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Article

Influencing Factors of Bidens pilosa L. Hyperaccumulating Cadmium Explored by the Real-Time Uptake of Cd2+ Influx around Root Apexes under Different Exogenous Nutrient Ion Levels

by
Siqi Wang
1,*,
Huiping Dai
2,
Dandan Ji
3,
Shuang Cui
1,
Chengzhi Jiang
1,
Lidia Skuza
4,
Lianzhen Li
5,*,
Dariusz Grzebelus
6 and
Shuhe Wei
3
1
Academy of Environmental and Chemical Engineering, Shenyang Ligong University, Shenyang 110159, China
2
Shaanxi Province Key Laboratory of Bio-Resources, Qinling-Bashan Mountains Bioresources Comprehensive Development C.I.C, State Key Laboratory of Biological Resources and Ecological Environment Jointly Built by Qinba Province and Ministry, College of Biological Science & Engineering, Shaanxi University of Technology, Hanzhong 723001, China
3
Key Laboratory of Pollution Ecology and Environment Engineering, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016, China
4
Centre for Molecular Biology and Biotechnology, Institute of Biology, University of Szczecin, 71-415 Szczecin, Poland
5
College of Environmental Sciences and Engineering, Qingdao University, Qingdao 266071, China
6
Department of Plant Biology and Biotechnology, Faculty of Biotechnology and Horticulture, University of Agriculture in Krakow, 31-120 Krakow, Poland
*
Authors to whom correspondence should be addressed.
Toxics 2023, 11(3), 227; https://doi.org/10.3390/toxics11030227
Submission received: 15 February 2023 / Revised: 22 February 2023 / Accepted: 23 February 2023 / Published: 27 February 2023
(This article belongs to the Special Issue Phytotoxicity of Heavy Metals in Contaminated Soils)
Browse Figures
Versions Notes

Abstract

:
Though Bidens pilosa L. has been confirmed to be a potential Cd hyperaccumulator, the accumulation mechanism is not yet clear. The dynamic and real-time uptake of Cd2+ influx by B. pilosa root apexes was determined using non-invasive micro-test technology (NMT), which partly explored the influencing factors of the Cd hyperaccumulation mechanism under the conditions of different exogenous nutrient ions. The results indicated that Cd2+ influxes at 300 μm around the root tips decreased under Cd treatments with 16 mM Ca2+, 8 mM Mg2+, 0.5 mM Fe2+, 8 mM SO42− or 18 mM K+ compared to single Cd treatments. The Cd treatments with a high concentration of nutrient ions showed an antagonistic effect on Cd2+ uptake. However, Cd treatments with 1 mM Ca2+, 0.5 mM Mg2+, 0.5 mM SO42− or 2 mM K+ had no effect on the Cd2+ influxes as compared with single Cd treatments. It is worth noting that the Cd treatment with 0.05 mM Fe2+ markedly increased Cd2+ influxes. The addition of 0.05 mM Fe2+ exhibited a synergistic effect on Cd uptake, which could be low concentration Fe2+ rarely involved in blocking Cd2+ influx and often forming an oxide membrane on the root surface to help the Cd uptake by B. pilosa. The results also showed that Cd treatments with high concentration of nutrient ions significantly increased the concentrations of chlorophyll and carotenoid in leaves and the root vigor of B. pilosa relative to single Cd treatments. Our research provides novel perspectives with respect to Cd uptake dynamic characteristics by B. pilosa roots under different exogenous nutrient ion levels, and shows that the addition of 0.05 mM Fe2+ could promote the phytoremediation efficiency for B. pilosa.

1. Introduction

Cadmium (Cd), a major pollutant of soils, is liable to transportation and accumulation in plants. The morphology and structure of roots are affected by Cd toxicity and this results in elongation limitation, epidermal tissue disturbance and root hair number decrease [1]. However, the roots of hyperaccumulators have a strong capability to uptake and immobilize Cd by compartmentalizing in cell walls and vacuoles, thus alleviating Cd stress [2]. Lan et al., (2018) discovered that the Cd-resistance mechanisms of Microsorum pteropus Copel. roots were the regulation of antioxidant enzyme system and the enhancement of energy metabolism [3]. The amount of bioavailable Cd was mainly determined by the soil characteristics, and the Cd bioavailability was influenced by multiple factors in soils, such as: soil texture, pH, CEC, contents of organic matter, clay and nutrient ions, etc., which all affected the Cd bioavailability in soils, and further affected Cd accumulation and distribution in plants [4,5].
Bidens pilosa L. belongs to the Bidens L. genus of Asteraceae. B. pilosa, an annual herb and it is a widespread weedy plant that originated from North America. It is characterized by fast growth and strong adaptability to adverse habitats [6,7]. Wei et al., (2008) also found that the Cd content in B. pilosa leaves and stems were 192 and 115 mg/kg, respectively, while the Cd concentration in contaminated soil was 100 mg/kg. The enrichment and translocation factors were all greater than 1.0, and the biomass was not significantly affected, as compared to the controls [8]. Sun et al., (2009) verified that the addition of Cd (≤25 mg/kg) increased the growth of B. pilosa by 34.5–104.4%. Cd content in stems and leaves was 103 and 110 mg/kg, respectively, and the bioaccumulation and transfer factors were 3.0 and 7.9, when the Cd concentration was 10 mg/kg in soils [9]. Han et al., (2020) showed that the aqueous extract from the stem of B. pilosa increased Cd accumulation capacity of Solanum nigrum L. by 44%, as compared to the controls, when the Cd concentration was 1.5 mg/kg soil. They also found that the addition of the aqueous extract improved enzyme activities and the number of microorganisms in soils [10]. Wei et al., (2018) suggested that the antioxidant enzyme activities of B. pilosa could up-regulate to cope with Cd stress, for instance, the CAT and POD activities of leaves increased significantly under the 10~40 mg/kg Cd stress relative to the controls, but the enzyme activities decreased under the 60 mg/kg Cd concentration. The height of plant was up to peak under treatment with 40 mg/kg Cd, and the net photosynthetic rate and the biomass of roots and stems were increased after exposure to both 40 mg/kg and 60 mg/kg Cd, but leaf biomass was not impacted significantly by the Cd treatments [11]. Dai et al., (2021) found that no significant differences were observed from chlorophyll a and b in the B. pilosa leaves between the controls and treatment with 2.57 mg/kg Cd, and the concentrations of chlorophyll increased with the increase in Cd contents in soils [12].
Non-invasive micro-test technology (NMT) has been applied universally in the detection of the dynamic and real-time uptake of ions by plant roots and it primarily originated from the advantages of dynamic measurements, non-destructive, multi-site scanning and high precision [13]. Wang et al. (2022) discovered that the highest Cd2+ influx appeared at 300 μm from the soybean seedling root apex. He also showed that the differences in Cd2+ influx to the root tips existed between different soybean cultivars and Cd2+ influxes increased significantly after pre-exposure to 5 µM Cd2+ compared with controls [14]. Wu et al., (2019) explored the impacts of exogenous Zn on Cd uptake by pakchoi roots by NMT. He also suggested that the net Cd2+ influx of pakchoi roots reduced with the increase in Zn levels, and the Cd2+ influx at 200 μm from the root quiescent center was inhibited under treatments with 1μM Zn2+ as compared to the controls [15]. Sun et al., (2013) explored the spatial characteristics of Cd transport in two ecotypes of Sedum alfredii Hance by using NMT and demonstrated that the highest Cd2+ influxes were mainly distributed in the root tips and root hairs [16]. Li et al., (2017a) selected three common wetland plant species as materials to explore the Cd uptake mechanisms by plants under NMT application and found that the highest Cd2+ influx was located in the meristematic zone (at positions 100 and 200 μm from the root tip of Typha latifolia Linn. and Canna indica L.) under 10 μM Cd stress and the Cd2+ fluxes reversed from efflux to influx at 500 μm of the root apex of Phragmites australis Trin. [17].
Numerous studies have concentrated on Cd enrichment by different organs of B. pilosa recently. Nevertheless, the quantification and real-time monitoring of Cd uptake by B. pilosa roots has been a conundrum up to now, and little research has been completed in support of the Cd2+ dynamic uptake. Thus, this experiment aimed to investigate the effects of different exogenous nutrient ions on Cd uptake by B. pilosa roots with the application of NMT. These new discovers are quite new. We hypothesized that the Cd2+ influx in B. pilosa roots exhibited significant differences under Cd treatments with different exogenous nutrient ions.

2. Materials and Methods

2.1. Plant Culture and Treatment

The experiment was conducted in a greenhouse located in the Shenyang Institute of Applied Ecology of the Chinese Academy of Sciences (123°59′ E and 41°92′ N). The seeds of B. pilosa were collected from plots and fields in the experimental station when they reached the maturity phase. The root integrity and activity were crucial to B. pilosa as qualified experimental materials in NMT and the sand culture was in favor of root growth and kept the root from rotting. So, sand culture was the main cultivation method in our experimental design. Twenty seeds of B. pilosa were sown in pots filled with sterile sand at a depth of 2 cm after prior surface disinfection. The seeds were cultivated in the greenhouse at 24 ± 2 °C at an 8 h/16 h dark/light cycle. Before germination, Hoagland’s solution was poured into each pot with 20 mL every day. After germination, uniform seedlings were screened to ten plants per pot, and intact seedlings of B. pilosa were treated with 10 μM Cd2+ (as CdCl2 × 2.5 H2O), KH2PO4 was replaced with KCl to avoid the formation of Cd phosphate precipitations in solution, and different concentrations of inorganic ions Ca2+, Mg2+, Fe2+, SO42−, Na+ and K+ treatments were used as shown in the Table 1. The pH of the solutions was kept at 5.5 ± 0.2 by the addition of 2 mM MES (2-morpholinoethanesulphonic acid). Meanwhile, the sterile nutrient solutions without Cd2+ were used as controls and 20 mL was poured every day. Every treatment was repeated three times and each pot was arranged randomly during the experiments. The plants were harvested after ten days from germination.

2.2. Measurements of Cd2+ Fluxes by NMT

Firstly, the primary root from the intact plant of B. pilosa seedlings was selected and fixed loosely in the measuring chamber. Secondly, the preparation of mother solutions consisting of 0.1 mM Ca(NO3)2, 0.1 mM KNO3, and 1 mM NaCl was completed and the measuring solution (100 μM Cd2+) and calibration solutions (50 μM Cd2+ and 500 μM Cd2+) were obtained on the basis of the mother solutions. Secondly, the roots of B. pilosa seedlings were cleaned and soaked in the measuring solution, then the roots were fixed in a culture dish filled with measuring solution. The Cd2+ fluxes from the root apex of B. pilosa were determined by the scanning ion-selective electrode technique (SIET system BIO-001A; Younger USA, LLC, Lothian, MA, USA). The positive values represent effluxes and negative values represent influxes. Meanwhile, the cadmium ion selective microelectrode was corrected by calibration solutions during testing. The scanning locations from the root apex were 0 μm, 100 μm, 200 μm, 300 μm, 400 μm, 500 μm, 600 μm, 700 μm and 800 μm and the data were processed using Mage Flux [14,18,19].

2.3. Measurements of Chlorophyll, Carotenoid and Root Vigor

Briefly, the fresh leaf samples of B. pilosa seedling were homogenized in 95% ethanol by using a pre-chilled pestle and mortar, and then the homogenates were centrifuged at 10,000 rpm for 20 min at 4 °C. The supernatant was used to separate chlorophyll a, b and carotenoid by 80% acetone. The concentrations of chlorophyll a, b and carotenoid were determined by a UV-visible near infrared spectrophotometer (UV-3600i Plus) at 665 nm, 649 nm and 470 nm [20,21]. Root vigor is a significant indicator of inorganic ion uptake by roots, and it is characterized by dehydrogenase activity, which is measured by the reduction amount of triphenyl tetrazole chloride (TTC) per unit time [22].

2.4. Determination of Biomass, Cd Concentration and Quality Control

The harvested roots and shoots of B. pilosa were separated and washed with ultra-pure water. The samples were oven dried at 100 °C for 30 min and then at 80 °C to a constant weight. The biomass was measured by a balance accurate to 0.001 g.
Briefly, the roots of B. pilosa seedlings were soaked in 0.02 M EDTA solution to remove any non-specifically bound Cd, and subsequently washed with deionized water, oven-dried for 35 min at 100 °C, then at 50 °C until constant weight, ground to powders and digested with a mixture of concentrated HNO3 and HClO4 (87:13, v/v) [23]. Meanwhile, the inductively coupled plasma optical emission spectrometer (ICP-OES) method was used to determine Cd concentration in all samples (Optima 8000) [24]. The measured contents of Cd in plants of B. pilosa seedlings were checked by using standard reference material for plant composition analysis (GBW07604, GSV-3, poplar leaves), and the Cd recovery rate was 91 ± 2% after determination [25].

2.5. Data Processing and Statistical Analysis

Microsoft EXCEL 2010 was used to calculate the average and standard deviation (SD) and for preparation of graphs. Data statistical analysis was conducted by SPSS 25.0 and DPS (V 9.01). Data in figures are shown as mean ± standard deviation (n = 3). Least significant difference (LSD) tests were used by for evaluating significant differences among Cd2+ influxes under different treatments at p < 0.05 level with different uppercase or lowercase letters, and a one-way ANOVA was used to compare the means of the physiological index under different treatments at p < 0.05 level with different uppercase or lowercase letters [26,27,28].

3. Results

3.1. Effects of Cd Treatments with Different Nutrient Ions on Cd2+ Influxes to the Root of B. pilosa

As shown in Figure 1A, the negative values of the net flux denoted the influxes from the solutions to the roots. So, the comparative analyses of Cd2+ influxes under different treatments were based on absolute values. Cd2+ influxes to the root apexes of Cd-treated plants were higher than that of the controls. The results also showed an obvious spatial distribution of Cd2+ influxes, with the highest Cd2+ influxes located at 300 μm from the root apex, which could be a typical site for an analysis of the differences in Cd uptake by B. pilosa roots under Cd treatments with different exogenous ions. The influxes gradually decreased at other locations around this site (Figure 1A). Uptake of Cd2+ into the root of B. pilosa was inhibited by Cd treatments with 16 mM Ca2+ and 8 mM Mg2+. However, the Cd treatments with 1 mM Ca2+ and 0.5 mM Mg2+ had little effect on the net Cd2+ influxes at 300 μm from the root tip, as compared to the Cd treatment alone (Figure 1B,C). Cd2+ uptake by B. pilosa roots was also reduced by adding 0.5 mM Fe2+ and 8 mM SO42−. The Cd treatment with 0.05 mM Fe2+ significantly increased (p < 0.05) the Cd2+ influxes from B. pilosa roots (Figure 1D). However, no significant differences (p > 0.05) were observed between Cd treatments with 0.5 mM SO42− and Cd stress alone (Figure 1E). Upon the increase in the K+ concentration in solutions from 2 mM to 18 mM, the net Cd2+ influx of the roots decreased by 62.14% at 300 μm from the root tips. However, there were no significant (p > 0.05) differences between Cd treatments with 2 mM K+ and the Cd treatments alone (Figure 1F).

3.2. Effects of Cd Treatments with Different Nutrient Ions on Biomass and Cd Accumulation of B. pilosa

As shown from Figure 2A, the shoot biomass of B. pilosa did not change significantly (p > 0.05) under 10 μM Cd stresses compared with the controls, which indicates that B. pilosa conformed to the basic characteristics of a Cd hyperaccumulator. Cd treatments with 16 mM Ca2+ and 8 mM Mg2+ significantly (p < 0.05) promoted the growth of B. pilosa as compared to single Cd treatments. However, no significant (p > 0.05) changes were observed between Cd treatments with 1 mM Ca2+, 0.5 mM Mg2+ and Cd treatment alone (Figure 2B,C). The shoot biomass increased significantly (p < 0.05) by 15.33% and 15.95% under Cd treatments with 0.5 mM Fe2+ and 8 mM SO42−, respectively, as compared to the Cd stress alone. However, Cd treatment with 0.05 mM Fe2+ decreased the biomass significantly (p < 0.05) by 14.20% (Figure 2D,E). A significant (p < 0.05) increase in shoot biomass (14.96%) of B. pilosa was found for Cd treatments with 18 mM K+. However, Cd treatments with 2 mM K+ had no effect on biomass relative to the Cd treatment alone (Figure 2F).
The Cd contents of B. pilosa plants were 501.95 mg/kg under 10 μM Cd treatments (Figure 2A). The Cd treatments with 16 mM Ca2+ and 8 mM Mg2+ significantly (p < 0.05) reduced the Cd accumulation of B. pilosa, as compared to the Cd stress alone. However, no significant (p > 0.05) changes were observed between Cd treatments with 1 mM Ca2+, 0.5 mM Mg2+ and Cd treatment alone (Figure 2B,C). Cd contents of B. pilosa were significantly (p < 0.05) decreased by 31.19% and 57.77% under Cd treatments with 0.5 mM Fe2+ and 8 mM SO42−, respectively, while the Cd contents increased by 35.06% when the plants were Cd-treated with the addition of 0.05 mM Fe2+, as compared to Cd treatment alone. However, Cd contents did not change significantly (p > 0.05) under Cd treatments with 0.5 mM SO42− relative to the Cd stress alone (Figure 2D,E). A significant (p < 0.05) reduction in Cd contents (39.63%) was found under Cd treatments with 18 mM K+. Furthermore, Cd treatments with 2 mM K+ had no effect on Cd content (Figure 2F).

3.3. Impacts of Cd Treatments with Different Nutrient Ions on Chlorophyll a and b of B. pilosa

As shown from Figure 3A, the chlorophyll a and b of B. pilosa did not have significant (p > 0.05) variations with 10 μM Cd treatments, which indicated that B. pilosa exhibited remarkable tolerance as a Cd hyperaccumulator. The concentrations of chlorophyll a and b from B. pilosa leaves under Cd treatments with different nutrient ions showed the same change trends (Figure 3). There were no significant (p > 0.05) differences between the Cd treatments with 1 mM Ca2+, 0.5 mM Mg2+ and single Cd treatments. Obviously, the chlorophyll a and b concentrations under Cd treatments with 16 mM Ca2+ and 8 mM Mg2+ were all higher than that of Cd stress alone (Figure 3B,C). The concentrations of chlorophyll a and b significantly (p < 0.05) increased by 10.04%, 14.96% and 17.77%, 27.05% under Cd treatments with 0.5 mM Fe2+ and 8 mM SO42−, respectively, as compared to single Cd treatments. The concentrations of chlorophyll a and b decreased by 11.82% and 12.61% under Cd treatments with 0.05 mM Fe2+, respectively, as compared with single Cd treatments. However, the concentrations of chlorophyll a and b showed no significant (p > 0.05) differences when the plants were Cd-treated with 0.5 mM SO42− as compared with the Cd stress alone (Figure 3D,E). Furthermore, the concentrations of chlorophyll a and b under Cd treatment with 18 mM K+ were significantly (p < 0.05) higher (26.15% and 27.57%) than that of Cd treatment alone. However, Cd treatments with 2 mM K+ had no effect on the concentrations of chlorophyll a and b (Figure 3F).

3.4. Effects of Cd Treatments with Different Nutrient Ions on Carotenoid and Root Vigor of B. pilosa

There were no significant (p > 0.05) changes in carotenoid concentrations and root vigor under 10 μM Cd treatments compared with controls; this was mainly determined by the tolerance of B. pilosa seedlings to Cd (Figure 4A). No significant (p > 0.05) variations of carotenoid concentrations were observed under Cd treatments with 1 mM and 16 mM Ca2+ compared with single Cd treatments, but the Cd treatments with 8 mM Mg2+ exhibited a significant (p < 0.05) increase (15.44%) in B. pilosa seedling leaves (Figure 4B,C). The Cd treatments with 0.05 mM Fe2+ significantly (p < 0.05) decreased the carotenoid concentrations (20.62%) compared to Cd treatments alone, while no significant (p > 0.05) changes were observed between Cd treatments with 0.5 mM Fe2+ and the Cd treatment alone (Figure 4D). Furthermore, the carotenoid concentrations with Cd treatment with 8 mM SO42− were significantly (p < 0.05) higher (11.44%) than that of single Cd treatments (Figure 4E). The concentrations of carotenoid increased by 23.08% under Cd treatments with 18 mM K+, as compared with single Cd treatments (Figure 4F).
The Cd treatments with 16 mM Ca2+ and 8 mM Mg2+ significantly (p < 0.05) increased the root vigor of B. pilosa compared to Cd treatment alone, while no significant (p > 0.05) changes were observed between Cd treatments with 1 mM Ca2+, 0.5 mM Mg2+ and the Cd treatment alone (Figure 4B,C). A significant (p < 0.05) decrease (23.08%) in root vigor was found in the Cd treatments with 0.05 mM Fe2+ as compared to Cd treatments alone. The root vigor was significantly (p < 0.05) increased by 15.38% and 20.50% under Cd treatment with 0.5 mM Fe2+ and 8 mM SO42−, respectively. However, Cd treatments with 0.5 mM SO42− had no effect on root vigor relative to the Cd treatment alone (Figure 4D,E). Furthermore, the root vigor under Cd treatment with 18 mM K+ was significantly (p < 0.05) higher (16.65%) than that of Cd treatment alone. However, Cd treatments with 2 mM K+ had no effect on root vigor relative to Cd stress alone (Figure 4F).

4. Discussion

4.1. The Dynamic Uptake of Cd2+ by Accumulator and Hyperaccumulator Roots

Li et al. (2017b) suggested that the distribution of Cd2+ influxes had obvious spatial organization around Sedum plumbizincicola seedling root tips, and the influx of Cd2+ was significantly higher in the meristematic zone. The Cd2+ influx rate was highest about 300 μm from the root tip, and steadily decreased in both directions from this location. In addition, the Cd2+ flux of 50 μM Cd2+ irradiation group was significantly increased. The addition of Cd2+ could regulate and induce transporters that mediate the Cd2+ influx in the plasma membrane of S. plumbizincicola [29]. The views above were basically consistent with our research results, and the highest Cd2+ influxes were located at 300 μm from the root tips of B. pilosa. Cd pretreatments could promote Cd2+ influx compared with controls. Li et al. (2012) studied the dynamic changes of halophyte Suaeda salsa root Cd2+ uptake by kinetic experiments and discovered that the net Cd2+ flux at the maximum flux location (approximately 150 mm from the root tip). Cd uptake was initially very fast, with a net inflow of Cd2+ of about 70 pmol cm−2 s−1, and then rapidly decreased, reaching a steady-state value about 5 min after the addition [30]. By contrast, the Cd stress concentration in our studies was 10 μM and the net Cd2+ influx at 300 μm from the root tip of B. pilosa was −92.12 pmol cm−2 s−1 under medium–low stress.

4.2. Impacts of Different Nutrient Ions on Cd2+ Fluxes of Roots

He et al., (2015) suggested that the Cd uptake by poplar roots was mediated by Ca, and the peak value of net Cd2+ influxes into roots was observed under 0.1 mM Ca2+ treatments [31]. Li et al., (2017b) found the Cd2+ uptake by Sedum plumbizincicola was reduced by 50% when the concentration of K+ increased to 10 mM. The net Cd2+ flux into the root of Sedum plumbizincicola changed from an influx to an efflux when the concentration of Ca2+ was up to 1.0 mM in measuring solutions, and the net Cd2+ influx decreased slightly by 4% at 300 μm from the root apex under treatment with 1.0 mM Mg2+ in solutions [29], Lu et al., (2010) verified that the Cd2+ influxes of Sedum alfredii roots decreased significantly when Ca2+ in nutrient solutions was elevated from 2.0 to 32.0 mM [32]. Perfus-Barbeoch et al. (2002) showed that Cd2+ affected guard cell regulation by entering the cytosol of Arabidopsis thaliana L. through Ca2+ channels [33]. Our results indicated that Cd2+ influxes at 300 μm from the root tips decreased by 37.55%, 48.46% and 62.14% under Cd treatments with 16 mM Ca2+, 8 mM Mg2+ or 18 mM K+. The studies listed above were basically consistent with the results of our studies. Rabêlo et al. (2017) studied the influence of S on Cd uptake by Massai grass roots and discovered that the Cd treatments with 1.9 mM SO42− inhibited the symplastic Cd2+ influx and improved the apoplastic Cd2+ influx in root compared with the Cd treatment alone [34]. Zhang et al., (2020) researched the underlying mechanisms of Cd uptake by the root tips of Vicia sativa with application of NMT and suggested that the Cd uptake was closely related to Fe uptake under Cd treatments with different Fe levels [35]. The views above basically agreed with our research, and the Cd2+ influxes at 300 μm from the root tips of B. pilosa decreased by 26.29% and 21.04%, respectively, under Cd treatments with 8 mM SO42− and 0.5 mM Fe2+ compared to the Cd stress alone. The Cd treatments with a high concentration of nutrient ions showed an antagonistic effect on Cd2+ uptake. It might be that these ions at a high concentration could take up the Cd2+ channels and compete for the binding sites in B. pilosa roots.

4.3. Effects of Different Nutrient Ions on Biomass, Cd Accumulation and Physicochemical Characteristics of Accumulator and Hyperaccumulator

Li et al., (2017b) found that the presence of 10 mM Ca2+ and Mg2+ significantly inhibited Cd2+ uptake by Sedum plumbizincicola, and the higher Ca2+ and Mg2+ concentrations induced lower Cd accumulation, for instance, the Cd contents in the plants reduced from 1121.8 μg/g to 562.5 μg/g when the concentration of Ca2+ shifted from 0.1 mM to 10 mM in solutions [29]. Hakeem et al., (2022) suggested that the root and shoot biomass of Fagopyrum esculentum was enhanced by 7.57% and 11.11%, respectively, under 200 mgL−1 Cd2+ treatments with 300 mgL−1 Ca2+ when compared to the controls, and the exogenous Ca2+ significantly promoted Cd retention in roots and alleviated the Cd-induced oxidative damage [36]. Liu et al. (2020) discovered that 25 μM Cd treatment with 0.5 mM Ca significantly increased the Cd contents in the roots of Sedum alfredii, but the Cd contents in shoots decreased under Cd treatment with 8 mM Ca [37]. Lu et al., (2010) showed that the shoot biomass of Sedum alfredii increased under Cd treatments with 8.0 mM Ca2+ compared with controls, but the biomass decreased obviously when the Ca2+ concentration was greater than 8.0 mM [32]. Our results suggested that Cd treatment with 16 mM Ca2+ induced the shoot biomass of B. pilosa to rise relative to the Cd stress alone, and no significant changes were observed under Cd treatments with 1 mM Ca2+. It was possible that the biomass would be promoted as Ca2+ concentration went up. Tian et al., (2011) explored the effects of Ca application on the antioxidant systems of Sedum alfredii H. roots under Cd-induced oxidative stress and found that the addition of exogenous Ca obviously improved root elongation and decreased the Cd contents in the root apex. The activities of superoxide dismutase (SOD) and catalase (CAT) reduced and the biosynthesis of glutathione (GSH) was promoted in the roots of S. alfredii under 400 μM Cd treatments with 6.0 mM Ca compared with single Cd stress [38]. Rabêlo et al., (2018) evaluated the S influence on alleviating Cd damage in Massai grass and suggested that the sufficient S supply (1.9 mmolL−1) was conducive to the uptake of Cd and the adequate S supply promoted the root length and surface, Cd translocation factor and the contents of other nutrients [39].

5. Conclusions

In summary, the Cd2+ influxes of B. pilosa root under different nutrient ions were measured by NMT, which indicated that Cd2+ influxes at 300 μm around the root apexes decreased under Cd treatments with 16 mM Ca2+, 8 mM Mg2+, 0.5 mM Fe2+, 8 mM SO42− or 18 mM K+ compared with single Cd treatments. The Cd treatments with a high concentration of nutrient ions showed an antagonistic effect on Cd2+ uptake. However, the Cd treatments with 1 mM Ca2+, 0.5 mM Mg2+, 0.5 mM SO42− or 2 mM K+ had little effect on the net Cd2+ influxes compared with the Cd treatment alone. Importantly, Cd treatment with 0.05 mM Fe2+ promoted Cd2+ uptake by the B. pilosa roots. The addition of 0.05 mM Fe2+ exhibited a synergistic effect on Cd uptake, which could be low concentration Fe2+ rarely involved in blocking Cd2+ influx and formed oxide membrane on root surface to help the Cd uptake by B. pilosa. The results also showed that the Cd treatments with a high concentration of nutrient ions significantly increased the concentrations of chlorophyll and carotenoid in leaves and the root vigor of B. pilosa relative to the Cd treatments alone. Our research has provided novel perspectives with respect to Cd uptake dynamic characteristics by B. pilosa roots under different exogenous nutrient ion levels, and the future research could focus on the effects of 0.05 mM Fe addition on the phytoremediation efficiency for B. pilosa by pot and field experiments.

Author Contributions

S.W. (Siqi Wang): Data processing, Writing—original draft and detection; H.D.: Data curation, Formal analysis, Writing—review and editing; D.J.: Resources, cultivation and detection; S.C.: Detection and data processing. C.J.: Detection and data processing; L.S.: Validation, Writing—review and editing; L.L.: Detection and data processing; D.G.: Validation, Writing—review and editing; S.W. (Shuhe Wei): Conceptualization, Methodology, Project administration, Supervision. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Open Fund of Cultivation State Key Laboratory of Qinba Biological Resources and Ecological Environment of Shaanxi University of Technology, China (SLGPT2019KF04-02), Scientific research project of City-University co-construction of Shaanxi Province, China (SXZJ-2301, SXJ-2101), Qinba Bioremediation and Resource Development Research and Innovation Base (2022-ZC-GXYZ-0029) and the project of Foreign Experts Bureau of Shaanxi province of China, China (G2022040018L, 2022WGZJ-20, G2021041011L, G20200241015). The General Program from the Education Department of Liaoning Province (LJKMZ20220595). The Scientific Research Funds for the Innovation Team Construction Plan of Shenyang Ligong University (SYLUTD202103). The Shenyang Scientific Plan Project (21-109-3-06).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The datasets used or analyzed during the current study are available from the corresponding author on reasonable request.

Conflicts of Interest

The authors have no relevant financial or non-financial interests to disclose.

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Figure 1. The Cd2+ influx at the root surface of Bidens pilosa L. from control groups (A) and Cd treatment groups with different concentrations of Ca2+ (B), Mg2+ (C), Fe2+ (D), SO42− (E) and K+ (F). Notes: The negative values of Cd2+ net flux denote the influx from the measuring solution to the root. The means of Cd2+ influx at different distances from the root tips marked with the same lowercase letters (a–h) were not significantly (p > 0.05) different, and the means of Cd2+ influx under different treatments marked with the same capital letters (A–C) were not significantly (p > 0.05) different.
Figure 1. The Cd2+ influx at the root surface of Bidens pilosa L. from control groups (A) and Cd treatment groups with different concentrations of Ca2+ (B), Mg2+ (C), Fe2+ (D), SO42− (E) and K+ (F). Notes: The negative values of Cd2+ net flux denote the influx from the measuring solution to the root. The means of Cd2+ influx at different distances from the root tips marked with the same lowercase letters (a–h) were not significantly (p > 0.05) different, and the means of Cd2+ influx under different treatments marked with the same capital letters (A–C) were not significantly (p > 0.05) different.
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Toxics 11 00227 g002a 550Toxics 11 00227 g002b 550
Figure 2. The shoot biomass and Cd contents of Bidens pilosa L. from control groups (A) and Cd treatment groups with different concentrations of Ca2+ (B), Mg2+ (C), Fe2+ (D), SO42− (E) and K+ (F). Notes: the Cd contents were from the whole seedling of B. pilosa, the means of biomass under different treatments marked with the same lowercase letters (a–c) were not significantly (p > 0.05) different, and the means of Cd contents under different treatments marked with the same uppercase letters (A–C) were not significantly (p > 0.05) different.
Figure 2. The shoot biomass and Cd contents of Bidens pilosa L. from control groups (A) and Cd treatment groups with different concentrations of Ca2+ (B), Mg2+ (C), Fe2+ (D), SO42− (E) and K+ (F). Notes: the Cd contents were from the whole seedling of B. pilosa, the means of biomass under different treatments marked with the same lowercase letters (a–c) were not significantly (p > 0.05) different, and the means of Cd contents under different treatments marked with the same uppercase letters (A–C) were not significantly (p > 0.05) different.
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Figure 3. The concentrations of chlorophyll a and b of Bidens pilosa L. from control groups (A) and Cd treatment groups with different concentrations of Ca2+ (B), Mg2+ (C), Fe2+ (D), SO42− (E) and K+ (F). Notes: the means of chlorophyll a concentrations under different treatments marked with the same lowercase letters (a–c) were not significantly (p > 0.05) different, and the means of chlorophyll b concentrations under different treatments marked with the same uppercase letters (A–C) were not significantly (p > 0.05) different.
Figure 3. The concentrations of chlorophyll a and b of Bidens pilosa L. from control groups (A) and Cd treatment groups with different concentrations of Ca2+ (B), Mg2+ (C), Fe2+ (D), SO42− (E) and K+ (F). Notes: the means of chlorophyll a concentrations under different treatments marked with the same lowercase letters (a–c) were not significantly (p > 0.05) different, and the means of chlorophyll b concentrations under different treatments marked with the same uppercase letters (A–C) were not significantly (p > 0.05) different.
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Figure 4. The concentrations of carotenoid and root vigor of Bidens pilosa L. from control groups (A) and Cd treatment groups with different concentrations of Ca2+ (B), Mg2+ (C), Fe2+ (D), SO42− (E) and K+ (F). under Cd treatments with different nutrient ion levels. Notes: the means of carotenoid concentrations under different treatments marked with the same lowercase letters (a–c) were not significantly (p > 0.05) different, and the means of root vigor under different treatments marked with the same uppercase letters (A–C) were not significantly (p > 0.05) different.
Figure 4. The concentrations of carotenoid and root vigor of Bidens pilosa L. from control groups (A) and Cd treatment groups with different concentrations of Ca2+ (B), Mg2+ (C), Fe2+ (D), SO42− (E) and K+ (F). under Cd treatments with different nutrient ion levels. Notes: the means of carotenoid concentrations under different treatments marked with the same lowercase letters (a–c) were not significantly (p > 0.05) different, and the means of root vigor under different treatments marked with the same uppercase letters (A–C) were not significantly (p > 0.05) different.
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Table
Table 1. Treatment design of additives to Hoagland solution in pots with Bidens pilosa L.
Table 1. Treatment design of additives to Hoagland solution in pots with Bidens pilosa L.
TreatmentsTreatment Details
ControlsHoagland solution
Cd treatments aloneHoagland solution (10 μM Cd2+)
Cd treatments with Ca2+Hoagland solution (10 μM Cd2+ + 1 mM Ca2+, other ingredients unchanged)
Hoagland solution (10 μM Cd2+ + 16 mM Ca2+, other ingredients unchanged)
Cd treatments with Mg2+Hoagland solution (10 μM Cd2+ + 0.5 mM Mg2+, other ingredients unchanged)
Hoagland solution (10 μM Cd2+ + 8 mM Mg2+, other ingredients unchanged)
Cd treatments with Fe2+Hoagland solution (10 μM Cd2+ + 0.05 mM Fe2+, other ingredients unchanged)
Hoagland solution (10 μM Cd2+ + 0.5 mM Fe2+, other ingredients unchanged)
Cd treatments with SO42−Hoagland solution (10 μM Cd2+ + 0.5 mM SO42−, other ingredients unchanged)
Hoagland solution (10 μM Cd2+ + 8 mM SO42−, other ingredients unchanged)
Cd treatments with K+Hoagland solution (10 μM Cd2+ + 2 mM K+, other ingredients unchanged)
Hoagland solution (10 μM Cd2+ + 18 mM K+, other ingredients unchanged)
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MDPI and ACS Style

Wang, S.; Dai, H.; Ji, D.; Cui, S.; Jiang, C.; Skuza, L.; Li, L.; Grzebelus, D.; Wei, S. Influencing Factors of Bidens pilosa L. Hyperaccumulating Cadmium Explored by the Real-Time Uptake of Cd2+ Influx around Root Apexes under Different Exogenous Nutrient Ion Levels. Toxics 2023, 11, 227. https://doi.org/10.3390/toxics11030227

AMA Style

Wang S, Dai H, Ji D, Cui S, Jiang C, Skuza L, Li L, Grzebelus D, Wei S. Influencing Factors of Bidens pilosa L. Hyperaccumulating Cadmium Explored by the Real-Time Uptake of Cd2+ Influx around Root Apexes under Different Exogenous Nutrient Ion Levels. Toxics. 2023; 11(3):227. https://doi.org/10.3390/toxics11030227

Chicago/Turabian Style

Wang, Siqi, Huiping Dai, Dandan Ji, Shuang Cui, Chengzhi Jiang, Lidia Skuza, Lianzhen Li, Dariusz Grzebelus, and Shuhe Wei. 2023. "Influencing Factors of Bidens pilosa L. Hyperaccumulating Cadmium Explored by the Real-Time Uptake of Cd2+ Influx around Root Apexes under Different Exogenous Nutrient Ion Levels" Toxics 11, no. 3: 227. https://doi.org/10.3390/toxics11030227

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