Potential synergistic effect of polystyrene nanoplastics on cadmium toxicity to Sedum alfredii Hance

Yuenan Li; Hongyan Cheng; Yixiu Wang; Yonghui Lv; Ruiyan Ning; Haibo Zhang; Qing Wang; Na Liu

doi:10.1371/journal.pone.0344578

Abstract

Micro/nanoplastics (MPs/NPs) and cadmium (Cd) are among the most serious pollutants in soils, and the coexistence of MPs/NPs and Cd is therefore inevitable. Several studies have investigated the effects of MPs/NPs or Cd stress alone on plant growth. However, little is known regarding the combined effects of NPs and Cd stress on plants and Cd accumulation, particularly in hyperaccumulators. The study selected Sedum alfredii Hance as a test material, and investigated the individual and combined effects of polystyrene nanoplastics (PS-NPs) (100 and 1000 mg·kg^-1) and Cd (0.6 and 4 mg·kg^-1) on the physiological indices, trace element contents, Cd content, Cd chelation, and Cd speciation. The growth of S. alfredii was significantly inhibited under PS-NPs or Cd alone, and the inhibitory effect of Cd stress was more significant than that of PS-NPs stress. Combined treatments increased the growth-inhibition effect. The individual PS-NPs treatments had no significant effects on antioxidant enzyme activity or malondialdehyde (MDA) and trace element contents, but combined treatments significantly increased antioxidant enzyme activity and MDA content, thereby reducing the trace element contents compared to the individual PS-NPs or Cd treatments. Combined treatments increased the contents of the exchangeable Cd, carbonate-bound Cd, and reduced organic-bound Cd, thereby significantly increasing the Cd content in the aboveground parts and roots of S. alfredii; the Cd content in the aboveground parts and roots of S. alfredii under combined Cd (4 mg·kg^-1) and PS-NPs (1000 mg·kg^-1) treatment was 1.2-fold and 1.36-fold higher, respectively, than under Cd stress alone (4 mg·kg^-1). Furthermore, Cd chelation under combined treatments increased significantly compared to the PS-NPs or Cd treatments alone. The nonprotein thiol (NPT) and phytochelatin (PC) contents under combined PS-NPs (1000 mg·kg^-1) and Cd (4 mg·kg^-1) increased by 12.9% and 13.0%, respectively, compared to Cd stress alone (4 mg·kg^-1). These findings elucidate the impact of NPs on Cd accumulation in hyperaccumulator plants, which holds significant implications for understanding the environmental risks associated with the combination of NPs and Cd.

Citation: Li Y, Cheng H, Wang Y, Lv Y, Ning R, Zhang H, et al. (2026) Potential synergistic effect of polystyrene nanoplastics on cadmium toxicity to Sedum alfredii Hance. PLoS One 21(3): e0344578. https://doi.org/10.1371/journal.pone.0344578

Editor: Babar Iqbal, Jiangsu University, CHINA

Received: June 20, 2025; Accepted: February 23, 2026; Published: March 10, 2026

Copyright: © 2026 Li et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the manuscript and its Supporting Information files.

Funding: The Distinguished and Excellent Young Scholar Cultivation Project of Shanxi Agricultural University [grant number 2022YQPYGC07]; the Shanxi Scholarship Council of China [grant number 2021-069]; and the Shanxi Province Excellent Doctor Award Fund [grant number SXBYKY2021038]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Approximately 1.2 × 10¹³ kg of plastic waste will accumulate in the natural environment by the mid-21st century [1,2]. Micro/nanoplastics (MPs/NPs) continuously accumulate in sediments, soils, and other media due to their small particle diameters and weak photodegradation ability [3]. At the second United Nations Environment Assembly in 2016, MPs/NPs pollution was highlighted as the second most important major scientific challenge in environmental and ecological research, in addition to ozone depletion and global climate change, these issues have become major global environmental challenges. The contents of MPs/NPs are generally higher in terrestrial environments than in aquatic environments [4], and research on these particles has shifted from aquatic environments to soil environments [5,6]. Currently, MPs/NPs have been detected in agricultural, industrial [7,8], and cultivated soils across various provinces in China [9,10]. Their abundances varied widely, ranging from 7100 to 42900 p kg⁻¹, with particle sizes ranging from 0.05–1 mm [9,11,12]. As one of the top five general-purpose plastics used around the world, polystyrene (PS) contributes a major share of environmental MPs/NPs. PS primarily enters the soil through organic fertilizer application, plastic waste in landfills, and sewage irrigation [13,14]. PS is non-biodegradable and can remain in the environment for a long time if not subjected to heating or ultraviolet treatment [15], resulting in high amounts of PS-MPs/NPs in the environment. MPs/NPs not only accumulate in soil environments, but also in plants, thereby affecting plant growth [16,17]. According to He et al. [18], the fresh weights of cabbage have been shown to decreased significantly when exposed to PE-MPs. This phenomenon can be attributed to the physical obstruction of root systems by MPs, which adsorb to root surfaces and likely clog pores, thereby impeding water and nutrient uptake. Furthermore, MPs can be internalized into root tissues via endocytosis or apoplastic transport, ultimately inhibiting plant growth and development [19]. However, Lian et al. [20] found that wheat biomass increased significantly following exposure to PS-MPs. The observed biomass increase under MPs exposure may result from an adaptive stress response in certain crop species. To counterbalance the stress, plants first initiate morphological adaptations, such as expanding the lateral root system and increasing the root-to-shoot ratio. Subsequently, these modifications help maintain root growth and enhance the uptake efficiency of water and nutrients, ultimately leading to a compensatory increase in overall biomass [21]. At present, most existing studies on the effects of MPs/NPs on plants concentrate on crops, whereas the influence of these particles on hyperaccumulator plants requires further investigation.

Most environmental research has focused on heavy metal pollution, and cadmium (Cd) is a key pollutant that is a subject of global concern due to its wide pollution gradient and high toxicity. In China, the area of Cd-polluted cultivated land is approximately 2 × 10⁵ km², and the geometric mean of Cd content in the agricultural soil is 0.473 mg·kg^-1; moreover, both the degree and area of Cd pollution are increasing annually [22,23]. Cd stress alone can alter antioxidant enzyme activity, in turn affecting plant growth [24]. As the most common Cd-accumulating plant, Sedum alfredii Hance (Crassulaceae) is effective in the remediation of Cd-contaminated soils [25]. MPs/NPs in ecosystems do not usually exist in isolation, as they can easily adsorb heavy metals and antibiotics in the environment onto their surfaces [26]. At present, various MPs–metal ion complexes have been detected in the environment, indicating that these particles can function as carriers of heavy metals [27]. Zhou et al. [28] reported that MPs can adsorb Cd, with the adsorption capacity depending on MPs type. Furthermore, they demonstrated that adding MPs altered the speciation of Cd in soil, specifically decreasing the exchangeable, carbonate-bound and Fe-Mn oxide-bound fractions, while increasing the organic-bound fraction [29]. Moreover, a combination of MPs/NPs and Cd were further found to inhibit plant growth compared to MPs/NPs stress alone and resulted in enhanced toxic effects [30,31]. Similarly, combined MPs/NPs and heavy metal stress reduced superoxide dismutase (SOD) and catalase (CAT) activities in the roots of rice seedlings [32]. Xie et al. [33] found that combined PLA-MPs and Cd significantly decreased the Mg, Zn, and Cd contents in pakchoi compared to the Cd treatment alone. The presence of MPs/NPs not only affects soil environments, but can also be an important factor affecting the transformation of heavy metal speciation in soil.

Pollution caused by MPs/NPs and Cd has received broad attention in recent years. The pollution caused by MPs/NPs and Cd has garnered considerable attention in recent years. While existing studies have documented the individual effects of MPs/NPs or heavy metals on crop growth and physiology, the specific aspect of combined PS-NPs and Cd in S. alfredii growth and soil properties remains unexplored. S. alfredii is of great scientific significance as a model plant for elucidating hypertolerance and hyperaccumulation traits, as well as for decontaminating heavy metals. It also serves as a core component of phytoremediation [34]. Therefore, this study selected S. alfredii as a test material to investigate the effects of PS-NPs and Cd, both alone and in combination, on physiological indices, trace element contents, Cd content, Cd chelation, and Cd speciation content in the soil. The findings of this study provide insights into the ecological effects of NPs and Cd on hyperaccumulator plants and can offer data to deepen our understanding of Cd accumulation in these plants.

Materials and methods

Experimental materials

S. alfredii is a typical Cd-hyperaccumulating plant obtained from Taizhou in Zhejiang Province, China. Healthy plants with uniform sizes were selected for pot experiments. The PS-NPs used for the pot experiments were purchased from the Electric Corporation of Japan. The specific morphology of PS-NPs was characterized using scanning electron microscopy (SEM) (JSM-7800, HITACHI-Regulus 8100, Hitachi, Tokyo, Japan) and the particle size was 100–500 nm (Fig 1).

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Fig 1. Scanning electron micrographs of polystyrene nanoplastics.

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Experimental design

The soil used for the experiment was brown calcareous soil. The physicochemical properties of the soil are presented in Table 1. A defined mass of PS-NPs powder was first thoroughly mixed with a small portion of dry, finely ground soil to achieve initial homogeneity. This premix was then gradually blended into the remaining bulk soil. Finally, a Cd solution was added during continuous stirring to achieve uniform moisture and distribution. The wet soil was sealed, incubated for 24 h for equilibrium, and remixed before use. This stepwise mixing protocol was designed to prevent NPs aggregation and ensure their uniform dispersion within the soil matrix. A basin (22.8 cm *17.0 cm *17.5 cm) was filled with 3.5 kg of air-dried sifted soil, and the soil was evenly mixed with PS-NPs and Cd solution (analytical-grade Cd (NO₃)₂·4H₂O dissolved in distilled water) at different concentration gradients. After the PS-NPs and Cd were evenly dispersed, S. alfredii plants at the same stage were transferred to various basins for cultivation. Plants were irrigated during the growth period, and the soil moisture content was maintained at 60% of the field water-holding capacity. Plants were cultivated under the controlled conditions: 25°C/20°C day/night temperature, a 60% relative humidity, 12/12 h (light/dark) photoperiod, and a 15,000 lux light intensity. The experiment included nine treatments (Table 2), with all treatments replicated three times. The concentrations of PS-NPs and Cd used in this study were set based on a previous study [2]. After six months, the S. alfredii were harvested.

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Table 1. Original physicochemical properties of soil.

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Table 2. Experimental treatment design.

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Measurement of growth and physiological parameters

The harvested plant samples were washed with tap water to remove the soil attached to their root surfaces. The samples were then labeled and stored in sealed Ziplock bags. The heights and root lengths of S. alfredii were measured using a ruler (accuracy of 0.1 cm). The fresh weight of roots and the aboveground parts of S. alfredii were weighed and recorded. The fresh leaves were stored in ziplock bags at −80°C until determination of antioxidant enzyme activity and malondialdehyde (MDA) content, and Cd chelation indices of each plant. Thereafter, the plant materials were initially dried in an oven maintained at 105°C for 30 min and then dried to a constant weight at 70°C, and their dry weights were recorded.

The SOD activity was determined using the nitrogen blue tetrazole photoreduction method; Peroxidase (POD) activity was determined based on a guaiacol assay; CAT activity was obtained using ultraviolet-visible absorption spectroscopy; MDA content was calculated using the thiobarbituric acid method [35]; Glutathione (GSH) content was determined using GSH assay kits (Keming Biotechnology Co., Ltd., Suzhou, China); Nonprotein thiol (NPT) content was determined using the 5,5-dithio-bis-(2-nitrobenzoic acid) color development method [36,37]; PCs content is calculated as the difference between NPT and GSH. The enzyme assays were conducted with three independent biological replicates.

Determination of trace element contents and Cd content in S. alfredii

Samples of the aboveground parts and roots of S. alfredii were dried and ground to powder. The powdered samples were digested using a mixture of nitric and perchloric acids (4:1 v:v). The solution was heated at 250°C until it became completely clear. Afterward, the solution was cooled to room temperature and transferred into a 25-mL volumetric flask. The heating test tube was washed three times with ultrapure water, and the cleaning solution was transferred into a volumetric flask, which was filled with ultrapure water to the scale mark and then shaken thoroughly. The sample solution was then passed through a 0.45-μm filter membrane, the Cd content was determined using an atomic absorption spectrometer (pinAAcle 900Z; PerkinElmer Inc., Shelton, CT, USA), the Zn, Cu and Mn contents were determined using an inductively coupled plasma optical emission spectrometer (ICP-OES) (Optima 5300DV, PerkinElmer, USA).

Determination of Cd speciation in soil

An accurately weighed 2 g soil sample was loaded into a 100 mL centrifuge tube for stepwise extraction. The speciation of Cd in soil was determined using Tessier’s sequential extraction procedure, which separates heavy metals into five geochemical forms through a series of chemical leaching steps. The Cd content of each extracted fraction was then quantified using atomic absorption spectrometry (pinAAcle 900Z; PerkinElmer Inc., Shelton, CT, USA).

Statistical analysis

Statistical analysis was performed using IBM SPSS Statistics 23.0 (IBM Corp., Armonk, NY, USA). One-way analysis of variance (ANOVA) was performed to determine significance differences between treatment means, followed by Tukey’s post-hoc test. Data are expressed as the mean±standard deviation. Statistical significance was set at P < 0.05. Graphs were generated using OriginPro 2018 (OriginLab Corp., Northampton, MA, USA).

Results

Individual and combined effects of PS-NPs and Cd on S. alfredii growth

The inhibitory effect of the individual PS-NPs stress on S. alfredii biomass was correlated positively with the concentration of PS-NPs. Compared to the control (CK), the fresh weights at a low concentration of PS-NPs (N1) and a high concentration of PS-NPs (N2) decreased significantly by 9.3% and 20.0%, respectively (P < 0.05). The individual PS-NPs stress had no significant effect on the dry weight of S. alfredii. The biomass under the individual Cd stress was lower significantly than CK, and the inhibitory effect was correlated positively with the Cd concentration (P < 0.05). The inhibitory effect of the individual Cd was more significant than that of the individual PS-NPs (Fig 2a).

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Fig 2. Individual and combined effects of PS-NPs and Cd stress on S. alfredii growth.

a): Fresh and Dry weights; b): Plant height and Root length.C1 and C2 respectively represented the concentration of Cd (0.6 and 4 mg·kg^-1), and N1 and N2 respectively represented the concentration of PS-NPs (100 and 1000 mg·kg^-1). Different letters indicate significant differences (P < 0.05).

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Combined PS-NPs and Cd decreased the biomass of S. alfredii compared to the individual PS-NPs or Cd stress. The dry weights of S. alfredii at low concentrations of Cd and PS-NPs (C1N1) and at low concentration of Cd and high concentrations of PS-NPs (C1N2) were significantly reduced by 4.0% and 7.2%, respectively, compared to the dry weight at a low concentration of Cd (C1) without PS-NPs (P < 0.05). The fresh weights of S. alfredii at a high concentration of Cd and a low concentration of PS-NPs (C2N1) and a high concentration of Cd and a high concentration of PS-NPs (C2N2) were significantly reduced by 13.1% and 24.6%, respectively, compared to the fresh weight at a high concentration of Cd (C2) without PS-NPs (P < 0.05) (Fig 2a).

The root length of S. alfredii under the individual Cd stress was lower significantly than CK, and the inhibitory effect increased with an increase in Cd concentration (P < 0.05). However, no significant differences were observed in the root length between the CK and singe PS-NPs stress. Combined PS-NPs and Cd stress significantly reduced the root length of S. alfredii compared to the individual PS-NPs (P < 0.05). The root lengths of S. alfredii in the C1N2 and C2N2 stresses decreased significantly by 15.2% and 27.1%, respectively, compared to the root length in the N2 stress. (Fig 2b).

The height of S. alfredii under the individual Cd stress was lower significantly than CK, and the inhibitory effect increased with an increase in Cd concentration (P < 0.05). Compared to CK, the plant height of S. alfredii decreased by 9.7% and 12.8% under N1 and N2 stress, respectively. Combined PS-NPs and Cd stress had a stronger inhibitory effect on plant height compared to the individual PS-NPs stress. The height of S. alfredii in the C1N1 and C2N1 stresses was significantly reduced by 29.1% and 51.3%, respectively, compared to the N1 (P < 0.05) (Fig 2b).

Individual and combined effects of PS-NPs and Cd on antioxidant enzyme activities and MDA content in S. alfredii

The SOD activity in S. alfredii in the individual Cd stress was significantly higher than that the CK, and the effect of Cd on SOD activity increased with an increase in Cd concentration (P < 0.05). However, the individual PS-NPs stress had no significant effect on SOD activity in S. alfredii. Combined PS-NPs and Cd increased significantly the SOD activity in S. alfredii compared to individual PS-NPs or Cd stress (P < 0.05). The SOD activity in S. alfredii in the C2N1 and C2N2 stresses increased significantly by 13.8% and 27.1%, respectively, compared to the C2 stress (Fig 3a).

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Fig 3. Individual and combined effects of PS-NPs and Cd on antioxidant enzyme activities and MDA content in S. alfredii.

(a): SOD: superoxide dismutase; (b): POD: peroxidase; (c): CAT: catalase; (d): MDA: malondialdehyde. PS-NPs: polystyrene nanoplastic; Cd: cadmium.C1 and C2 respectively represented the concentration of Cd (0.6 and 4 mg·kg^-1), and N1 and N2 respectively represented the concentration of PS-NPs (100 and 1000 mg·kg^-1). Different letters indicate significant differences in the results; the same letters indicate non-significant differences in the results (P < 0.05).

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Furthermore, the effect of Cd on POD activity increased with an increase in the Cd concentration, which was consistent with the trend exhibited by SOD activity. A low PS-NPs concentration (N1) had no significant effect on POD activity in S. alfredii, although a high PS-NPs concentration (N2) increased POD activity by 34.1% compared to CK. Combined PS-NPs and Cd stress increased the POD activity compared to the individual PS-NPs and Cd stress. The POD activity in S. alfredii under the C2N1 and C2N2 stresses increased significantly by 8.3% and 19.1%, respectively, compared to that under the C2 (P < 0.05) (Fig 3b).

The individual PS-NPs stress had no significant effect on CAT activity, which was consistent with the trend exhibited by SOD activity. The effect of Cd on CAT activity increased with an increase in the concentration of Cd. Combined PS-NPs and Cd increased CAT activity compared to the individual PS-NPs and Cd stress. The CAT activity in S. alfredii under the C2N1 and C2N2 stresses increased significantly by 7.5% and 17.5%, respectively, compared to the CAT activity in C2 (P < 0.05) (Fig 3c).

The MDA contents under the individual Cd stress were significantly higher than CK, and the effect of Cd on the MDA content was enhanced with an increase in the Cd concentration (P < 0.05). Combined PS-NPs and Cd considerably increased the MDA content of S. alfredii compared to the individual PS-NPs stress (P < 0.05). The MDA content in the C1N1 stress significantly increased by 36.8% compared to that under N1 (P < 0.05). The MDA content of S. alfredii in the C2N1 stress was 1.1-fold higher than that in the N1 stress. The combined PS-NPs and Cd stress had no significant effect on MDA content compared to the individual Cd stress in S. alfredii (Fig 3d).

Individual and combined effects of PS-NPs and Cd on Cd chelation in S. alfredii leaves

The GSH content of S. alfredii under the C1 and C2 increased significantly by 32.9% and 87.1%, respectively, compared to that of the control group (P < 0.05). However, no significant differences in the GSH content were observed between the CK and the individual PS-NPs stress. Combined PS-NPs and Cd stress increased the GSH content in S. alfredii compared to the individual Cd stress. Specifically, the GSH content significantly increased by 10.1% and 17.8% under the C1N1 and C1N2 stresses, respectively, compared to that of C1 (P < 0.05) (Fig 4).

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Fig 4. Individual and combined effects of PS-NPs and Cd on Cd chelation (GSH, NPT and PCs) in S. alfredii leaves.

GSH: glutathione; NPT: nonprotein thiol; PCs: phytochelatins. PS-NPs: polystyrene nanoplastic; Cd: cadmium.C1 and C2 respectively represented the concentration of Cd (0.6 and 4 mg·kg^-1), and N1 and N2 respectively represented the concentration of PS-NPs (100 and 1000 mg·kg^-1). Different letters indicate significant differences in the results; the same letters indicate non-significant differences in the results (P < 0.05).

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The individual Cd stress significantly increased the NPT content of S. alfredii compared to that of CK, and the effect of Cd increased with an increase in the Cd concentration (P < 0.05). A low PS-NPs concentration (N1) had no significant effect on the NPT content. In contrast, a high PS-NPs concentration (N2) significantly increased the NPT content of S. alfredii, by 33.6%, compared to that of CK (P < 0.05). Combined PS-NPs and Cd significantly increased the NPT content compared to the individual Cd stress. In addition, the NPT content under the C2N1 and C2N2 stresses significantly increased by 3.8% and 12.9%, respectively, compared to that in the C2 (P < 0.05) (Fig 4).

The individual Cd stress significantly increased the PCs content of S. alfredii compared to that of CK, while the effect of PS-NPs on the PCs content was not significant. Combined PS-NPs and Cd increased significantly the PCs content compared to the individual Cd. Specifically, the PCs content of S. alfredii in the C2N1 and C2N2 significantly increased by 3.8% and 13%, respectively, compared to that in C2 (P < 0.05) (Fig 4).

Individual and combined effects of PS-NPs and Cd on Cd and trace element contents in S. alfredii

The Cd contents in the aboveground parts of S. alfredii in the C1 and C2 were increased by 2.6-fold and 3.8-fold compared to those of CK, respectively (P < 0.05). Cd accumulation in the aboveground parts of S. alfredii under combined PS-NPs and Cd stress was considerably enhanced compared to that under the individual PS-NPs and Cd stress. Specifically, the Cd content in the aboveground parts of the plant significantly increased by 81.8% in the C1N1 stress compared to that of C1 (P < 0.05). The Cd content in the aboveground parts in the C2N2 was 1.2-fold that of C2. The trends of Cd accumulation in S. alfredii roots affected by individual and combined effects of PS-NPs and Cd were similar to those of Cd accumulation in S. alfredii aboveground parts. Combined PS-NPs and Cd application promoted Cd accumulation compared to the individual Cd stress (Fig 5a).

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Fig 5. Individual and combined effects of PS-NPs and Cd stress on Cd and trace element contents in S. alfredii.

(a): Cd content (mg·kg^-1); (b): Zn content (mg·kg^-1); (c): Cu content (mg·kg^-1); (d): Mn content (mg·kg^-1). PS-NPs: polystyrene nanoplastic; Cd: cadmium.C1 and C2 respectively represented the concentration of Cd (0.6 and 4 mg·kg^-1), and N1 and N2 respectively represented the concentration of PS-NPs (100 and 1000 mg·kg^-1). Different letters indicate significant differences in the results; the same letters indicate non-significant differences in the results (P < 0.05).

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The Zn, Cu and Mn contents of S. alfredii in individual and combined stress of PS-NPs and Cd was significantly reduced compared to the CK except in the N1 stress. The Zn, Cu and Mn contents of aboveground parts in the N2 stress decreased significantly by 13.3%, 13.3% and 14.3% respectively compared to the CK. The Zn, Cu and Mn contents of aboveground parts in the individual Cd stress was significantly lower than that the CK (P < 0.05). The C2 stress resulted in a 55.8% decrease in Zn content, a 58.4% decrease in Cu content, and a 53.8% decrease in Mn content in the aboveground parts. Combined PS-NPs and Cd stress had a stronger inhibitory effect on the Zn, Cu and Mn contents of aboveground parts compared to the individual Cd stress. The Zn, Cu and Mn contents of S. alfredii under the C2N2 stress reduced significantly by 17.9%, 16.0% and 12.3%, respectively, compared to the C2 stress (P < 0.05) (Fig 5b, 5c, 5d).

The results of the trace elements contents of root in individual and combined stress of PS-NPs and Cd were similar to the aboveground parts. The Zn and Cu contents of root showed the most significant effects in the individual PS-NPs stress. The C2 stress showed a 65.4% decrease in Zn content, a 51.2% decrease in Cu content, and a 51.9% decrease in Mn content. Combined PS-NPs and Cd stress had a stronger inhibitory effect on the Zn, Cu and Mn contents of roots compared to the individual Cd stress. The Zn, Cu and Mn contents of roots under the C2N2 stress reduced significantly by 13.5%, 16.9% and 2.9%, respectively, compared to the C2 stress (P < 0.05) (Fig 5b, 5c, 5d).

Individual and combined effects of PS-NPs and Cd on Cd speciation in soil

Compared with CK, PS-NPs stress alone had no significant effect on the speciation of Cd in the soil. The proportions (%) of different Cd speciation were in the order of carbonate-bound Cd > residue-bound Cd > Fe-Mn oxide-bound Cd > exchangeable Cd > organic-bound Cd Compared with CK, Cd stress alone significantly increased the proportions of exchangeable Cd, carbonate-bound Cd, and Fe-Mn oxide-bound Cd, while decreasing the proportions of organic-bound Cd and residue-bound Cd. Moreover, the changes in these proportions became more pronounced with increasing Cd concentration. Combined stress of PS-NPs and Cd (C1N1, C1N2, C2N1, C2N2) further increased the proportions of exchangeable Cd and carbonate-bound Cd compared with Cd stress alone (C1, C2). The proportion of exchangeable Cd and carbonate-bound Cd under the C1N2 stress increased significantly by 40.90% and 16.77%, respectively, compared to the C1 stress (P < 0.05); however, the proportion of Fe-Mn oxide-bound Cd, organic-bound Cd and residue-bound Cd under the C2N2 stress increased significantly by 15.78%, 19.55% and 18.00%, respectively, compared to the C2 stress (P < 0.05). In other words, the combined stress of PS-NPs and Cd increased the bioavailability of Cd in the soil (Fig 6)

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Fig 6. Individual and combined effects of PS-NPs and Cd stress on Cd speciation contents in soil.

PS-NPs: polystyrene nanoplastic; Cd: cadmium.C1 and C2 respectively represented the concentration of Cd (0.6 and 4 mg·kg^-1), and N1 and N2 respectively represented the concentration of PS-NPs (100 and 1000 mg·kg^-1). Different letters indicate significant differences in the results; the same letters indicate non-significant differences in the results (P < 0.05).

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Discussion

Individual and combined effects of PS-NPs and Cd on S. alfredii growth

According to the results of the present study, the individual PS-NPs stress decreased the height and fresh weight of S. alfredii, and the inhibitory effect of PS-NPs on plant height and fresh weight increased with an increase in the concentration of PS-NPs. Consistent with our findings, Xie et al. [33] reported that polyvinyl chloride (PVC) significantly inhibited the growth of Chlorella vulgaris, with a higher concentration of microplastics (1000 mg·L^-¹) amplifying this inhibitory effect The addition of MPs/NPs has been shown to inhibit free individual cells and crop growth, with PS-MPs of different particle sizes exerting varying effects on plant growth [38–40]. We speculate that this may be due to the fact that the irregular surfaces of MPs/NPs cause damage to plant roots, with higher concentrations posing greater harm; and additives in these particles (e.g., plasticizers, stabilizers, and pigments et al.) can be entered into soils, which can cause hazardous effects to the growth of plants [9,41]. In addition, MPs/NPs may enter and block roots and root epidermis of plants, inhibiting the absorption of water and nutrients directly [16,42]. However, Yang et al. [43] found that the application of PS-NPs increased the height of Isatis indigotica. The addition of MPs/NPs, as high-molecular polymers with the high content of carbon, can lead to the increase of total carbon content in soils, which might be beneficial to plants.

Furthermore, the present study found that individual Cd stress inhibited the growth of S. alfredii in a concentration-dependent manner, a result consistent with the findings of Yang et al.. [44]. The individual Cd stress can damage the apical meristem, chloroplast ultrastructure, membrane system, and various organelles in S. alfredii. In addition, the individual Cd stress inhibits GSH biosynthesis, leading to the accumulation of excess H₂O₂ and reactive oxygen species (ROS), thereby affecting the activity of related enzymes and the overall growth of S. alfredii.

The experimental results showed that a combination of PS-NPs and Cd stress exerted a stronger inhibitory effect on the growth of S. alfredii than the individual PS-NPs or Cd stress. PS-NPs can adsorb Cd through electrostatic attraction between Cd and functional groups on the surface of PS, and the adsorbed Cd would co-transport with its carrier PS [45], the amount of Cd accumulated in plants would be increased, inhibiting the absorption of water and nutrients, thereby restricting root growth. In addition, combined PS-NPs and Cd may more seriously restrict photosynthesis and enhance oxidative stress damage, thereby affecting the growth of plants. According to previous study by Liu et al. [32], combined PS-MPs and Pb can decrease growth indices compared to the individual PS-MPs stress and enhance growth inhibition effects among plants. Furthermore, Dong et al. [46] observed that when plants were exposed to combined arsenic (As) and PS (at concentrations of 0.04 and 0.1 g·L⁻¹), the reduction in root and leaf biomass was less than that under As the individual stress, while the application of combined As and PS at 0.2 g·L⁻¹ reduced root and leaf biomass more than the individual As stress. When MPs and heavy metals are present in combination, these particles can act as carriers of heavy metals to exacerbate their toxicity of heavy metals, resulting in a synergistic effect and enhancing plant growth inhibition. However, a study by Zong et al. [30] found that combined PS-NPs and Cd stress had a strong positive effect on the shoot length of Triticum aestivum L. compared to the individual Cd stress, indicating that PS-NPs countered the negative impact of Cd on the growth of T. aestivum L. Due to differences in their composition and surface functional groups, MPs/NPs exhibit variations in their Cd adsorption-desorption properties, which result in differential effects on plant growth in soils containing combined MPs/NPs and Cd.

Individual and combined effects of PS-NPs and Cd on antioxidant enzyme activities and MDA content in S. alfredii

Plants cope with external stress through the activity of various antioxidant enzymes. These enzymes maintain a dynamic balance between the generation and elimination of free radicals in plant tissues through synergistic effects to prevent oxidative damage caused by the excessive production of free radicals, thereby alleviating the toxic effects of the external environment on plants. However, the excessive accumulation of ROS under stress conditions damages the expression systems and structure of antioxidant enzymes, resulting in reduced enzyme activity [47,48].

In this study, it was observed that the individual PS-NPs stress increased SOD activity, and the effects increased with an increase in the concentration of PS-NPs. The increase of SOD activity may be attributed to the large accumulation of ROS, hence causing oxidative stress and increasing the levels of antioxidants in roots and leaves, thereby producing antioxidant enzymes. Guo et al. [49] and Niu et al. [50] both found that the SOD activity was significantly reduced under the individual PE-MPs or PS-NPs stress compared to the CK. These differences in results may be due to the variation in the concentration of MPs/NPs and the plants used. On the one hand, the concentrations of PS-NPs used in the previous research were too high to endure the individual MPs/NPs stress, resulting in reduced SOD activity. On the other hand, the Cd hypertolerance and hyperaccumulation traits of S. alfredii are supported by its physiological status response to external Cd level and high Cd accumulation concentration in shoots [51]. A highly intricate network of Cd tolerance genes of S. alfredii orchestrates multiple physiological processes. These processes include the antioxidant system, induction of defense-related genes, and calcium signaling pathways, collectively contributing to the plant’s robust Cd-tolerance mechanism [52]. Furthermore, in the present study, no significant differences were observed in POD activity between the control and low PS-NPs concentration, while a high PS-NPs concentration increased POD activity compared to the control. A high PS-NPs concentration induced the production of free radicals, and S. alfredii responded to excess ROS by increasing POD activity, thereby alleviating the toxic effects of the external environment on S. alfredii. According to research by Guo et al. [47] and Niu et al. [53], the effects of MPs on POD exhibited a hormesis effect, implying that a low concentration of MPs increased POD activity, while a high MPs concentration damaged the antioxidant defense system of plants, thereby decreasing POD activity. This may have occurred because the excessive accumulation of ROS under a high MPs concentration destroys the expression systems and structure of antioxidant enzymes, resulting in reduced enzyme activity.

The present study showed that the individual Cd stress increased antioxidant enzyme activity and MDA content, and the effect was positively correlated with the Cd concentration. Previous research indicated that antioxidant enzyme activity increased significantly under the individual Cd stress [54]. Qin et al. [55] found that antioxidant enzyme activity increased at low heavy metal concentrations but decreased at high heavy metal concentrations, possibly because high heavy metal concentrations caused severe damage in plants.

According to the results of the present study, the combined treatment of low-concentration PS-NPs and Cd exerted no significant effect on the antioxidant enzyme activity in S. alfredii. However, the combination of a high PS-NPs concentration and Cd increased SOD and CAT activities compared to the individual PS-NPs and Cd stress. These results could be due to the change in the PS-NPs concentration. The adsorption of Cd onto PS-NPs increased with the increase of the PS-NPs concentration, which increasing the levels of antioxidants in roots and leaves owing to the oxidative stress on plant function. However, according to a study by Liu et al. [32], combined PS-MPs and Pb increased SOD activity and decreased CAT activity, and the effect was reduced with an increase in the combined PS-MPs concentration. This finding is inconsistent with the results of this study, which could be due to differences in the types of heavy metals, MPs/NPs, and plant species used.

Individual and combined effects of PS-NPs and Cd on Cd chelation in S. alfredii

The experimental results showed that GSH, NPT, and PCs increased significantly and increased with the increase of the Cd concentration. The increased NPT, PCs, and GSH contents in S. alfredii could be due to a defense mechanism induced under the individual Cd stress to generate NPT and GSH, which chelate with Cd²⁺ to form thiopeptide complexes that protect plant cells and maintain the natural structure of plants [56,57]. According to a study by Liu et al. [58], the GSH and PCs contents increase significantly under the individual Cd stress, and they also increase with an increase in Cd concentration, in Salix variegata. Yu et al. [59] also found that the GSH and PCs contents were positively correlated with the Cd concentration in Oryza sativa L.

According to the results of the present study, combined PS-NPs and Cd stress increased the levels of GSH, NPT, and PCs in S. alfredii leaves. Combined PS-NPs and Cd stress can increase the Cd content in plants, thereby enhancing the levels of GSH, NPT, and PCs. In addition, NPs that adsorbed Cd enter plants, thereby increasing the Cd content and the levels of GSH, NPT, and PCs in S. alfredii. Combined MPs and Cd have been shown to significantly increase Cd accumulation in S. alfredii, AHG347, and wheat [60,61]. A previous study by Duan et al. [31] revealed that combined MPs and Cd increased Cd accumulation in sorghum. The organic substances on MPs surfaces can form water-soluble or heavy metal complexes with metal ions, contributing to the accumulation of Cd [62], thereby inducing Cd chelation. Therefore, the exposure of plants to the combination of PS-NPs and Cd can promote Cd accumulation and the synthesis of GSH, NPT, and PCs to a great extent.

Individual and combined effects of PS-NPs and Cd on trace element, Cd and Cd speciation contents in S. alfredii

In the present study, we found combined PS-NPs and Cd stress significantly increased the Cd contents in S. alfredii. We speculate that this may have been due to the fact that PS-NPs can adsorb Cd through electrostatic attraction between Cd and functional groups on the surface of PS, and the adsorbed Cd would co-transport with its carrier PS [45,63], and may be more easily absorbed by plants [20]. Both individual Cd stress and combined PS-NPs/Cd stress elevated the exchangeable Cd fraction in soil, which in turn enhanced Cd accumulation in S. alfredii. However, Xie et al. [64] indicated that PLA-MPs significantly reduced the Cd contents in pakchoi under the highest Cd-concentration stress. On the one hand, we postulate that the reason for decreased Cd contents in pakchoi may have been that MPs/NPs have been found to adsorb onto root surfaces [65] to compete with Cd for adsorption sites. On the other hand, MPs/NPs may improve the bioavailability of Fe and Mn in soil and their uptake in rice roots, thus facilitating the formation of iron-manganese plaques on plants roots to reduce Cd accumulation.

In addition, our study showed that the Zn, Cu and Mn contents of S. alfredii were significantly reduced under most treatments compared to the CK. Xie et al. [33] observed that PLA-MPs significantly reduced the Mg and Mn contents in pakchoi under the highest Cd-concentration stress. As the concentration of Cd increases, S. alfredii exhibits a significant decrease in the accumulation of trace metals Zn, Cu and Mn. Combined PS-NPs and Cd stress had a stronger inhibitory effect on the Zn, Cu and Mn contents compared to the individual Cd stress. This phenomenon could be attributed to the potential of PS-MPs to adsorb metal ions from the environment, thereby reducing the concentration of metal ions available for plant absorption in soil, and the accumulation of these trace metals [66]. Alternatively, the presence of PS-NPs and Cd might interfere with the normal physiological and ecological functions of S. alfredii, leading to changes in the S. alfredii ‘s demand for trace metals [64].

MPs/NPs may alter the mobility and bioavailability of heavy metals in soils, which has implications for crop growth and heavy metal accumulation. In the present study, the results for the different speciation of Cd content in soil showed that the changes of the proportion of Cd in each speciation of soil in the all stresses was significant under the individual Cd stress and combined PS-NPs and Cd stress. The addition of MPs/NPs can affect the soil pH, soil aeration, microporosity and total carbon content and so on [67,68], thereby changing the forms of Cd content in soil [69]. Li et al. [70] found that MPs can adsorb Cd in the soil through their strong adsorption properties or affect the bioavailability of Cd. Cao et al. [71] indicated that polypropylene (PP) microplastics increased the concentration of bioavailable Cd in soils via decreasing soil retention of Cd by the organo-mineral complexes fraction. And MPs can alter the physicochemical properties and microbial community of soil, thereby indirectly affecting the form and bioavailability of heavy metals [70,72]. Studies have shown that different types of MPs affected Cd bioavailability; the type, aging degree, and soil environmental conditions of MPs may impact MPs influencing Cd form [73–75].

Our study showed that combined PS-NPs and Cd stress increased the content of the exchangeable state, carbonate-bound state, and Fe-Mn oxide-bound state of Cd and reduced the content of the organic-bound state. The change of the speciation of Cd content in soil can increase the bioavailability and mobility of heavy metals in the soil and thus enhancing the toxicity of heavy metals to plants [31,33]. The decrease of biomass, contents of Zn, Mn, and Cu and the increase of activities of antioxidants could also prove the increasing of toxicity under combined PS-NPs and Cd stress. The changes in Cd form caused by MPs/NPs can affect the migration of Cd to organisms, thus requiring a new assessment of the ecological risks of combined PS-NPs and Cd.

Conclusions

In conclusion, the findings of this study suggested that Sedum alfredii Hance growth was inhibited and that oxidative damage was induced under the individual polystyrene nanoplastics (PS-NPs) or cadmium (Cd) stress, and the inhibitory effect of the individual Cd stress was more significant than the individual PS-NPs stress. Combined PS-NPs and Cd stress enhanced the inhibitory effect of growth, antioxidant enzyme activities and MDA content compared to individual PS-NPs or Cd stress. Furthermore, combined PS-NPs and Cd increased the Cd contents of the exchangeable state, carbonate-bound state and Fe-Mn oxide-bound state, and reduced the Cd content of the organic-bound state, thereby enhancing the toxicity of Cd to S. alfredii. Combined PS-NPs and Cd stress promoted Cd accumulation in S. alfredii., thereby increasing Cd chelation (GSH, NPT, and PCs) compared to the individual Cd stress.

These findings discoverd that combined PS-NPs and Cd treatments increased the contents of the exchangeable Cd and carbonate-bound Cd, thereby significantly increasing the Cd content and restraining the growth in S. alfredii. PS-NPs and Cd had potential synergistic effects on the toxicity of the S. alfredii, which holds significant implications for understanding the environmental risks associated with the combination of NPs and Cd. This study provided new perspectives for a deeper understanding of hyperaccumulator plants and provide data support for the management of pollution through it.

Supporting information

S1 File.

Supporting information 1. Dataset in this study.

https://doi.org/10.1371/journal.pone.0344578.s001

(XLSX)

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Figures

Abstract

Introduction

Materials and methods

Experimental materials

Experimental design

Measurement of growth and physiological parameters

Determination of trace element contents and Cd content in S. alfredii

Determination of Cd speciation in soil

Statistical analysis

Results

Individual and combined effects of PS-NPs and Cd on S. alfredii growth

Individual and combined effects of PS-NPs and Cd on antioxidant enzyme activities and MDA content in S. alfredii

Individual and combined effects of PS-NPs and Cd on Cd chelation in S. alfredii leaves

Individual and combined effects of PS-NPs and Cd on Cd and trace element contents in S. alfredii

Individual and combined effects of PS-NPs and Cd on Cd speciation in soil

Discussion

Individual and combined effects of PS-NPs and Cd on S. alfredii growth

Individual and combined effects of PS-NPs and Cd on antioxidant enzyme activities and MDA content in S. alfredii

Individual and combined effects of PS-NPs and Cd on Cd chelation in S. alfredii

Conclusions

Supporting information

S1 File.

References