavy metals in soil on bioaccumulation and transfer. Food Chemistry 452:139615. 10.1016/j.foodchem.2024.139615

Naveed, S., Oladoye, P.O., and Alli, Y.A. 2023. Toxic heavy metals: a bibliographic review of risk assessment, toxicity, and phytoremediation technology. Sustainable Chemistry for the Environment 2:100018. 10.1016/j.scenv.2023.100018.

Neilson, S., and Rajakaruna, N. 2012. Roles of rhizospheric processes and plant physiology in applied phytoremediation of contaminated soils using Brassica oilseeds, In: Anjum, N.A., et al. (Eds.) The Plant Family Brassicaceae: Contribution Towards Phytoremediation, pp. 313–330. Environmental Pollution Book Series, Vol. 21, Springer (Science + Business Media), Dordrecht, The Netherlands.

Nie, G., Tu, T., Hu, L., Wu, L., and Zhou, Y. 2023. Accumulation characteristics and evaluation of heavy metals in soils and vegetables of plastic-covered sheds in typical red soil areas of China. Quality Assurance and Safety of Crops & Foods 15(3):22–35. 10.15586/qas.v15i3.1222

Ningombam, L., Hazarika, B.N., Yumkhaibam, T., Heisnam, P., and Singh, Y.D. 2024. Heavy metal priming plant stress tolerance deciphering through physiological, biochemical, molecular and omics mechanism. South African Journal of Botany, 168:16–25. 10.1016/j.sajb.2024.02.032

Nolan, K. 2003. Copper toxicity syndrome. Journal of Orthomolecular Psychiatry. 12:270–282.

Purakayastha, T.J., Viswanath, T., Bhadraray, S., Chhonkar, P.K., Adhikari, P.P., and Suribabu, K. 2008. Phytoextraction of zinc, copper, nickel and lead from a contaminated soil by different species of Brassica. International Journal of Phytoremediation 10:61–72. 10.1080/15226510701827077

Quispe, N., Zanabria, D., Chavez, E., Cuadros, F., Carling, G., and Paredes, B. 2021. Health risk assessment of heavy metals (Hg, Pb, Cd, Cr and As) via consumption of vegetables cultured in agricultural sites in Arequipa, Peru. Chemical Data Collections 33:100723. 10.1016/j.cdc.2021.100723

Ruan, X., Ge, S., Jiao, Z., Zhan, W., and Wang, Y. 2023. Bioaccumulation and risk assessment of potential toxic elements in the soil-vegetable system as influenced by historical wastewater irrigation. Agricultural Water Management 279:108197. 10.1016/j.agwat.2023.108197

Singh, R., Singh, P.K., Madheshiya, P., Khare, A.K., and Tiwari, S. 2024. Heavy metal contamination in the wastewater irrigated soil and bioaccumulation in cultivated vegetables: assessment of human health risk. Journal of Food Composition and Analysis. 128:106054. 10.1016/j.jfca.2024.106054.

Sawut, R., Kasim, N., Maihemuti, B., Hu, L., Abliz, A., Abdujappar, A., and Kurban, M. 2018. Pollution characteristics and health risk assessment of heavy metals in the vegetable bases of northwest China. Science of the Total Environment 642:864–878. 10.1016/j.scitotenv.2018.06.034.

Shuai, Z., Liu, H., Cui, H., and Wei, S. 2022. Effects of interaction of zinc and cadmium on growth and cadmium accumulation of Brassica campestris L. Environmental Science 43(11):5234–5243. 10.13227/j.hjkx.202201202

Smith A.H., Lingas E.O., and Rahman M. 2000. Contamination of drinking-water by arsenic in Bangladesh: a public health emergency. Bulletin of the World Health Organization 78:1093–1103.

Tariq, F.S., Samsuri, A.W., Karam, D.S., Aris, A.Z., and G. Jamilu. 2019. Bioavailability and mobility of arsenic, cadmium, and manganese in gold mine tailings amended with rice husk ash and Fe-coated rice husk ash. Environmental Monitoring and Assessment 191(4):232. 10.1016/j.envpol.2019.113645

Türkdogan M.K., Kilicel F., Kara K., Tuncer I., and Uygan I. 2003. Heavy metals in soil, vegetables and fruits in the endemic upper gastrointestinal cancer region of Turkey. Environmental Toxicology and Pharmacology 13(3):175–179.

Wang, C., Li, M., Yan, C., Wen, T., Deng, Z., Wang, Z., Xu, W., Tuo, Y., and Xiang, P. 2022. Refining health risk assessment of heavy metals in vegetables from high geochemical background areas: role of bioaccessibility and cytotoxicity. Process Safety and Environmental Protection 159:345–353. 10.1016/j.psep.2022.01.003

Wang, Z., Chen, X.M., Yu, D.Q., Zhang, L.X., Wang, J.N., and Lv, J.S. 2021. Source apportionment and spatial distribution of potentially toxic elements in soils: a new exploration on receptor and geostatistical models. Science of The Total Environment 759(2):143428. 10.1016/j.scitotenv.2020.143428.

Wei, L. 2019. Study of simulated-Cd-pollution on growth and accumulation of cadmium in green vegetables and radish. Journal of Kashi University 40(3):44–48. 10.13933/j.cnki.2096-2134.2019.03.010

Wen, Y.B., Li, W., Yang, Z.F., Guan, D., Song, Y., Guo, C., and Ji, J. 2020. Evaluation of various approaches to predict cadmium bioavailability to rice grown in soils with high geochemical background in the karst region, southwestern China. Environmental Pollution 258:113645. 10.1016/j.envpol.2019.113645

Xu, L., Lu, A., Tian, X., He, H., and Yin, J. 2017. Accumulation characteristics and risk assessment of heavy metals in typical greenhouse vegetable bases. Scientia Agricultura Sinica 50(21):4149–4158. 10.3864/j.issn.0578-1752.2017.21.009

Yu, X., Li, H., Yang, Q., Sun, Z., and Ma, Y. 2023. Accumulation of Cr in different vegetables and derivation of soil Cr threshold using the species sensitivity distribution method. Ecotoxicology and Environmental Safety 258: 114993. 10.1016/j.ecoenv.2023.114993

Yuan, X., Li, Y., and Zhang, X. 2008. Effect of copper addition on the growth and the activities of protective enzymes in leaves of Brassica chinensis L. Journal of Agro-Environment Science (in Chinese) 27(2):467–471. https://kns.cnki.net/kcms2/article/abstract?v=j6HAoO1nZAz7slBtgW8MeA5v6IeLp4OsLBaoH56CwSbFd4tyo83QjOKopIhsDgV4XrstmQTHzjXFLR5Tu7bvHbvxf6LGsQMullbsI-bQjD97AsG7sPWbR29HBt_6ugS_INDidfsUyic=&uniplatform=NZKPT&language=CHS.

Yvette, C.M.M., Mamadou, T., Bertrand, Z.Z., Amina, A., Sadrac, O.O., Aline, B.N., Didier, B., Jules, R., Ndam, N., Zacharia, G., and Hassan, B.N. 2024. Evidence of heavy metal in soil, irrigation water and vegetable cultivated in peri-urban area of Yaoundé-Cameroon. Scientific African 25:e02280. 10.1016/j.sciaf.2024.e02280

Zubair, M., Shafqat, A., Jabben, N., Shafiq, M., Balal, R.M., Tahir M.A., Hashmi, M. M., Naqvi, S.A.A., Ali, N., Abbas, S.M., Shahid, M.A., Korany, S.M., Alsherif, E.A., and Alomrani, S.O. 2024. Enhancing cabbage resilience against heavy metal stress through silicon amendments and melatonin: a depth investigation. Scientia Horticulturae 324: 112571. 10.1016/j.scienta.2023.112571

Zunaidi, A.A., Lim, L.H., and Metali, F. 2023. Comparative assessment of the heavy metal phytoextraction potential of vegetables from agricultural soils: a field experiment. Heliyon 9(2):e13547. 10.1016/j.heliyon.2023.e13547

Zunaidi, A.A., Lim, L.H and Metali, F. 2024. Heavy metal tolerance and accumulation in the Brassica species (Brassica chinensis var. parachinensis and Brassica rapa L.): a pot experiment. Heliyon 10(8):e29528. 10.1016/j.heliyon.2024.e29528