Next Article in Journal
Linking Microstructure and Hydraulic Behavior in Cocopeat–Based Substrates Using Pore-Scale Flow Simulation and Micro-CT
Previous Article in Journal
Data-Driven Multi-Objective Optimization Design of Micro-Textured Wet Friction Pair
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Agriculture
Volume 15
Issue 20
10.3390/agriculture15202153
agriculture-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Synergistic Effects of Phosphorus and EDDS on Enhancing Phytoremediation Efficiency of Ricinus communis L. in Cu and Cd Co-Contaminated Soils

by
Wenying Liu
1,
Rongli Tang
1,
Xinlei Peng
2,
Xueting Yang
1,
Yi Wang
1 and
Hongqing Hu
2,*
1
Chongqing Academy of Agricultural Sciences, Chongqing 401329, China
2
College of Resources and Environment, Huazhong Agricultural University, Wuhan 430070, China
*
Author to whom correspondence should be addressed.
Agriculture 2025, 15(20), 2153; https://doi.org/10.3390/agriculture15202153
Submission received: 17 September 2025 / Revised: 12 October 2025 / Accepted: 15 October 2025 / Published: 16 October 2025
(This article belongs to the Section Agricultural Soils)
Browse Figures
Versions Notes

Abstract

The use of biodegradable chelating agents and fertilizer to improve phytoremediation is a cost-effective and environmental-friendly method for remediation of copper (Cu)- and cadmium (Cd)-polluted agricultural soil. A pot experiment was conducted to investigate the effects of phosphorus (P) fertilizer and the chelator ethylenediamine disuccinic acid (EDDS), both individually and in combination, on the phytoremediation efficiency of castor plants. The experiment included six treatments with three replicates, which were as follows: control (no P or EDDS), EDDS alone, P at 100 mg kg−1, P at 300 mg kg−1, P at 100 mg kg−1 + EDDS, and P at 300 mg kg−1 + EDDS. The results demonstrated that phosphorus significantly promoted the growth of castor plants. In the treatment in which 300 mg kg−1 P2O5 and 5.0 mmol kg−1 EDDS were added, the shoot dry weight and root dry weight increased by 42.0% and 67.6%, respectively, when compared to the treatment only applying EDDS, and this treatment significantly promoted the absorption of Cd by shoots of castor. In the absence of phosphorus application, EDDS significantly diminished the dry weight of castor roots by 27.3%. Nevertheless, it improved the concentrations of Cu in the shoots and roots of castor plants, which were 3.43 times and 3.27 times higher than those of the control, respectively. Furthermore, when combined with phosphorus fertilizers, EDDS further promoted the absorption of Cu and Cd in the shoots of castor, which significantly increased by 13.34 times and 0.47 times, respectively, with addition of 100 mg kg−1 phosphorus and 5.0 mmol kg−1 of EDDS compared with the control. Phosphorus and EDDS synergistically decreased the activity of POD enzymes in leaves and roots compared with those treated with only EDDS and alleviated the toxicity of EDDS and heavy metals to castor plants. These findings provide scientific evidence for the use of agronomic measures and chelators to optimize phytoremediation efficiency in Cu and Cd co-contaminated soils.

1. Introduction

In the last few decades, the continuous development of industry and agricultural activities has led to heavy metal pollution in agricultural soil [1,2]; the results of Adnan et al. (2024) [3] highlight the significance of heavy metal contamination caused by mining and smelting operations in China. Soil pollution by heavy metals has become a severe environmental problem around the world [4]. Copper (Cu) and cadmium (Cd) have become the main elements in combined pollution due to their high toxicity, mobility, and bioaccumulation. Cd is a major environmental contaminant and a nonessential element for plants, and the high toxicity and persistence of Cd in soil is related to plant metabolic disorders and crop reduction, which can cause negative effects on the growth of plants, food security, and human health [5,6,7,8]. Furthermore, Cd can be assimilated by plants’ roots and transported to shoots, and Cd2+ in plants can inhibit carbon assimilation by blocking Fe (III) reductase, which is a key enzyme in the photosynthetic pathway [9]. Cu is a significant microelement for living beings. However, its excessive presence in agriculture also damages plant growth and even poses a serious threat to living organisms via food chains [10]. Compared to single-source pollution, the interaction of heavy metals in combined pollution (such as the competitive adsorption of Cu and Cd) significantly increases the difficulty of remediating polluted soil [11,12]. Therefore, it is urgent to develop efficient and sustainable repair technologies to remediate large areas of Cu and Cd co-contaminated mine soil in China.
Phytoremediation refers to the removal of heavy metals by plant uptake and transport to above-ground areas, decreasing total heavy metals content in the soil, which has attracted considerable attention because it is a cost-effective, environmentally friendly, and operationally easy method [13]. Recently, many phytoremediation technologies have been used to repair heavy metals in soils with hyperaccumulators and other different types of plants [14,15]. For example, Cd hyperaccumulator plants that have been extensively studied include Amaranthus hypochondriacus [16], Bidens pilosa [17], Medicago sativa [18], and Solanum nigrum [19]. Cu hyperaccumulator plants, mainly including Ricinus communis L. [20], Elsholtzia splendens, and Silene vulgaris [21], have been used to remediate Cu-contaminated soil. Nevertheless, the efficiency of traditional phytoremediation techniques with hyperaccumulators is limited because of their low biomass [9,22]. The castor plant (Ricinus communis L.), which grows quickly and has a high biomass, developed root system, and strong ability to absorb heavy metals in mine soil, has garnered significant attention in phytoremediation research.
Recently, research emphasis has been put on improving the efficiency of phytoremediation by soil amendment with fertilizers and chelating agents or plants with a large biomass to improve the uptake and transport of heavy metals by plants [23]. In our previous study, P fertilizer not only enhanced the phytoremediation efficiency of R. communis on Cu- and Cd-contaminated soils, but it also facilitated detoxification [10,24,25]. Chelating agents enhance the efficiency of phytoremediation by altering the forms of heavy metals, enhancing plants’ uptake of Cd [26]. Meanwhile, EDDS has the advantages of being biodegradable and environmentally friendly, and it has been a research hotspot that promotes phytoremediation of heavy-metal-contaminated soil [27].
However, current research is mainly based on a single strengthening measure. There are limitations to a single measure. Although phosphate fertilizer can enhance the biomass of plants, it may immobilize heavy metals, with the soluble form of phosphate reducing the availability of heavy metals in soil [10,28]. Many studies have shown that applying EDDS 7–15 days before harvest can relieve the toxicity of EDDS to plants, but short-term interaction between EDDS and heavy metals is not conducive to improving the efficiency of phytoremediation [29,30]. Therefore, whether the combination of phosphate fertilizer and a chelating agent has a better phytoremediation efficiency needs to be further explored.
Therefore, this study was set up to evaluate the available Cu and Cd concentration and nutrient changes in soil caused by application of P fertilizer and EDDS, investigate the growth and detoxification mechanisms of castor, and analyze the differences in Cu and Cd absorption by castor with EDDS and phosphate fertilizer added.

2. Materials and Methods

2.1. Experiment Materials

Cu and Cd co-contaminated agricultural soil were collected from the tillage layer (0–20 cm) in Huangshi, Hubei Province, China (29°48′40″ N, 115°25′53″ E). Plant residues and gravel were removed from the soil, which was naturally air-dried and then passed through a 2 mm nylon sieve for later use in the pot experiments. The soil pH value was 7.79, the concentrations of total Cu, Cd, and P were 352 mg kg−1, 1.05 mg kg−1, and 0.70 g kg−1, respectively, and the concentrations of available Cu, Cd, and P were 5.51 mg kg−1, 0.22 mg kg−1, and 9.93 mg kg−1, respectively. The basic physical and chemical properties of soil were consistent with Liu et al. (2023) [25]. Analytical-grade pure reagent EDDS was purchased from Hefei Bomei Biotechnology Co., Ltd. (Hefei, China), which had a pH of 7.7 when dissolved in water. Castor seeds were obtained from Huangshi, Hubei Province. Seeds with a uniform size, full particles, and a smooth surface were selected, soaked in 75% alcohol for 30 s, and then washed 3–4 times with distilled water for further use.

2.2. Pot Experimental Design

A pot experiment was set up stochastically in a greenhouse at the Huazhong Agriculture University in 2021 with a room temperature of 25 °C. The pot experiment was carried out using plastic pots with a diameter of 15 cm and a height of 12 cm. We placed plastic bags at the bottom of the pots to prevent soil particles and nutrients from being lost, and 1.5 kg of air-dried soil was placed in each pot. Nitrogen and potassium fertilizers were uniformly added to the soils as fertilizers at doses of 100 mg N kg−1 soil and 100 mg K2O kg−1 soil. We added three levels of P fertilizer (Ca(H2PO4)2) to the soils, which were 0 (P0), 100 (P100) and 300 (P300) mg P2O5 kg−1 soil, respectively, and then equilibrated the soils for two weeks with deionized water to maintain the soil–water ratio at about 25%. Two weeks later, the sterilized castor seeds were put into the soils. When the seedlings reached the two-leaf stage, three seedlings with uniform sizes were kept in each pot. After 30 days of growing in Cu and Cd co-contaminated soils, the castor seedlings were treated with 0 or 5 mmol kg−1 of EDDS, which was added directly to each pot of soil in the form of a solution. The treatment without phosphate fertilizer or EDDS was the control (CK). The castor was harvested and separated into shoots and roots for further analysis 30 days after the application of EDDS, and each treatment was replicated three times.

2.3. Soil Solution Analysis

We collected rhizosphere soil at harvest, removed plant residues, dried the soil naturally, and sieved it through a 2 mm mesh and 0.15 mm mesh. In accordance with to Bao (2000) [31], we determined the basic chemical properties of the soil. The soil pH was measured by pH meter (Mettler-Toledo FE20, Shanghai, China) at a soil-to-CO2-free distilled water ratio of 1:2.5 (v/v). The soil-available P was extracted by 0.5 mol L−1 NaHCO3 and P in the extraction solution was determined by the molybdenum blue method. The soil-available Cu and Cd were extracted by 0.005 mol L−1 DTPA extraction solution (pH 7.3) at a ratio of 1:5 (w/v), and the Cu and Cd concentrations were determined by atomic absorption spectrophotometer (AAS, Varian 240FS, Melbourne, Australia). The concentration of soil NH4+-N was determined with 2 mol L−1 potassium chloride (KCl) extraction at a ratio of 1:5 (w/v) and the concentration of soil NO3−-N was determined with saturated calcium sulfate solution (CaSO4). The soil DOC content was extracted using a 1:5 (w/v) soil-to-water ratio, centrifuged by oscillation, and then filtered with a 0.45 µm filter membrane and determined using a TOC instrument (Vario, Hessen, Germany). The soils were digested with HCl-HNO3-HClO4 (3:1:1) by the following steps: we weighed 0.2000 g dried soil in a 50 mL triangular flask, and then added a 10 mL mixture of HCl and HNO3 (3:1), digested at 180 °C, and, after the brown oxide was basically removed, added 2.5 mL HClO4. The digested solutions were diluted to 100 mL with distilled water. The P concentrations in the digested solutions were determined by a spectrophotometer (UV-1500, Shanghai, China), and the Cu and Cd concentrations were determined by atomic absorption spectrophotometer (AAS, Varian 240FS).

2.4. Cu, Cd, N, and P in Castor

The two plant samples were collected, separated into shoots and roots, and washed with tap water and distilled water separately. The plants were dried in an oven at 65 °C to constant weight, and then we recorded their dry weight. The total Cu and Cd concentrations in the roots and shoots were determined by the following steps: A total of 0.5 g dried plant roots and shoots were digested with 10 mL mixed HNO3-HClO4 (4:1) [32]. The digested solutions were diluted to 50 mL with distilled water, and the Cu and Cd in the extraction solution were analyzed through the same method as the soil extraction solution above. The plants were digested with H2SO4 and H2O2 to measure N and P concentrations.
The Cu and Cd transport capacities from roots to shoots were assessed by calculating the transfer factor (TF) values of Cu and Cd in shoots as follows:
TF-Cu = [Cu in shoots]/[Cu in roots]
TF-Cd = [Cd in shoots]/[Cd in roots]
where Cu in shoots, Cu in roots, Cd in shoots, and Cd in roots are the concentrations (mg kg−1).

2.5. Chlorophyll, Lipid Peroxidation, and Antioxidative Enzymes in Castor

One plant from each pot at harvest was collected and immediately frozen with liquid nitrogen and then stored in a −80 °C refrigerator. The third leaf from the top was taken to determine the content of the plant’s physiological index. Briefly, photosynthetic pigments were determined using a modified method based on Mesnoua et al. (2016) [33]. Malondialdehyde (MDA) was measured using 2-thiobarbituric acid (TBA) as described by Wang et al. (2010) [34].
The activity of antioxidative enzymes was measured according to the following steps: A 0.5000 g fresh sample was homogenized in a buffer solution (5 mL potassium phosphate, pH 7.8) under pre-chilled conditions, and the supernatant was stored at 4 °C for further analysis. Total superoxide dismutase (SOD) activity was assayed using the NBT-illumination method [35]. Glutathione (POD) was determined by guaiacol colorimetry, also based on Cao et al. (2022) [35]. Catalase (CAT) activity was measured following the degradation of H2O2 (1 mL 0.3%) for 60 s at 240 nm [36].

2.6. Statistical Analysis

All the data were analyzed by Microsoft Office Excel 2007 and SPSS Statistics (IBM SPSS 22.0) using Duncan’s multiple comparison test at a significance level of p < 0.05. All figures were made using Origin 8.5. In all figures and tables, data are shown as mean value ± standard error (SE), n = 3.

3. Results

3.1. Uptake and Translocation of Cu and Cd by Castor

There was a significant enhancement in Cu in the shoots and roots of castor plants with addition of EDDS to Cu and Cd co-contaminated soil when compared to plants without EDDS treatment (Table 1). An addition of 5.0 mmol kg−1 EDDS to the soil in the absence phosphorus treatment increased the Cu concentration by 3.43 times and 3.27 times, respectively, in shoots and roots (p < 0.05). The application of P fertilizer significantly increased Cd concentration in the shoots of castor plants, but there was no promotional effect for Cu uptake.
Combined treatment with phosphorus and EDDS further promoted the absorption of Cu and Cd in the shoots of castor plants. The Cu and Cd concentrations in the shoots of plants treated with addition of 100 mg kg−1 P5O2 and 5.0 mmol kg−1 EDDS significantly increased by 13.34 times and 0.47 times, respectively (p < 0.05), when compared with the treatments without phosphorus and EDDS.
Figure 1a shows that applying EDDS or phosphorus fertilizer alone has no significant effect on the transport coefficient of Cu from roots to shoots in castor plants, while applying phosphorus and then adding EDDS significantly promoted the transport of Cu to above-ground areas. The TFs of Cu in the castor plants treated with P100+EDDS and P300+EDDS were 0.53 and 0.33, respectively. Simultaneously, the TF of Cu increased by 3.82 times in plants treated with P100+EDDS when compared with plants treated with P100-EDDS and P0+EDDS (p < 0.05).
Figure 1b shows that EDDS and phosphorus fertilizer significantly promoted the transport of Cd from the roots to the shoots of castor plants. Applying 300 mg kg−1 P5O2 alone, the TF of Cd was 0.76, which increased by 484.6% compared to in the CK treatment (p < 0.05). The TF-Cd value was further increased under the P300+EDDS treatment, increasing by 114.5% and 918.8% as compared to under the P300-EDDS and P0+EDDS treatments (p < 0.05). However, applying 100 mg kg−1 P5O2 or 5.0 mmol kg−1 EDDS alone had no significant effects on the TF-Cd of castor plants.

3.2. The Growth of Castor Plants Under P and EDDS Treatments

The growth of castor plants under all treatments is shown in Figure 2. EDDS or 100 mg kg−1 P5O2 alone caused no significant differences in shoot dry weights. The dry weights of shoots increased significantly in plants treated with P300-EDDS and P300+EDDS. For the P300+EDDS treatment, the shoot dry weights increased by 38.5% and 42.0%, respectively, compared with the CK and P0-EDDS treatments (p < 0.05).
Nevertheless, EDDS had a negative effect on root growth, but phosphate fertilizer had a positive effect on promoting root growth. In the absence of phosphorus application, the addition of EDDS to the soil significantly reduced the dry weights of castor roots by 27.3% (p < 0.05). After adding 300 mg kg−1 P5O2 and 5.0 mmol kg−1 EDDS, the roots dry weights increased by 78.7% and 67.6%, respectively, compared to under the P100+EDDS and P0+EDDS treatments (p < 0.05).
Therefore, phosphorus application could promote the growth of castor plants. However, adding EDDS alone reduced the root dry weight of castor plants, and application of phosphorus fertilizer and EDDS combined alleviated the stress effect of EDDS on root growth.

3.3. Chlorophyll and Carotenoid Content in Leaves of Castor Plants Under Various Treatments

The changes in chlorophyll a, chlorophyll b, and carotenoid content in castor leaves after phosphorus application and EDDS addition are shown in Figure 3. Increasing P levels in the soil had no significant effect on chlorophyll and carotenoid content, while a promoting effect appeared when 5.0 mmol kg−1 EDDS was applied to soil. For example, in the non-phosphorus treatment, adding 5.0 mmol kg−1 EDDS increased the chlorophyll a content from 1.34 mg g−1 to 1.64 mg g−1. The P100+EDDS treatment resulted in an increase of 25.2% in leaf chlorophyll a content compared to the EDDS-free treatment, and P300+EDDS resulted in an increase of 22.6% compared to the P300-EDDS treatment.
The content of chlorophyll b increased with the addition of EDDS. Under the P100+EDDS treatment, the chlorophyll b content increased significantly by 24.5% compared with under the P100-EDDS, Under the P300+EDDS treatment, the chlorophyll b content increased significantly by 19.3% compared with the P300-EDDS treatment.
EDDS significantly improved the leaf carotenoid content of castor plants under all treatments. For the treatment with only addition of EDDS, the carotenoid content increased by 16.67% compared with the CK treatment. Under the P100+EDDS treatment, the carotenoid content increased significantly by 18.0% compared with the P100-EDDS treatment.

3.4. The Effect of MDA Content of Castor Plants Treated with P and EDDS

Malondialdehyde (MDA) content in leaves and roots of castor plants is shown in Figure 4. The application of phosphate fertilizer decreased the MDA content in leaves compared with the CK. The MDA content in leaves significantly declined by 14.48% and 19.02% (p < 0.05) under the P100-EDDS and P300-EDDS treatments compared with the CK, respectively. Simultaneously, EDDS-treated leaves had lower MDA levels compared with leaves that were not treated with EDDS.
In contrast, the MDA content of roots increased under the P300-EDDS treatment, but the difference was not significant compared to the CK. Under the same phosphorus application level, adding 5 mmol kg−1 EDDS increased the MDA content in the roots of castor plants. For example, the highest content of MDA (5.83 nmol g−1) was recorded in castor roots under the P100+EDDS treatment, which were increased by 64.7% compared to the CK (p < 0.05).

3.5. Antioxidant Enzyme Activities of Leaves and Roots of Castor Plants Under Various Treatments

There were different changes in the activities of antioxidant enzymes in leaves and roots of castor plants treated with phosphate fertilizer and EDDS (Figure 5). Applying phosphate fertilizer alone had no significant effects on the activities of POD, CAT and SOD enzymes in leaves and roots (p > 0.05). However, in the absence of the phosphate fertilizer treatment, castor plants treated with EDDS had significantly increased POD activities both in leaves and roots tissues by 128.8% and 116.0% (p < 0.05). Simultaneously, addition of only EDDS to soil promoted CAT activities and SOD activities in the roots of castor plants, but there were no significant promotion effects. Furthermore, combined application of phosphorus fertilizer and EDDS significantly decreased POD activities in leaves and roots of castor plants when compared to plants treated only with EDDS.

3.6. N and P Concentrations in Leaves and Roots of Castor Plants

The N and P changes in leaves and roots are shown in Figure 6. There was no significant effect on the nitrogen content in the aboveground parts of castor plants when phosphorus fertilizer and EDDS alone or in combination were added. Nevertheless, for the P0+EDDS and P100+EDDS treatments, N concentrations in the roots were significantly promoted by 43.2% and 44.9% (p < 0.05), respectively, when compared to the CK. There was an improvement in P concentrations in the roots of castor plants after addition of P fertilizer and EDDS (Figure 6b,d). Under the P100-EDDS and P300-EDDS treatments, the P concentrations of roots were increased by 78.4% and 61.4% (p < 0.05), respectively, as compared with the P0-EDDS treatment. Without phosphorus treatment, addition of EDDS increased the root P concentration by 121.6% as compared with the CK (p < 0.05). The addition of EDDS or phosphorus fertilizer had no significant promotional effect for P concentrations in the shoots of castor plants.

3.7. The Changes in Soil Properties

The physicochemical properties in soil after phosphorus and EDDS treatment are shown in Table 2. Under the non-phosphorus treatment, the soil pH increased by 0.1 units with addition of EDDS. The application of phosphorus fertilizer increased soil pH by 0.2 units, and the co-addition of phosphorus and EDDS had no significant effects on soil pH.
Phosphorus application significantly increased the soil-available phosphorus content. Under the P100-EDDS and P300-EDDS treatments, the available P concentrations were significantly improved by 45.1% and 153.0% compared to the P0-EDDS treatment, respectively (p < 0.05). Under phosphorus application, adding 5.0 mmol kg−1 EDDS further increased soil-available P concentrations, the P100+EDDS treatment showed an increase of 40.0% compared to the P100-EDDS treatment, and the available P concentrations in the P300+EDDS treatment were 27.81 mg kg−1, which increased by 4.81 mg kg−1 compared to the P300-EDDS treatment.
Under low phosphorus conditions, the NH4+-N concentrations in soil were significantly increased with application of EDDS. The soil NH4+-N concentrations were increased by 14.1% when only EDDS was added compared to the CK, and in the P100+EDDS treatment, it increased by 21.3% compared to in the P100-EDDS treatment. P fertilizer alone significantly decreased soil NO3−-N concentrations. The addition of EDDS in the absence of P fertilizer significantly increased soil NO3−-N concentrations; the soil NO3−-N concentration increased from 4.29 mg kg−1 to 22.54 mg kg−1. Furthermore, when the phosphorus application rate was 100 mg kg−1 P2O5, the soil NO3−-N concentration was increased by 7.40 times after addition of EDDS when compared to the P100-EDDS treatment (p < 0.05). Under the P300+EDDS treatment, the soil NO3−-N concentration significantly increased by 14.16 times compared to the P300-EDDS treatment (p < 0.05).
The lone addition of EDDS increased the DOC concentration in the soil, but the effect of P fertilizer alone on the DOC was not significant. The co-application of phosphorus and EDDS was more conducive to increasing soil DOC content. The soil DOC content under the P100+EDDS treatment reached its maximum value (162.96 mg kg−1), while the soil DOC content under the P300+EDDS treatment took second place, with a significant increase of 46.87% compared to the P300-EDDS treatment (p < 0.05).
In summary, phosphorus application significantly increased the content of soil-available phosphorus but decreased the content of soil NH4+-N and NO3−-N. The addition of EDDS increased the content of soil NH4+-N, NO3−-N, and DOC. The combined action of phosphorus and EDDS further increased the content of soil-available phosphorus and DOC.
The effects of EDDS on soil-available Cu and Cd vary under different phosphorus levels (Figure 7). In the treatment without phosphorus fertilizer, EDDS treatment was relatively more effective in promoting available Cu and Cd in the soil, thus they increased by 40.7% and 47.8% (p < 0.05), respectively. Nevertheless, in the P300+EDDS treatment, the content of available Cu and Cd in the soil was reduced relative to the P300-EDDS treatment.

4. Discussion

4.1. Castor Growth in Cd/Cu Co-Contaminated Soil Under P and EDDS Application

Plant biomass played a vital role in affecting soil Cu and Cd extraction [38,39]. Castor growth was facilitated by the addition of phosphate fertilizer in this study because P could directly promote the growth of castor plants and alleviated the toxicity of heavy metals to plants [40,41]. Yu et al. (2020) [42] showed that the application of phosphorus promoted the growth of Polygonum pubescens blume in Mn-contaminated soil and increased their biomass by 135%. There was no inhibiting impact on shoot growth of castor plants under EDDS treatments in our study, which could have been because EDDS did not directly act on the shoots, hence the stress on the shoots was low. Secondly, the final decomposition products of EDDS were CO2 and NH4+-N, and then NH4+-N was converted into NO3−-N through nitrification [43], which added to the content of NH4+-N and NO3−-N in the soil and promoted plant uptake of nitrogen. However, under the same phosphorus level, the root biomass was diminished and the MDA of root was increased with EDDS added. In a study by Kaurin et al. (2020) [44], similar conclusions were reached; the researchers found that the growth of buckwheat in EDDS-washed soil was 67% suppressed. These results might be explained by the chelates formed by heavy metals and EDDS, those chelates facilitated the uptake of heavy metals by plants, hence destroying root channel cells [45]. On the other hand, the increased Cu concentrations in the castor roots generated stress to the plant roots (Table 1) and damaged its membranous organelles [9].
Plants have their own regulatory mechanisms to combat oxidative damage and alleviate the toxicity of heavy metals [35], such as plants activating antioxidative defense mechanisms by increasing antioxidant defense system enzyme activity (SOD, POD, CAT, etc.) [46]. In this study, the application of EDDS in the absence of phosphorus treatment significantly improved the activity of POD enzymes in roots and leaves of castor plants (Figure 6). However, when EDDS was added to the phosphorus treatment, POD enzyme activity was reduced in roots and leaves compared with P0+EDDS, which may be because P fertilizer alleviated the heavy metal and EDDS stress on the castor plants. Therefore, the stress of heavy metals and EDDS on plants, under different phosphorus application levels, lead to different changes in plant antioxidant defense systems.

4.2. Plant Uptake of Cu and Cd Under Different Treatments

The bioavailability of heavy metals in soil was another crucial factor affecting the efficiency of phytoremediation. Chelants formed stable complexes with heavy metal ions, which increased the solubility and mobility of heavy metals in soil. Our previous soil cultivation experiments have found that application of EDDS significantly improved the available and weak acid extraction state Cu and Cd concentrations in soil [37], and in this study, EDDS increased the available Cu and Cd concentrations without phosphorus addition after harvesting (Figure 7), which promoted castor uptake of Cu and Cd. Zulkernain et al. (2023) [14] indicated that chelating agents enhance the rate of metal uptake and transport up to 45% of it from roots to shoots during PTE phytoremediation. According to Wang et al. (2018) [47], in soil contaminated to different degrees with Cu, the addition of 5 mmol kg−1 EDDS increased the Cu concentration in the shoots of Commelina communis L. by 15.0–47.0%. Biodegradable chelators and slightly soluble heavy metals formed water-soluble heavy metal-chelating agents [48,49], accordingly facilitating the mobilization of heavy metals in soil and their accumulation by plants [50].
The results showed that addition of EDDS effectively enhanced Cu uptake in castor plants; however, phosphorus application alone had no significant promoting effects on Cu uptake. Simultaneously, EDDS displayed differences in promoting Cu absorption by castor plants under different phosphorus application levels. The P300+EDDS treatment reduced the concentrations of Cu in roots and shoots compared to P100+EDDS, maybe because the high concentration of phosphorus reduced available Cu in the soil. Moreover, EDDS increased the transfer coefficient of Cu in castor plants, and the combined effect of phosphorus and EDDS further promoted the transport of Cu to shoots, indicating that EDDS increased the mobility of heavy metals and promoted plant absorption. Zhao et al. (2016) [51] had a similar conclusion that EDDS significantly increases the concentration of Pb in the stems of P. sinensis and increases the transport coefficient of Pb.
EDDS increased the shoot Cd concentration of castor plants, but decreased the root Cd concentration (Table 1). Cd mainly accumulated in castor roots, and the transfer of Cd was affected by the stomatal conductance and transpiration rate of plants [39], which differed from the transfer of Cu. Our results demonstrated that the application rate was 300 mg kg−1 P2O5, and addition of EDDS was more conducive to promoting the transport of Cd to above-ground areas and enhanced the accumulation of Cd in castor shoots.
This difference in castor uptake of Cu and Cd may be caused by factors such as different mobilities of Cd and Cu in soil, different thermal stability with EDDS, different concentrations of Cu and Cd in soil, and differences in plant uptake and transport of Cu and Cd themselves.
The increase in above-ground heavy metal phytoextraction was more conducive to indicating the effect of auxiliary measures in promoting phytoremediation. In this study, combined application of phosphate fertilizer and EDDS was more conducive to the phytoextraction of Cu and Cd by castor plants.

5. Conclusions

In the present study, P fertilizer significantly promoted the growth of castor plants, improved their dry weights, and facilitated the transport of Cd to their shoots. However, EDDS increased the malondialdehyde (MDA) content of castor roots, inhibited the growth of the roots of castor plants, and reduced root biomass. Simultaneously, EDDS significantly influenced Cu extraction in castor plants, improved the Cu concentration in shoots, and promoted the transfer of Cu to shoots. When phosphorus and EDDS are applied in combination, they significantly promoted the growth of castor plants, alleviated plant stress, promoted the transport of heavy metals to castor shoots, increased the Cu and Cd contents in the shoots of castor plants, and improved the efficiency of phytoremediation. These findings demonstrate that the combined application of phosphate fertilizer and ethylenediamine disuccinic acid (EDDS) significantly enhances phytoextraction efficiency of castor plants in copper (Cu) and cadmium (Cd) co-contaminated soils by reducing heavy metal concentrations in soils.

Author Contributions

Conceptualization, W.L.; methodology, W.L.; validation, W.L. and X.Y.; formal analysis, W.L.; investigation, W.L., Y.W. and X.P.; resources, H.H.; writing–original draft preparation, W.L. and R.T.; writing–review and editing, H.H. and R.T.; supervision, H.H.; project administration, H.H.; funding acquisition, Y.W. and X.Y. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by Performance Incentive Guidance for Scientific Research Institution of Chongqing (CSTB2024JXJL-YFX0015) and Chongqing Natural Science Foundation (CSTB2023NSCQ-MSX0436).

Data Availability Statement

The original contributions presented in this study are included in the article. Further inquiries can be directed to the corresponding author.

Conflicts of Interest

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.

References

  1. Ren, S.; Song, C.; Ye, S.; Cheng, C.; Gao, P. The spatiotemporal variation in heavy metals in China’s farmland soil over the past 20 years: A meta-analysis. Sci. Total Environ. 2022, 806, 150322. [Google Scholar] [CrossRef] [PubMed]
  2. Shi, J.; Zhao, D.; Ren, F.; Huang, L. Spatiotemporal variation of soil heavy metals in China: The pollution status and risk assessment. Sci. Total Environ. 2023, 871, 161768. [Google Scholar] [CrossRef]
  3. Adnan, M.; Xiao, B.; Ali, M.; Xiao, P.; Zhao, P.; Wang, H.; Bibo, S. Heavy metals pollution from smelting activities: A threat to soil and groundwater. Ecotoxicol. Environ. Saf. 2024, 274, 116189. [Google Scholar] [CrossRef] [PubMed]
  4. Pouresmaieli, M.; Ataei, M.; Forouzandeh, P.; Azizollahi, P.; Mahmoudifard, M. Recent progress on sustainable phytoremediation of heavy metals from soil. J. Environ. Chem. Eng. 2022, 10, 108482. [Google Scholar] [CrossRef]
  5. Awan, S.; Khan, I.; Rizwan, M.; Irshad, M.; Wang, X.; Zhang, X.; Huang, L. Reduction in the cadmium (Cd) accumulation and toxicity in pearl millet (Pennisetum glaucum L.) by regulating physio-biochemical and antioxidant defense system via soil and foliar application of melatonin. Environ. Pollut. 2023, 328, 121658. [Google Scholar] [CrossRef]
  6. Wu, S.; Yang, Y.; Qin, Y.; Deng, X.; Zhang, Q.; Zou, D.; Zeng, Q. Cichorium intybus L. is a potential Cd-accumulator for phytoremediation of agricultural soil with strong tolerance and detoxification to Cd. J. Hazard. Mater. 2023, 451, 131182. [Google Scholar] [CrossRef]
  7. Wang, Y.; Xu, Y.; Qin, X.; Liang, X.; Huang, Q.; Peng, Y. Effects of EDDS on the Cd uptake and growth of Tagetes patula L. and Phytolacca americana L. in Cd-contaminated alkaline soil in northern China. Environ. Sci. Pollut. Res. 2020, 27, 25248–25260. [Google Scholar] [CrossRef]
  8. Yu, L.; Chen, S.; Wang, J.; Qin, L.; Sun, X.; Zhang, X.; Wang, M. Environmental risk thresholds and prediction models of Cd in Chinese agricultural soils. Sci. Total Environ. 2024, 906, 167773. [Google Scholar] [CrossRef]
  9. Xu, L.; Li, J.; Najeeb, U.; Li, X.; Pan, J.; Huang, Q.; Zhou, W.; Liang, Z. Synergistic effects of EDDS and ALA on phytoextraction of cadmium as revealed by biochemical and ultrastructural changes in sunflower (Helianthus annuus L.) tissues. J. Hazard. Mater. 2020, 407, 124764. [Google Scholar] [CrossRef]
  10. Zhou, X.; Wang, S.; Liu, Y.; Huang, G.; Yao, S.; Hu, H. Coupling phytoremediation efficiency and detoxification to assess the role of P in the Cu tolerant Ricinus communis L. Chemosphere 2020, 247, 125965. [Google Scholar] [CrossRef]
  11. Sheng, P.; Ting, Y.; Chen, J. Biosorption of heavy metal ions (Pb, Cu and Cd) from aqueous solutions by the marine alga Sargassum sp. in single-and multiple-metal systems. Ind. Eng. Chem. Res. 2007, 46, 2438–2444. [Google Scholar] [CrossRef]
  12. Cerqueira, B.; Covelo, E.; Andrade, L.; Vega, F. The influence of soil properties on the individual and competitive sorption and desorption of Cu and Cd. Geoderma 2011, 162, 20–26. [Google Scholar] [CrossRef]
  13. Yang, Z.; Yang, F.; Liu, J.; Wu, H.; Yang, H.; Shi, Y.; Liu, J.; Zhang, Y.; Luo, Y.; Chen, K. Heavy metal transporters: Functional mechanisms, regulation, and application in phytoremediation. Sci. Total Environ. 2022, 809, 151099. [Google Scholar] [CrossRef]
  14. Zulkernain, N.; Uvarajan, T.; Ng, C. Roles and significance of chelating agents for potentially toxic elements (PTEs) phytoremediation in soil: A review. J. Environ. Manag. 2023, 341, 117926. [Google Scholar] [CrossRef]
  15. Han, M.; Ullah, H.; Huan, Y.; Yu, G.; You, S.; Liu, J.; Chen, B.; Shahab, A.; Antoniadis, V.; Shaheen, S.; et al. Cadmium uptake and membrane transport in roots of hyperaccumulator Amaranthus hypochondriacus L. Environ. Pollut. 2023, 331, 121846. [Google Scholar] [CrossRef] [PubMed]
  16. Xie, Y.; Luo, Y.; Sheng, M.; Peng, H.; Gu, Y.; Xu, H.; Zhao, Y. 24-Epibrassinolide combined with heavy metal resistant bacteria enhancing phytoextraction of Amaranthus hypochondriacus L. in Cd-contaminated soil. J. Hazard. Mater. 2020, 399, 123031. [Google Scholar] [CrossRef]
  17. Zhang, X.; Gu, P.; Liu, X.; Huang, X.; Wang, J.; Zhang, S.; Ji, J. Effect of crop straw biochars on the remediation of Cd-contaminated farmland soil by hyperaccumulator Bidens pilosa L. Ecotoxicol. Environ. Saf. 2021, 219, 112332. [Google Scholar] [CrossRef]
  18. Chen, L.; Beiyuan, J.; Hu, W.; Zhang, Z.; Duan, C.; Cui, Q.; Zhu, X.; He, H.; Huang, X.; Fang, L. Phytoremediation of potentially toxic elements (PTEs) contaminated soils using alfalfa (Medicago sativa L.): A comprehensive review. Chemosphere 2022, 293, 133577. [Google Scholar] [CrossRef]
  19. Al-Huqail, A. Stimulating the efficiency of Cd-phytoremediation from contaminated soils by Solanum nigrum L.: Effect of foliar and soil application of yeast extract. S. Afr. J. Bot. 2023, 161, 512–518. [Google Scholar] [CrossRef]
  20. Wang, S.; Zhao, Y.; Guo, J.; Zhou, L. Effects of Cd, Cu and Zn on Ricinus communis L. growth in single element or co-contaminated soils: Pot experiments. Ecol. Eng. 2016, 90, 347–352. [Google Scholar] [CrossRef]
  21. Song, J.; Zhao, F.; Luo, Y.; McGrath, S.; Zhang, H. Copper uptake by Elsholtzia splendens and Silene vulgaris and assessment of copper phytoavailability in contaminated soils. Environ. Pollut. 2004, 128, 307–315. [Google Scholar] [CrossRef]
  22. Yao, S.; Zhou, B. Enhancing phytoremediation of cadmium and arsenic in alkaline soil by Miscanthus sinensis: A study on the synergistic effect of endophytic fungi and biochar. Sci. Total Environ. 2024, 923, 171458. [Google Scholar] [CrossRef] [PubMed]
  23. Guo, J.; Lei, M.; Yang, J.; Yang, J.; Wan, M.; Chen, T.; Zhou, X.; Gu, S.; Guo, G. Effect of fertilizers on the Cd uptake of two sedum species (Sedum spectabile Boreau and Sedum aizoon L.) as potential Cd accumulators. Ecol. Eng. 2017, 106, 409–414. [Google Scholar] [CrossRef]
  24. Huang, G.; Rizwan, M.; Ren, C.; Guo, G.; Fu, Q.; Zhu, J.; Hu, H. Influence of phosphorous fertilization on copper phytoextraction and antioxidant defenses in castor bean (Ricinus communis L.). Environ. Sci. Pollut. Res. 2018, 25, 115–123. [Google Scholar] [CrossRef]
  25. Liu, W.; Gao, J.; Wan, X.; Li, Q.; Fu, Q.; Zhu, J.; Hu, H. Effect of phosphorus fertilizer on phytoextraction using Ricinus communis L. in Cu and Cd co-contaminated soil. Int. J. Phytorem. 2023, 25, 822–831. [Google Scholar] [CrossRef]
  26. Chen, L.; Yang, J.; Wang, D. Phytoremediation of uranium and cadmium contaminated soils by sunflower (Helianthus annuus L.) enhanced with biodegradable chelating agents. J. Clean. Prod. 2020, 263, 121491. [Google Scholar] [CrossRef]
  27. Epelde, L.; Hernández-Allica, J.; Becerri, J.M.; Blanco, F.; Garbisu, C. Effects of chelates on plants and soil microbial community: Comparison of EDTA and EDDS for lead phytoextraction. Sci. Total Environ. 2008, 401, 21–28. [Google Scholar] [CrossRef] [PubMed]
  28. Wang, H.; Wang, T.; Ahmad, I. Involvement of phosphate supplies in different transcriptional regulation pathway of Oryza sativa L.’s antioxidative system in response to arsenite and cadmium stress. Ecotoxicology 2015, 24, 1259–1268. [Google Scholar] [CrossRef]
  29. Wang, K.; Liu, Y.; Song, Z.; Wang, D.; Qiu, W. Chelator complexes enhanced Amaranthus hypochondriacus L. phytoremediation efficiency in Cd-contaminated soils. Chemosphere 2019, 237, 124480–124488. [Google Scholar] [CrossRef]
  30. Wang, Y.; Xu, Y.; Qin, X.; Zhao, L.; Liang, X. Effects of s,s-ethylenediamine disuccinic acid on the phytoextraction efficiency of Solanum nigrum L. and soil quality in cd-contaminated alkaline wheat soil. Environ. Sci. Pollut. Res. 2021, 28, 42959–42974. [Google Scholar] [CrossRef]
  31. Bao, S. Agro-Chemical Analysis for Soil; Chinese Agricultural Press: Beijing, China, 2000. [Google Scholar]
  32. Wu, X.; Song, H.; Guan, C.; Zhang, Z. Boron mitigates cadmium toxicity to rapeseed (Brassica napus) shoots by relieving oxidative stress and enhancing cadmium chelation onto cell walls. Environ. Pollut. 2020, 263, 114546. [Google Scholar] [CrossRef] [PubMed]
  33. Mesnoua, M.; Mateos-Naranjo, E.; Barcia-Piedras, J.; Perez-Romero, J.; Lotmani, B.; Redondo-Gomez, S. Physiological and biochemical mechanisms preventing Cd-toxicity in the hyperaccumulator Atriplex halimus L. Plant Physiol. Biochem. 2016, 106, 30–38. [Google Scholar] [CrossRef]
  34. Wang, C.; Zhang, S.; Wang, P.; Li, W.; Lu, J. Effects of ammonium on the antioxidative response in Hydrilla verticillata (L.f.) Royle plants. Ecotoxicol. Environ. Saf. 2010, 73, 189–195. [Google Scholar] [CrossRef]
  35. Cao, X.; Cui, X.; Xie, M.; Zhao, R.; Xu, L.; Ni, S.; Cui, Z. Amendments and bioaugmentation enhanced phytoremediation and micro-ecology for PAHs and heavy metals co-contaminated soils. J. Hazard. Mater. 2022, 426, 128096. [Google Scholar] [CrossRef]
  36. Aebi, H. Catalase in vitro. Methods Enzymol. 1984, 105, 121–126. [Google Scholar] [CrossRef]
  37. Liu, W.; Wu, G.; Hu, H. Effect of EDDS application on soil Cu/Cd availability and uptake/transport by castor. Environ. Sci. 2024, 45, 1803–1811. [Google Scholar] [CrossRef]
  38. Janssen, J.; Weyens, N.; Croes, S.; Beckers, B.; Meiresonme, L.; Peteghem, P.; Carleer, R.; Vangronsveld, J. Phytoremediation of metal contaminated soil using willow: Exploiting plant-associated bacteria to improve biomass production and metal uptake. Int. J. Phytorem. 2015, 17, 1123–1136. [Google Scholar] [CrossRef]
  39. Li, Y.; Xie, T.; Zha, Y.; Du, W.; Yin, Y.; Guo, H. Urea-enhanced phytoremediation of cadmium with willow in pyrene and cadmium contaminated soil. J. Hazard. Mater. 2020, 405, 124257. [Google Scholar] [CrossRef]
  40. Gupta, D.; Chatterjee, S.; Datta, S.; Veer, V.; Walther, C. Role of phosphate fertilizers in heavy metal uptake and detoxification of toxic metals. Chemosphere 2014, 108, 134–144. [Google Scholar] [CrossRef] [PubMed]
  41. Wang, B.; Xie, Z.; Chen, J.; Jiang, J.; Su, Q. Effects of field application of phosphate fertilizers on the availability and uptake of lead, zinc and cadmium by cabbage (Brassica chinensis L.) in a mining tailing contaminated soil. J. Environ. Sci. 2008, 20, 1109–1117. [Google Scholar] [CrossRef] [PubMed]
  42. Yu, F.; Li, C.; Dai, C.; Liu, K.; Li, Y. Phosphate: Coupling the functions of fertilization and passivation in phytoremediation of manganese-contaminated soil by Polygonum pubescens blume. Chemosphere 2020, 260, 127651. [Google Scholar] [CrossRef]
  43. Ju, W.; Duan, C.; Liu, L.; Jin, X.; Bravo-Ruiseco, G.; Mei, Y.; Fang, L. Reduction of Cu and nitrate leaching risk associated with EDDS-enhanced phytoextraction process by exogenous inoculation of plant growth promoting rhizobacteria. Chemosphere 2022, 287, 132288. [Google Scholar] [CrossRef] [PubMed]
  44. Kaurin, A.; Gluhar, S.; Tilikj, N.; Lestan, D. Soil washing with biodegradable chelating agents and EDTA: Effect on soil properties and plant growth. Chemosphere 2020, 260, 127673. [Google Scholar] [CrossRef] [PubMed]
  45. Zhao, Y.; Cui, J.; Chan, T.; Chen, Y.; Li, X. Mechanistic insight into the interactions of EDDS with copper in the rhizosphere of polluted soils. Environ. Pollut. 2020, 267, 115453. [Google Scholar] [CrossRef]
  46. Khilji, S.; Waseem, M.; Tariq, S.; Jabeen, S.; Jamal, A.; Alomranil, S.; Javed, T.; Riaz, A. Microbe assisted phytoremediation of heavy mental contaminated soil by using African marigold (Tagetes erecta L.). Plant Stress 2024, 11, 100369. [Google Scholar] [CrossRef]
  47. Wang, J.; Zhu, Q.; Shan, Y.; Wang, Y.; Song, X.; Lei, X. A comparative study on the efficiency of biodegradable EDDS and micro-electric field on the promotion of the phytoextraction by Commelina communis L. in Cu-contaminated soils. Geoderma 2018, 314, 1–7. [Google Scholar] [CrossRef]
  48. Jalali, M.; Khanlari, Z. Redistribution of fractions of zinc, cadmium, nickel, copper, and lead in contaminated calcareous soils treated with EDTA. Arch. Environ. Contam. Toxicol. 2007, 53, 519–532. [Google Scholar] [CrossRef]
  49. Sarkar, D.; Andra, S.; Saminathan, S.; Datta, R. Chelant-aided enhancement of lead mobilization in residential soils. Environ. Pollut. 2008, 156, 1139–1148. [Google Scholar] [CrossRef]
  50. Yin, F.; Li, J.; Wang, Y.; Yang, Z. Biodegradable chelating agents for enhancing phytoremediation: Mechanism, market feasibility, and future studies. Ecotoxicol. Environ. Saf. 2024, 272, 116113. [Google Scholar] [CrossRef]
  51. Zhao, L.; Li, T.; Yu, H.; Zhang, X.; Zheng, Z. Effects of [S, S]-ethylenediaminedisuccinic acid and nitrilotriacetic acid on the efficiency of Pb phytostabilization by Athyrium wardii (Hook.) grown in Pb-contaminated soils. J. Environ. Manag. 2016, 182, 94–100. [Google Scholar] [CrossRef]
Agriculture 15 02153 g001
Figure 1. Effects of phosphorus and EDDS on TFs of Cu (a) and Cd (b) in castor plants. −EDDS means no EDDS added; +EDDS means with EDDS added. Columns with different letters represent significant differences in the TFs of Cu and Cd among different treatment groups at p < 0.05 levels (n = 3) according to the Duncan test.
Figure 1. Effects of phosphorus and EDDS on TFs of Cu (a) and Cd (b) in castor plants. −EDDS means no EDDS added; +EDDS means with EDDS added. Columns with different letters represent significant differences in the TFs of Cu and Cd among different treatment groups at p < 0.05 levels (n = 3) according to the Duncan test.
Agriculture 15 02153 g001
Agriculture 15 02153 g002
Figure 2. Effects of phosphorus and EDDS on dry weights of castor shoots (a) and roots (b). −EDDS means no EDDS added; +EDDS means with EDDS added. Columns with different letters represent significant differences in the dry weights of shoots and roots among different treatments at p < 0.05 levels (n = 3) according to the Duncan test.
Figure 2. Effects of phosphorus and EDDS on dry weights of castor shoots (a) and roots (b). −EDDS means no EDDS added; +EDDS means with EDDS added. Columns with different letters represent significant differences in the dry weights of shoots and roots among different treatments at p < 0.05 levels (n = 3) according to the Duncan test.
Agriculture 15 02153 g002
Agriculture 15 02153 g003
Figure 3. Effects of phosphorus and EDDS on castor photosynthetic pigments. (a) Chlorophyll a of leaves, (b) chlorophyll b of leaves, (c) carotenoid content of leaves. −EDDS means no EDDS added; +EDDS means with EDDS added. Columns with different letters represent significantly different chlorophyll a, chlorophyll b, and carotenoid contents in the leaves of under different treatments at p < 0.05 levels (n = 3) according to Duncan test.
Figure 3. Effects of phosphorus and EDDS on castor photosynthetic pigments. (a) Chlorophyll a of leaves, (b) chlorophyll b of leaves, (c) carotenoid content of leaves. −EDDS means no EDDS added; +EDDS means with EDDS added. Columns with different letters represent significantly different chlorophyll a, chlorophyll b, and carotenoid contents in the leaves of under different treatments at p < 0.05 levels (n = 3) according to Duncan test.
Agriculture 15 02153 g003
Agriculture 15 02153 g004
Figure 4. Effects of phosphorus and EDDS on castor leaves MDA (a) and roots MDA (b) levels. −EDDS means no EDDS added; +EDDS means with EDDS added. Columns with different letters represent significant differences in the content of MDA in leaves and roots among different treatments at p < 0.05 levels (n = 3) according to the Duncan test.
Figure 4. Effects of phosphorus and EDDS on castor leaves MDA (a) and roots MDA (b) levels. −EDDS means no EDDS added; +EDDS means with EDDS added. Columns with different letters represent significant differences in the content of MDA in leaves and roots among different treatments at p < 0.05 levels (n = 3) according to the Duncan test.
Agriculture 15 02153 g004
Agriculture 15 02153 g005aAgriculture 15 02153 g005b
Figure 5. Effects of phosphorus and EDDS on antioxidant activities of leaves POD (a), CAT (c) and SOD (e) and of roots POD (b), CAT (d) and SOD (f) of castor plants. −EDDS means no EDDS added; +EDDS means with EDDS added. Columns with different letters represent significantly different antioxidant enzyme activities in the leaves and roots under different treatments at p < 0.05 levels (n = 3) according to the Duncan test.
Figure 5. Effects of phosphorus and EDDS on antioxidant activities of leaves POD (a), CAT (c) and SOD (e) and of roots POD (b), CAT (d) and SOD (f) of castor plants. −EDDS means no EDDS added; +EDDS means with EDDS added. Columns with different letters represent significantly different antioxidant enzyme activities in the leaves and roots under different treatments at p < 0.05 levels (n = 3) according to the Duncan test.
Agriculture 15 02153 g005aAgriculture 15 02153 g005b
Agriculture 15 02153 g006aAgriculture 15 02153 g006b
Figure 6. Effects of phosphorus and EDDS on shoots N (a), roots N (c), shoots P (b), and roots P (d) of castor plants. −EDDS means no EDDS added; +EDDS means with EDDS added. Columns with different letters represent significantly different N and P concentrations in shoots and roots of castor plants under different treatments at p < 0.05 levels (n = 3) according to the Duncan test.
Figure 6. Effects of phosphorus and EDDS on shoots N (a), roots N (c), shoots P (b), and roots P (d) of castor plants. −EDDS means no EDDS added; +EDDS means with EDDS added. Columns with different letters represent significantly different N and P concentrations in shoots and roots of castor plants under different treatments at p < 0.05 levels (n = 3) according to the Duncan test.
Agriculture 15 02153 g006aAgriculture 15 02153 g006b
Agriculture 15 02153 g007
Figure 7. Effects of phosphorus and EDDS on content of available Cu (a) and Cd (b) in Cu and Cd co-contaminated soil. −EDDS means no EDDS added; +EDDS means with EDDS added. Columns with different letters represent significantly different available Cu and Cd concentrations in soil under different treatments at p < 0.05 levels (n = 3) according to the Duncan test.
Figure 7. Effects of phosphorus and EDDS on content of available Cu (a) and Cd (b) in Cu and Cd co-contaminated soil. −EDDS means no EDDS added; +EDDS means with EDDS added. Columns with different letters represent significantly different available Cu and Cd concentrations in soil under different treatments at p < 0.05 levels (n = 3) according to the Duncan test.
Agriculture 15 02153 g007
Table 1. The concentrations of Cu and Cd in castor plants.
Table 1. The concentrations of Cu and Cd in castor plants.
TreatmentsCu (mg kg−1)Cd (mg kg−1)
ShootRootShootRoot
P0-EDDS7.35 ± 0.01 c81.21 ± 9.20 c0.91 ± 0.10 d6.89 ± 0.39 a
P0+EDDS32.55 ± 1.63 b346.91 ± 85.26 a0.93 ± 0.03 cd5.82 ± 0.19 ab
P100-EDDS6.33 ± 0.14 c57.39 ± 2.86 c1.07 ± 0.02 bc3.33 ± 0.48 c
P100+EDDS105.44 ± 8.91 a206.73 ± 30.39 b1.34 ± 0.01 a5.25 ± 0.58 b
P300-EDDS6.58 ± 0.67 c59.10 ± 5.46 c1.10 ± 0.05 b1.61 ± 0.32 d
P300+EDDS34.05 ± 0.15 b101.10 ± 0.98 bc1.25 ± 0.00 a0.79 ± 0.00 d
Note: P0-EDDS = no P nor EDDS (control), P0+EDDS = 5.0 mmol kg−1 of EDDS after 30 days of cultivation, P100-EDDS = 100 mg kg−1 P5O2, P100+EDDS = 100 mg kg−1 P5O2 and 5.0 mmol kg−1 of EDDS after 30 days of cultivation [37], P300-EDDS = 300 mg kg−1 P5O2, P300+EDDS = 300 mg kg−1 P5O2 and 5.0 mmol kg−1 of EDDS after 30 days of cultivation. Data are the means of three replicates (mean ± SE). For each column, values marked with a different letter show a significant difference at p < 0.05 levels according to the Duncan test.
Table 2. Effects of P and EDDS application on soil chemical properties.
Table 2. Effects of P and EDDS application on soil chemical properties.
TreatmentsSoil pHSoil-Available P
mg kg−1		Soil NH4+-N
mg kg−1		Soil NO3−-N
mg kg−1		Soil DOC Concentrations
mg kg−1
P0-EDDS7.75 + 0.04 a9.09 + 0.28 d6.46 + 0.28 abc4.29 ± 0.48 b100.55 ± 3.91 c
P0+EDDS7.85 ± 0.02 a9.09 ± 0.45 d7.37 ± 0.22 a22.54 ± 0.60 a138.89 ± 9.92 b
P100-EDDS7.95 ± 0.02 a13.19 ± 0.50 cd5.54 ± 0.12 c2.56 ± 0.50 b99.28 ± 0.95 c
P100+EDDS7.88 ± 0.05 a18.47 ± 3.15 bc6.72 ± 0.16 ab21.51 ± 2.12 a162.96 ± 9.16 a
P300-EDDS7.80 ± 0.00 a23.00 ± 0.93 ab5.55 ± 0.36 c1.59 ± 0.27 b99.95 ± 3.41 c
P300+EDDS7.83 ± 0.03 a27.81 ± 0.54 a6.00 ± 0.31 bc24.11 ± 3.45 a146.80 ± 6.31 ab
Note: P0-EDDS = no P nor EDDS (control), P0+EDDS = 5.0 mmol kg−1 of EDDS after 30 days of cultivation, P100-EDDS = 100 mg kg−1 P5O2, P100+EDDS = 100 mg kg−1 P5O2 and 5.0 mmol kg−1 of EDDS after 30 days of cultivation, P300-EDDS = 300 mg kg−1 P5O2, P300+EDDS = 300 mg kg−1 P5O2 and 5.0 mmol kg−1 of EDDS after 30 days of cultivation. Data are the means of three replicates (mean ± SE). For each column, values marked with different letters are significant differences at p < 0.05 levels according to the Duncan test.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Liu, W.; Tang, R.; Peng, X.; Yang, X.; Wang, Y.; Hu, H. Synergistic Effects of Phosphorus and EDDS on Enhancing Phytoremediation Efficiency of Ricinus communis L. in Cu and Cd Co-Contaminated Soils. Agriculture 2025, 15, 2153. https://doi.org/10.3390/agriculture15202153

AMA Style

Liu W, Tang R, Peng X, Yang X, Wang Y, Hu H. Synergistic Effects of Phosphorus and EDDS on Enhancing Phytoremediation Efficiency of Ricinus communis L. in Cu and Cd Co-Contaminated Soils. Agriculture. 2025; 15(20):2153. https://doi.org/10.3390/agriculture15202153

Chicago/Turabian Style

Liu, Wenying, Rongli Tang, Xinlei Peng, Xueting Yang, Yi Wang, and Hongqing Hu. 2025. "Synergistic Effects of Phosphorus and EDDS on Enhancing Phytoremediation Efficiency of Ricinus communis L. in Cu and Cd Co-Contaminated Soils" Agriculture 15, no. 20: 2153. https://doi.org/10.3390/agriculture15202153

APA Style

Liu, W., Tang, R., Peng, X., Yang, X., Wang, Y., & Hu, H. (2025). Synergistic Effects of Phosphorus and EDDS on Enhancing Phytoremediation Efficiency of Ricinus communis L. in Cu and Cd Co-Contaminated Soils. Agriculture, 15(20), 2153. https://doi.org/10.3390/agriculture15202153

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop