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Chemical and Biological Technologies in Agriculture
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Differential effects of pH on cadmium accumulation in Artemisia argyi growing in low and moderately cadmium-contaminated paddy soils

Chemical and Biological Technologies in Agriculture volume 11, Article number: 158 (2024) Cite this article

Abstract

Background

Phytoremediation is affected by physical and chemical properties of the soil such as soil pH, moisture, and nutrient content. Soil pH is a key element influencing Cd bioavailability and can be easily adjusted in agricultural practices. The soil pH level may relate to the effectiveness of phytoremediation; however, this has not been extensively investigated. In the current study, we evaluated the effect of Cd contamination level (0.56 and 0.92 mg/kg) and soil pH (5, 6, and 7) on Cd accumulation and allocation in Artemisia argyi, a fast-growing perennial crop.

Results

Our results indicated that higher soil Cd concentrations reduce A. argyi biomass, and the loss of the root mass was particularly significant. Higher soil pH decreased Cd content in stems and roots of A. argyi cultivated in moderately Cd-polluted soil, and increased Cd content in stems and roots of the plant grown in low Cd-polluted soil. Higher soil pH decreased the percentage of Cd distributed in the soluble fraction and cell walls and increased the percentage of Cd in the organelles of leaf cells for moderate soil Cd levels. The bioconcentration and translocation factor exceeded 4.0 and 1.0, respectively, across all tested treatments, indicating that A. argyi is a promising candidate for phytoremediation. Notably, the effects of soil pH on Cd accumulation and subcellular distribution in A. argyi differed between low and moderately Cd-contaminated soils.

Conclusion

Adjustments to soil pH based on the degree of Cd contamination can enhance Cd extraction by A. argyi, thereby reducing the overall remediation cycle of cadmium-polluted paddy fields of South China.

Graphical Abstract

Introduction

Cadmium (Cd), as a nonessential and highly poisonous heavy metal, has detrimental effects on organisms [1]. Moreover, its entry into the food chain can result in bioconcentration, which threatens human health, thereby increasing public concern worldwide [2]. According to the Ministry of Environmental Protection of China [3], 7% of the investigated sites in China were polluted by Cd, particularly the paddy fields of South China. As a staple food crop in China, approximately 10% of samples of brown rice have levels of Cd over the acceptable limit of 0.2 mg/kg [4]. Consequently, remediation of Cd-polluted soils is a prerequisite for food safety and ecosystem health.

Phytoremediation is considered a sustainable and cost-effective method to mitigate heavy metal contamination [5]. Several plant species, such as Sedum alfredii, Amaranthus hypochondriacus, and Solanum nigrum, have been reported to possess an exceptional Cd-absorption capacity in contaminated soils [6,7,8]. However, most Cd-accumulating species have slow growth rates, long phytoextraction cycles, and low economic value after harvest, which limit the implementation of large-scale phytoremediation [9]. Consequently, identifying highly effective accumulators to enhance phytoremediation efficacy in Cd-polluted soils has become urgent [10].

The efficiency of phytoremediation is influenced by plant genotype, soil physicochemical characteristics, and rhizosphere microbial communities [5]. Among these, soil pH has attracted the most attention because it is a pivotal determinant of Cd bioavailability and is easily regulated by agricultural practices [11,12,13]. Generally, a decrease in soil pH increases Cd ion availability and enhances Cd accumulation in plants [14, 15], whereas an increase in soil pH reduces Cd availability and inhibits its accumulation in plants [13].

However, the effects of soil pH on plant Cd extraction and soil remediation efficiencies are complex. For instance, soil pH of < 5 inhibited corn growth and did not lead to an increase in Cd uptake [16]. A lower pH promoted Cd absorption by sunflowers in a low-pollution environment, but hindered the remediation effect in heavily polluted conditions [17]. Acidic soil conditions led to higher Cd accumulation in Polygonum hydropiper in moderately Cd-contaminated paddy soil, whereas near-neutral pH caused higher Cd accumulation in P. hydropiper in low Cd-contaminated soil [8]. Consequently, a synergistic effect of the degree of soil Cd contamination and pH on the efficiency of phytoremediation may exist; however, it has not been extensively investigated.

In the present study, we investigated the effects of soil pH on Cd accumulation and allocation in Artemisia argyi growing in low and moderately Cd-contaminated paddy soils. A. argyi, a perennial herb characterized by a high biomass and rapid growth rate, is widely used as a raw material in herbal medicine, healthcare, and textiles in China [18]. A recent study demonstrated that this species can effectively extract Cd from contaminated soil and translocate it from roots to shoots [19]. We hypothesized that: (1) an increase in soil Cd content would increase Cd accumulation but constrain A. argyi growth; and (2) a decrease in soil pH would enhance Cd absorption by A. argyi in both low and moderately Cd-contaminated soils. We conducted a pot experiment using three soil pH levels (5, 6, and 7) and two Cd-polluted paddy soils (0.56 and 0.92 mg/kg). Our findings will contribute to the overall understanding of the effect of pH on Cd absorption by accumulators and provide a valuable reference for phytoremediation strategies aimed at Cd-contaminated paddy soils.

Materials and methods

Research site

The experiment was conducted in an outdoor greenhouse at the Research Station for Agricultural and Environmental Monitoring, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha City, Hunan Province, China (28° 22′ N, 112° 58′ E). The study area has a subtropical monsoon climate with an average annual temperature of 17.2 °C and total annual precipitation of 1200–1500 mm. Soil samples were collected from two paddy-field patches with varying levels of Cd pollution. The total Cd contents of the two paddy soils were 0.56 ± 0.03 and 0.92 ± 0.06 mg/kg, which falls within light (0.3–0.6 mg/kg) and moderate (0.9–1.5 mg/kg) contamination ranges, respectively (Table 1) [8]. In the early stage of preparation, both soil types used in the experiment were air-dried, sieved (2.54 mm), mixed homogeneously, and stored in the greenhouse for future use.

Table 1 Basic physical and chemical properties of soil in experiments (mean ± SE)
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Experimental design

The rhizomes of A. argyi were collected from Qichun County, Hubei Province, China (30° 13′ N, 115° 25′ E). This region has a similar climate with our research site, with an average annual temperature of 16.8 °C and total annual precipitation of 1341.7 mm. Following collection, the plants were cultivated in a nursery bed starting in August 2021. On September 18, 2021, 90 plants with similar heights and fresh weights (15 ± 2 g) were selected and transplanted into 30 plastic buckets (height: 45 cm; diameter: 35 cm) with three plants in each bucket. Each bucket had five small holes at the bottom and a nylon mesh on the holes that allowed water to enter from the bottom while preventing soil loss. Fifteen buckets contained 8 kg of lightly contaminated soil and 15 contained 8 kg of moderately contaminated soil.

We used a randomized block design with six treatments (three soil pH levels × two Cd contamination levels) and five replications. Three buckets of lightly polluted soil and three of moderately polluted soil were placed in large water tanks (150 × 80 × 100 cm). The water level in the tanks was maintained at 35 cm (0 cm for the plants). Following a 6-week growth period, weighed quantities of citric acid monohydrate and calcium oxide (analytically pure) were added to the buckets homogeneously. The initial pH of both types of paddy soils was 6. Citric acid monohydrate and calcium oxide were added to the soil to adjust the pH values to approximately 5, 6, and 7.

Processing of plant and soil samples

On December 17, 2021, after the lower leaves of A. argyi had begun to partially wilt, plants were harvested. The top 6–8 leaves were collected and refrigerated at 4 °C for subcellular structural analysis. After harvesting, we initially washed plant surfaces with tap water to remove soil and subsequently, rinsed them with distilled water. The plants were partitioned into stems, leaves, and roots, and placed in an oven heat at 105 °C for 30 min to terminate enzyme activity and then dried at 80 °C for 48 h to reach a steady weight. Each part of the plant sample was ground and homogenized individually with a grinder and subsequently placed in a sealed bag for further analysis. Following harvesting, soil samples were air-dried and ground up for further experimental analysis through a 100-mesh screen.

Analysis of Cd content in plants and soils

We utilized the technique outlined by Wang et al. [20] to ascertain the subcellular distribution of Cd in A. argyi leaves. Plant cell walls, organelles, and cell fluids were isolated using 10 mL of pre-cooled extraction buffer (250 mM sucrose, 50 mM Tris–HCl [pH 7.5], and 1 mM dithiothreitol).

The nitric–perchloric acid digestion method was employed to ascertain the Cd content of the plant samples [19]. The aqua regia–perchloric acid digestion method was utilized to quantify the total Cd content of the soil, and the 0.01% CaCl2 extraction method was employed to calculate available Cd content [21]. The total and available Cd contents in the soil and Cd contents in various plant organs were quantified using an inductively coupled plasma emission spectrometer (ICP–OES 720; Varian, Palo Alto, CA, USA). Blank and certified reference materials, GBW07602 Chinese plant samples, and GBW070011 Chinese soil samples (Science and Exhibition Biotech Co., Ltd., Beijing, China) were used for quality control. The recoveries of plant and soil samples were 98.1–104.7% and 96.8–102.6%, respectively.

Calculation of plant bioconcentration and translocation capacity indexes

We assessed the capacity of A. argyi to transport and absorb Cd using translocation (TF) and bioconcentration (BCF) factors, respectively [22]. The formulas were as follows:

$${\text{TF}} = {\text{Cd}}\;{\text{content}}\;{\text{in}}\;{\text{plant}}\;{\text{shoots}}\;\left( {{\text{mg}}/{\text{kg}}} \right)/{\text{Cd}}\;{\text{content}}\;{\text{in}}\;{\text{plant}}\;{\text{roots}}\;\left( {{\text{mg}}/{\text{kg}}} \right).$$
$${\text{BCF}} = {\text{Cd}}\;{\text{content}}\;{\text{in}}\;{\text{each}}\;{\text{plant}}\;{\text{organ}}\;\left( {{\text{mg}}/{\text{kg}}} \right)/{\text{total}}\;{\text{Cd}}\;{\text{content}}\;{\text{in}}\;{\text{the}}\;{\text{soil}}\;\left( {{\text{mg}}/{\text{kg}}} \right).$$

Statistical analysis

A general linear model (GLM) was employed to assess the impacts of soil pH and Cd pollution on plant biomass, Cd accumulation and distribution, and Cd translocation. Tukey’s test was used for multiple comparisons of averages at a significance level of 0.05 (p < 0.05). All statistical analyses were performed using R (version 4.04; R Core Team 2023).

Results

Plant biomass accumulation

The interaction between soil pH and Cd levels had a significant impact on A. argyi shoot mass. However, no significant effect of these parameters on shoot biomass was found when each of them was considered separately (Table 2; Fig. 1A). Soil Cd levels had a significant impact on root mass and total biomass of A. argyi, and significant interactions were observed between soil pH and Cd levels (Table 2; Fig. 1B, C). In low-pollution soils, treatment with a pH of 6 yielded the highest biomass for A. argyi, with root, shoot, and total biomass being 4.84 g, 7.48 g, and 12.32 g, respectively. Higher soil Cd levels decreased root mass and total biomass of A. argyi.

Table 2 Influence of each term (F-value) in a general linear model (GLM) analyzing the influence of soil pH and cadmium (Cd) level interaction on biomass accumulation of Artemisia argyi
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Fig. 1
figure 1

Shoot mass (A), root mass (B), and total biomass (C) of Artemisia argyi growing under three soil pH conditions at two cadmium (Cd) contamination levels. Different lowercase letters (a, b, c) indicate significant differences among the three pH treatments. The * and ns symbols indicate differences between the two soil Cd levels (**p < 0.01, ***p < 0.001, nsp > 0.05)

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Cd content in plant organs

The amount of Cd in the soil had a significant effect on the Cd content of A. argyi stems and roots, and significant interactions between soil pH and Cd levels were observed (Table 3; Fig. 2A, C). The content of Cd in the stems and roots of A. argyi increased with higher amounts of Cd in the soil. In moderate-pollution soils, treatment with a pH of 5 yielded the highest Cd content for A. argyi, with content in stems, leaves, and roots being 3.62 mg/kg, 8.41 mg/kg, and 5.45 mg/kg, respectively. Higher pH values enhanced the amount of Cd in the stems and roots of A. argyi at low soil Cd levels. In contrast, higher pH values and moderate soil Cd levels decreased the content of Cd in the stems and roots of A. argyi.

Table 3 Effect of each term (F-value) in a general linear model (GLM) examining the influence of soil pH and cadmium (Cd) content interaction on Cd accumulation in Artemisia argyi
Full size table
Fig. 2
figure 2

Cadmium (Cd) content in stem (A), leaf (B), and root (C) of Artemisia argyi growing under three soil pH conditions at two Cd contamination levels. Different lowercase letters (a, b, c) indicate significant differences among different pH treatments. The * and ns symbols indicate differences between the two soil Cd levels (**p < 0.01, ***p < 0.001, nsp > 0.05)

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The interaction between soil pH and Cd level had a significant impact on the content of Cd in A. argyi leaves (Table 3, Fig. 2B). Higher pH values increased the content of Cd in leaves at low soil Cd levels, whereas at moderate soil Cd levels, a higher pH value reduced the amount of Cd in the leaves.

Cd distribution in subcellular structures

Higher soil Cd levels reduced the percentage of Cd immobilized in the cell walls of leaf cells and increased the percentage of Cd distributed in the leaf cell organelles (Fig. 3A–C). At moderate soil Cd levels, higher soil pH reduced the percentage of Cd found in the soluble fraction and cell wall of leaf cells but increased the percentage of Cd distributed in the leaf cell organelles.

Fig. 3
figure 3

Subcellular distribution of Cd in the leaves of Artemisia argyi under three soil pH conditions at two Cd contamination levels. Different lowercase letters (a, b, c) indicate significant differences among different pH treatments

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Bioconcentration and translocation factors

Under all treatments, BCF for each organ of the A. argyi was > 4.0. Soil Cd level had a significant impact on the BCF of roots, stems, and leaves, with significant interactions between soil pH and Cd levels (Table 3). In low-pollution soils, the highest BCF value for A. argyi, with stems, leaves, and roots being 5.43, 11.48, and 9.18, respectively. Increased soil Cd levels decreased the BCF of stems, leaves, and roots. Higher soil pH increased the BCF of stems and roots at low soil Cd levels (Fig. 4A, C). Higher soil pH decreased the BCF of stems and leaves at medium soil Cd levels (Fig. 4A, B).

Fig. 4
figure 4

Bioconcentration factors for the stem (A), leaf (B), and root (C), along with the translocation factor of Artemisia argyi (D) under three soil pH conditions at two Cd contamination levels. Different lowercase letters indicate significant differences among the three pH treatments. The * and ns symbols indicate differences between the two soil Cd levels (**p < 0.01, ***p < 0.001, nsp > 0.05)

Full size image

In all treatments, the TF of A. argyi exceeded 1.0. Soil Cd levels had a significant impact on the TF of A. argyi, with significant interactions between soil pH and Cd levels (Table 3). Higher soil Cd levels decreased the TF of A. argyi.

Soil-available Cd content after plant harvest

Soil pH and Cd levels were observed to have significant effects on soil-available Cd content, with significant interactions (Table 3). Higher soil-available Cd content was observed in soils with moderate Cd levels (Fig. 5). Under a pH of 5, the available Cd content in low-pollution and moderate-pollution soils reached a maximum of 0.17 mg/kg and 0.22 mg/kg, respectively. Available soil Cd content decreased with increasing soil pH (Fig. 5).

Fig. 5
figure 5

Available Cd content under three soil pH conditions at two Cd contamination levels. Different lowercase letters indicate significant differences among the three pH treatments. The * and ns symbols indicate differences between the two soil Cd levels (**p < 0.01, ***p < 0.001, nsp > 0.05)

Full size image

Discussion

Higher soil Cd level decreases biomass of A. argyi

Although several studies have found a stimulatory effect of moderate Cd levels on the growth of some plant species [23, 24], our results indicated that moderate Cd contamination led to a decrease in the root and total biomass of A. argyi. This could be explained because high Cd concentrations create an imbalance between the production and elimination of reactive oxygen species within plant cells, leading to membrane system damage, further exacerbating plant physiological damage, and inhibiting growth [6, 25]. Growth inhibition by high Cd levels has also been reported in other Cd accumulators, such as Amaranthus spinosus and Acacia nilotica [26, 27]. Our results suggest that A. argyi is not a Cd-tolerant species and may not be suitable for the remediation of heavily Cd-contaminated sites. Our first hypothesis, that an increase in soil Cd content would increase Cd accumulation but constrain A. argyi growth, was generally supported.

In addition, we found adverse effects of acidic conditions on the growth of A. argyi in low-Cd-polluted soils, which primarily affected root growth. This might be caused by a decrease in soil pH, leading to an alkaline cation imbalance and resulting in the loss of soil nutrients and subsequent root development of A. argyi [28].

Soil pH has a differential effect on A. argyi Cd accumulation in low and moderately Cd-polluted soils

Our findings revealed that A. argyi exhibited higher Cd absorption in each organ under acidic soil conditions (pH 5) when grown in moderately polluted soil. Increased Cd absorption and extraction rates with decreasing soil pH have also been observed in Helianthus annuus, Bidens pilosa, and Lolium perenne [17, 29, 30]. The underlying mechanism may be that reduced soil pH modifies the chemical form of heavy metals, accelerating the conversion of residual Cd into bioavailable Cd in the soil, thereby enhancing Cd absorption and accumulation by plants [31].

However, in low Cd-polluted soils, higher soil pH increased Cd accumulation in A. argyi. Plant growth may be primarily influenced by soil alkalinity in low Cd-polluted soils because heavy metal stress does not exceed the detoxification threshold of plants [6]. Excessive acidic cations limit root development and subsequently reduce the ability of root networks to capture heavy metals [12, 32]. Therefore, a synergistic effect between soil pH and Cd levels on Cd accumulation in A. argyi exists. Our second hypothesis, that a decrease in soil pH would enhance Cd absorption by A. argyi in both low and moderately Cd-contaminated soils, was not supported.

Higher soil Cd level increases the percentage of Cd in leaf cell organelles

In low Cd-contaminated soils, Cd was primarily concentrated in the cell walls in A. argyi leaves. The cell wall serves as a crucial barrier to heavy metal penetration. Upon the entry of heavy metals into the cell, chelating compounds are initially released at the cell wall, effectively intercepting the metals before they can penetrate other cells [33, 34]. However, in moderately Cd-polluted soils, higher soil pH increased the amount of Cd in the leaf cell organelles and decreased the amount distributed in the soluble fraction and cell walls of leaf cells. This elevation in Cd cation content leads to Cd2+ competing with other cations for ion channels and carrier proteins in plants. This competition and the Cd amount above that which can be immobilized by the cell walls allow the metal to enter the cytosol and organelles and be bound [8, 35]. Consequently, the percentage of Cd in the cell wall decreases, whereas its distribution in the organelles increases. Several studies have consistently shown that subcellular distribution of Cd within plants is a reliable indicator of Cd tolerance and detoxification mechanisms [36]. The interaction between soil pH and Cd content had a profound impact on subcellular Cd distribution in A. argyi, highlighting the complexity of Cd distribution within plant cells.

Capacity of Artemisia argyi for Cd bioaccumulation and translocation

The bioaccumulation factor provides a direct measure of a plant’s ability to absorb heavy metals from the soil through its roots [37]. Our results indicate that under low-pollution conditions, A. argyi achieves a maximum bioaccumulation factor of 11.48 and 9.18 in stems and leaves, respectively. Compared to other commonly used remediation plants, such as Phytolacca americana L., Acacia nilotica L., and Phragmites australis, A. argyi demonstrates a distinct advantage [26, 37, 38]. However, in moderately contaminated soils, the bioaccumulation factor of A. argyi decreases with increasing pH, likely because of the reduced availability of Cd at higher pH levels (Fig. 5) [8].

The translocation coefficient reflects the plant’s capacity to transfer absorbed heavy metals from roots to aboveground parts. Generally, a translocation coefficient greater than 1 indicates a plant with strong translocation capability [39]. Numerous studies have shown that varying translocation capacities among different plants result in varying outcomes during remediation processes [40,41,42]. We found that A. argyi consistently exhibited translocation coefficients greater than 1 across all treatments, signifying its strong translocation ability and effective performance in various environments. These findings further confirm A. argyi’s effective Cd absorption and translocation, suggesting that adjusting soil pH according to contamination levels can enhance its remediation potential.

Conclusions

Our results indicate a synergistic effect of soil pH and Cd levels on the growth, Cd accumulation, and subcellular distribution of Cd in A. argyi. Lower soil pH increased Cd accumulation in moderately polluted soil but decreased Cd accumulation of A. argyi under low polluted soil. In addition, under moderate pollution, a higher pH reduced the proportion of Cd in the cell wall and soluble fraction and increased the proportion of Cd in organelles of the leaf cells. Given its high capacity for Cd accumulation and translocation, as well as its potential economic value, A. argyi has emerged as a promising candidate for phytoextraction of low to moderately Cd-polluted soil. Strategic adjustments to soil pH based on pollution levels can enhance the Cd extraction capacity of A. argyi, thereby reducing the overall remediation cycle of cadmium-polluted paddy fields of South China.

Availability of data and materials

No datasets were generated or analysed during the current study.

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Acknowledgements

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Funding

This work was supported by the National Natural Science Foundation of China (32471657, 42177025).

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Authors and Affiliations

  1. School of Resources and Environmental Engineering, Anhui University, Hefei, 230601, China

    Ze Zhang, Jia-shun Zhong, Xin-zhi Guo & Xin-sheng Chen

  2. Anhui Shengjin Lake Wetland Ecology National Long-term Scientific Research Base, Dongzhi, 247230, China

    Ze Zhang, Jia-shun Zhong, Xin-zhi Guo & Xin-sheng Chen

  3. Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, 410125, China

    Chao Xu, Dao-you Huang & Xin-sheng Chen

  4. Baiyangdian Basin Ecological Environment Monitoring Center, Baoding, 071051, China

    Jing Liu

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  1. Ze Zhang
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Contributions

Ze Zhang: methodology, data collection, writing. Jia-shun Zhong: writing—review and editing. Xin-zhi Guo: methodology, data collection. Chao Xu: methodology, data collection. Dao-you Huang: conceptualization, data collection. Jing Liu: writing—review and editing. Xin-sheng Chen: conceptualization, methodology, writing—review and editing. Each author contributed to the work and approved the updated version.

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Correspondence to Xin-sheng Chen.

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Zhang, Z., Zhong, Js., Guo, Xz. et al. Differential effects of pH on cadmium accumulation in Artemisia argyi growing in low and moderately cadmium-contaminated paddy soils. Chem. Biol. Technol. Agric. 11, 158 (2024). https://doi.org/10.1186/s40538-024-00690-x

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