Skip to content
BY 4.0 license Open Access Published by De Gruyter Open Access January 30, 2023

Study on arsenic speciation and redistribution mechanism in Lonicera japonica plants via synchrotron techniques

  • Jiaqi Qiao , Juntong Zhou , Congnan Peng , Xin Yuan , Li Yao , Yilin Fan , Kailin Qi , Dongliang Chen , Zhiying Guo , Xiaolong Gan , Yaxuan Sun , Xueling Dai , Guohao Wu EMAIL logo and Qing Huo EMAIL logo
From the journal Open Chemistry

Abstract

The absorption, distribution, and transport trends of organic and inorganic arsenic (As) in honesuckle (Lonicera japonica) were studied using synchrotron X-ray fluorescence spectroscopy (μ-XRF). The root, stem, and leaf samples were analyzed by μ-XRF, proving that in the presence of dimethyl arsenate acid, a small amount of As accumulated in local areas of the epidermis and cortex of roots, while most of As migrated to the upper plant through the middle vascular column. After reaching the stem, As was mainly distributed in the outer skin, indicating that the root and stem of L. japonica blocked the transport of As in the plant. In the presence of As(iii), A large amount of As accumulated in the epidermis and cortex of the root, reducing its further transport from the plant roots. Once As entered the stem of L. japonica from the root, it achieved a strong transport capacity, thus causing severe harm to plants. The element correlation analysis revealed that As in L. japonica had the strongest correlation with Cu and Zn elements, for the future research on the influence of As pollution on plants, the interference based on the above two elements can be considered.

1 Introduction

With global industrial development, growing amounts of heavy metals in solid by-products, wastewater, and smoke pollute the soil, water, and air, jeopardizing ecological safety, and biological survival [1]. Arsenic (As) is a highly toxic heavy metal, which high-concentration inorganic compounds are present is groundwater of such countries as Argentina, Bangladesh, China, Chili, Mexico, and United States [2]. The maximum allowable concentration of As in water is 0.05 mg/L, while its toxic dose for an adult human is 5–50 mg, and the lethal dose is 50–340 mg. Tobacco plants are susceptible to accumulating inorganic As from soil, while herbal drugs may accumulate As during their drying, storage, transportation, and manufacturing [3,4,5,6,7]. According to the ISO international standard “Traditional Chinese Medicine-Determination of heavy metals in herbal medicines used in Traditional Chinese Medicine” [8], the limit ratios of 3.46, 4.03, 2.91, and 1.41% for lead, As, cadmium, and mercury, respectively, were exceeded during the examined period from 2000 to 2016. Excessive content of heavy metals has become the main factor deteriorating the quality and reputation of traditional Chinese herbal drugs and hindering their global expansion [7,8]. Studies on the uptake rules, accumulation rules, and influencing factors of heavy metals in the environment by medicinal plants, as well as the distribution, morphology, and transformation mechanism of heavy metals in plants, are beneficial for the development of relevant traditional Chinese medicine plant breeding and regulation of the production of traditional Chinese medicine.

As exists in organic and organic forms. Inorganic As includes As(iii) and As(v), and organic As includes methylmalonic acid (MMA(v)), dimethyl arsenate acid (DMA(v)), and trimellitic acid (TMA(v)). Generally, inorganic As is more toxic than organic one, and As(iii) is the most toxic [9,10]. The toxicity of different speciations of As varies. To study the accumulation of As in Chinese medicinal materials, a close attention should be paid to the total amount of As and shares of different speciations of As [11].

The common As speciation detection method is inductively coupled plasma-mass spectrometry (ICP-MS), through which all six common As speciations can be detected [12]. Determination of As by hydride generation-atomic fluorescence spectrometry (HG-AFS) can only detect four As speciations, namely As(iii), As(v), MMA, and DMA, but not arsenic betaine and arsenic choline [13]. In addition, some researchers have used hydride generation-cold trap-atomic absorption spectrometry, high-performance capillary zone electrophoresis-ultraviolet detection, and other methods to study the speciations of As [14]. Numerous As intermediates co-exist in the degradation process of various compounds. In addition, there are macromolecular organic As compounds in nature. Thus, it is difficult to use traditional analytical methods such as chromatography/mass spectrometry combined with organic separation analysis methods to accurately detect As’s speciation and content changes in Chinese herbal medicines.

After years of development, synchrotron radiation (SR) has gradually become a “must-have” tool for studying metal elements’ speciation, composition characteristics, and transformation process [15]. Synchrotron X-ray fluorescence (XRF) analysis is a sensitive, rapid, and nondestructive multi-element simultaneous analysis method that can analyze the element distribution of substances and measure them in situ. The spatial distribution information of elements in tissue or organ slices can be obtained at the micron scale by scanning samples [16]. Pickering et al. conducted μ-SXRF scanning analysis on the root, leaf axis, and leaf of Pteris vittata (commonly known as the Chinese brake) and observed that arsenate As(v) was distributed in the center of the vein, while As sulfide As(SR)3 was similar to a cylindrical shell, closely surrounding the arsenate on the vein [17]. Voegelin et al. used μ-XRF and extended X-ray absorption fine structure spectra to study the distribution and morphology of As in polluted riparian soil and plant roots and revealed the distribution relationship of various elements in soil [18]. Lombi et al. applied the X-ray absorption near edge structure (XANES) technique to P. vittata leaves, which revealed that the main speciation of As was As(iii), which finding was confirmed by later studies [19]. Wu et al. used the μ-XRF and XANES techniques to assess the As distribution in rice hulls, bran, and embryos. DMA(v) was the main As speciation in rice, its share exceeding 60% of the total As, and there was a high correlation between As and Fe in soil [20].

However, to the best of the authors’ knowledge, no reports on As content and distribution in Lonicera japonica’s biological samples have been published yet. To fill this gap, the current study performed SR microarea X-ray fluorescence analysis (μ-XRF) of L. japonica (honeysuckle) plant samples. Samples were taken from the 4W1B beamline experimental station of the Beijing Synchrotron Radiation Laboratory, and the plant slices were prepared by freezing section technology. In situ analyses of the distribution characteristics and content changes of As and related multi-elements in plants’ roots, stems, and leaves were carried out by μ-XRF to study As’s absorption, accumulation, and speciation transformation.

2 Materials and methods

2.1 Reagents and instruments

Hogeland Reagent, SAKURA frozen section embedding agent, Standard substance sodium arsenate (NaHAsO4·4H2O As(v); purity ≥98.5%, Dr. Ehrenstorfer GmbH), sodium arsenite (NaAsO2, As(iii), purity ≥95.0%, Saiya Reagent), dimethyl arsenic acid (C2H6AsNaO2·3H2O, DMA, purity ≥98.0%, Beijing Beinachuanglian Institute of Biotechnology), glutathione (GSH, purity >98%), Cr metal flakes, XRF Tape, and Kapton Tape are used.

PQX-450H artificial climate chamber (China Yi Guoke (Beijing) Technology Co.); Milli-Q50 Ultrapure Water System (Millipore, USA); CM3050S cryogenic frozen slicer (Leica, Germany); FW-4 Powder Tablet Press (Tianjin Tianguang Optical Instrument Co., Ltd.); PHS-3C Precision PH Meter (Shanghai Magnetics Instruments Co., Ltd.); BCD-216YH Refrigerator (−4℃/−20℃) (Qingdao Haier Group); Premium U410 −80°C ultralow temperature refrigerator (Eppendorf, Germany); 4W1B X-ray fluorescence spectrometer (Beijing Synchrotron Radiation Source) are also used.

2.2 Experimental

2.2.1 Material processing

The test material was a 2-year-old L. japonica sapling purchased in Linyi, Shandong Province, China. First, the L. japonica plant was cultured in pollution-free soil for 2 months, and after the leaves of the L. japonica plant thrived, they were removed. Leaves were cleaned with 0.3% KMnO4, washed with deionized water three times, and placed in a constant-temperature incubator for hydroponical cultivation. L. japonica plants were cultured in 1/6 Hoagland solution for 1 week, transferred to 1/2 Hoagland solution for 1 week, and finally placed in whole Hoagland nutrient solution for 1 week. The incubator was set in a day and night mode. The incubator was ventilated, and plants were grew under the natural light intensity. 0.1 mmol/L HCl or 0.1 mmol/L NaOH was used every day to adjust the pH of the nutrient solution to approximately 5.6. The temperature was 28℃/20℃ day and night, the humidity was 40%/60% day and night, and the nutrient solution was changed every 3 days. After 3 weeks of hydroponic cultivation of L. japonica plants, different concentrations of As were added to the nutrient solution, and the nutrient solution entered a state of As stress.

The whole Hoagland nutrient solution comprised the following components: mixed reagent (mg/L): potassium sulfate 607 mg/L, ammonium dihydrogen phosphate 115 mg/L, magnesium sulfate 493 mg/L, ferric sodium EDTA 20 mg/L, ferrous sulfate 2.86 mg/L, borax 4.5 mg/L, manganese sulfate 2.13 mg/L, copper sulfate 0.05 mg/L, and zinc sulfate 0.22 mg. 1.26 g of mixed reagent was weighed, and 0.945 g of calcium nitrate was dissolved in 1 L of water, thoroughly stirred, and dissolved, producing the Hoagland solution required by plants.

2.2.2 Hydroponic experimental method

  1. Organic As DMA hydroponic experiment: taking whole Hoagland nutrient solution as the culture solution, DMA was added to the nutrient solution at a concentration of 70 mg/L; sampling and analysis were performed after 10 days of treatment (three plants per replication, with three replications per treatment).

  2. Inorganic As sodium arsenite (NaAsO2, As(iii)) hydroponic experiment: The whole Hoagland nutrient solution was used as the culture solution, and sodium arsenite (As(iii)) was added to the nutrient solution at concentrations of 20, 30, and 50 mg/L. After 10 days of treatment, the samples were analyzed. Three plants were used per replication, with three replications per treatment.

  3. Control group hydroponic experiment: The whole Hoagland nutrient solution was used as the culture solution. L. japonica plants were cultured in the culture solution for ten days before sampling and analysis. Three plants were used per replication, with three replications per treatment.

As(v) can be easily converted into As(iii) in plants, and As(iii) is highly toxic, so inorganic As in this study was As(iii); organic As included MMA(v), DMA(v), and TMA(v). Among them, DMA was the most toxic. Our previous study on honeysuckle revealed a high ratio of DMA [21], which was chosen as organic As in this study.

2.2.3 μ-XRF study on the distribution characteristics of multi-elements in the roots, stems, and leaves of L. japonica

The experiment included the control plant, 70 mg/L DMA, and 30 mg/L As(iii) stress groups. When the samples were collected, all plants were soaked in 20 mM EDTA-Na2 solution for 20 min to remove the As adsorbed on the surface of the plants and washed with ultrapure water three times. L. japonica plants were split into three parts: root, stem, and leaf. The tissues of each plant were cut into 30 μm thick tissue slices at −20°C using a freezing microtome and then placed on XRF tape for immediate experiments.

The distribution characteristics of As(iii), DMA, and other elements in the roots, stems, and leaves of L. japonica were studied at the 4W1B beamline station of X-ray fluorescence analysis in the synchrotron radiation facility (BSRF) of the Institute of High Energy Physics, Chinese Academy of Sciences in Beijing, China. The scanning time of a single spot was in the range of 1–3 s according to the content of each tissue of the plant. The spot size was adjusted according to the tissue size, and the scanning energy range was 11.81–11.91 keV. The monochromatic incident X-ray energy was produced a W/B4C double grating multilayer monochromator, and the energy was focused on the 50 μm diameter beam by a capillary lens. The angle between the projected beam and the sample was set at 45°. The sample stage traveled 50 μm in the X direction and 50 μm in the Y direction. The sample stage could simultaneously collect the fluorescence intensity of Ca, Mn, Fe, Zn, Cu, and As, and the emission intensity was proportional to the element intensity. The fluorescence data were processed by PyMCA 5.5.0-win64. The Origin2019b software of the Originlab Company, USA, was used to generate two-dimensional distribution maps of As elements

3 Results and discussion

3.1 Distribution of different species of As in the roots of L. japonica

To study the spatial distribution of As in medicinal plants of L. japonica, the plants’ roots, stems, and leaves were scanned by the X-ray fluorescence method. The integrated intensity of each element was calculated according to the spectrum and was normalized to the intensity of the Compton scattering peak. The distributions of As, Ca, Mn, Fe, Zn, and Cu elements in the root and stem leaves obtained by scanning are shown in Figures 13. The color scale from red to blue represents the highest to lowest XRF intensity of standardized elements, that is, the concentration of elements from high to low. Figure 1 shows the distribution of As, Ca, Cu, Fe, Mn, and Zn μ-XRF elements in the root of L. japonica. The epidermis, cortex, and vascular column are from outside to inside. Among them, the vascular column is the longitudinal transport system of the root.

Figure 1 
                  As and other related elements in the root section of honeysuckle μ-XRF distribution. A: 70 mg/L DMA group, B: control group, C: 30 mg/L As(iii) group.
Figure 1

As and other related elements in the root section of honeysuckle μ-XRF distribution. A: 70 mg/L DMA group, B: control group, C: 30 mg/L As(iii) group.

Figure 2 
                  Honeysuckle stem As and other related element μ-XRF distribution. (A) 70 mg/L DMA group, (B) control group, and (C) 30 mg/L As(iii) group.
Figure 2

Honeysuckle stem As and other related element μ-XRF distribution. (A) 70 mg/L DMA group, (B) control group, and (C) 30 mg/L As(iii) group.

Figure 3 
                  The μ-XRF distribution of As and other related elements in honeysuckle leaves. (A) 70 mg/L DMA group, (B) control group, and (C) 30 mg/L As(iii) group.
Figure 3

The μ-XRF distribution of As and other related elements in honeysuckle leaves. (A) 70 mg/L DMA group, (B) control group, and (C) 30 mg/L As(iii) group.

Honeysuckle is a Dicotyledones; the primary structure of the Dicotyledones consists of the epidermis, cortex, and vascular column. The epidermis is the outermost cell layer of the stem, small and closely arranged with epidermal hairs and stomatal apparatus; the cortex is inside the epidermis and outside the vascular column and consists of layers of thick-angular and parenchyma tissue; the vascular column is the inner part of the cortex and consists of vascular bundles, pith rays, and pith. Compared with the microscopic image of the stem [22], the epidermis, cortex, and vascular column can be roughly distinguished from the XRF image.

It can be seen from the control group in Figure 1b that As in the root of L. japonica mainly accumulated in the central vascular column, while its contents in the epidermis and cortex were relatively low. Figure 1a shows that As accumulated in the epidermis and cortex was higher than that in the vascular-cylinder zone in the middle section, As was concentrated in certain zones of the cortex annular ring in the presence of DMA. According to Figure 1c, the content of As in vascular columns was lower than in the epidermis and cortex in the presence of sodium arsenite (NaAsO2), which might be due to the more apparent toxic effect of As(iii) on plants. Most As accumulated in the epidermis and cortex. Its accumulation in vascular columns was slight, making it difficult for As to migrate from L. japonica roots through vascular columns and thus minimizing its content.

According to Figure 1, the distribution of Cu was quite similar to that of As under As stress. The correlation analysis data in Table 1 prove a significant positive correlation between As and Ca, Mn, Fe, Cu, and Zn at a 0.05 level.

Table 1

Pearson coefficient (R) of correlation between As and other elements in honeysuckle roots

As Ca Mn Fe Cu Zn
DMA70 0.39782* 0.56329* 0.41786* 0.87505* 0.18203*
Control group 0.22473* 0.22473* 0.029 0.767* 0.59757*
As(iii)30 0.5908* 0.59513* 0.16369* 0.90664* 0.85296*

*Note: The correlation was significant at the 0.05 level.

Compared with the control group, there was no substantial change in the correlation between the As stress group elements. Cu had the highest correlation with As, indicating that the absorption among elements might be similar for samples of the same honeysuckle plant. By analyzing the effects of As stress on other nutrient elements, we found that the distribution of Ca and Cu in roots was not affected by organic and inorganic As stresses, while the accumulation of Cu in the root cortex was promoted by inorganic As stress. The distribution of Fe and Mn in roots changed significantly under the organic and inorganic As stresses, with slight accumulations in the epidermis and cortex. At the same time, the vascular column in the center exhibited no distribution of Fe and Mn. In particular, the distribution of Mn was found in the control group’s epidermis, cortex, and vascular column. The As(iii) stress group images show that only a small area of the epidermis had Mn distribution. The distribution of Zn in roots was affected by organic and inorganic stresses, and the distribution migrated from the central vascular column to the peripheral epidermis and cortex.

3.2 Distribution of different speciation of As in the stem of L. japonica

Figure 2 shows the distribution of As, Ca, Cu, Fe, Mn, and Zn μ-XRF in the stem of L. japonica. The middle of the stem was hollow. The outer skin, cambium, xylem, and pith were from the outside to the inside. The stem could not transfer the nutrients absorbed by the root system to the aboveground part. According to Figure 2b, in the control group, As was mainly distributed in the cambium and xylem rather than the central pith, and its accumulation in the cuticle was less than that in the cambium and xylem. According to Figure 2a, the content of As in the cuticle exceeded that in the cambium and xylem, there was no As distribution in the central pith in the presence of DMA. According to Figure 2c, the As(iii) group differed from the DMA group in terms of the As distribution. There was a high concentration of As in the xylem; As contents in the cambium and xylem exceeded those in the outer skin in the presence of sodium arsenite (NaAsO2). As the transport tissue of plants, the xylem is responsible for transporting the water absorbed by roots and the ions dissolved in water, indicating that the stem of L. japonica had a stronger As transmission capacity.

According to the element correlation analysis results tabulated in Table 2, As exhibited a significant positive correlation with Ca, Mn, Fe, Cu, and Zn at a 0.05 level, with the strongest correlation with Zn. In the control group, five elements were mainly distributed in the outer skin and cambium of the stem, and the cambium had a high aggregation concentration. The distribution of Fe in stems was not affected by organic and inorganic As stresses. The distribution areas of Cu, Mn, Zn, and Ca under organic As stress did not change, being mainly concentrated in the outer skin and cambium. They had zero distribution in the pith of the center, and their accumulation decreased slightly. After inorganic As stress, the accumulation of the above four elements in the stem increased. In addition to the outer skin and cambium, contents of these four elements were significant in the inner xylem.

Table 2

Pearson coefficient (R) of correlation between As and other elements in honeysuckle stems

As Ca Mn Fe Cu Zn
DMA70 0.47147* 0.58328* 0.51529* 0.53559* 0.59277*
Control group 0.5134* 0.62562* 0.457* 0.81593* 0.61086*
As(iii)30 0.6455* 0.69642* 0.21007* 0.14029* 0.8303*

*Note: The correlation was significant at a 0.05 level.

3.3 Distribution of different speciation of As in the leaves of L. japonica

The observed distribution of elements in L. japonica leaves revealed the protective mechanism of As tolerance of this plant. As shown in Figure 3, As was mainly distributed along the lateral and middle veins of L. japonica leaves. As was transported through the rhizome and stored in the veins. Since veins were primarily composed of vascular bundle (the supporting structure of leaves), they contained no chlorophyll and did not participate in photosynthesis.

In the leaves subjected to organic As stress, as shown in Figure 3a, a high concentration of As accumulated in the middle veins. According to Figure 3c, As accumulated in the veins, which diffusion into the mesophyll (for photosynthesis) would cause significant harm to the plant. To avoid this, the plant accumulated As in the lateral veins of its leaves in the presence of sodium arsenite (NaAsO2). Noteworthy is that relevant studies on plant hyperaccumulators, i.e., plants capable of extracting metals from the soil and accumulating them to extraordinary concentrations in aboveground tissues, revealed similar protective mechanisms. Thus, Toaspern et al. reported that the leaves of the nonhyperaccumulator Thlaspi arvense L. had the poor capacity to transport zinc from veins to mesophyll tissue, while the hyperaccumulator Thlaspi caerulescens had a relatively strong zinc transportation capacity [23]. The characteristics of As accumulation in vein vascular bundles have also been reported in a study of the As hyperaccumulator P. vittata [24]. This distribution characteristic of As was beneficial in reducing the toxic effect of As on leaves, which might be the protective mechanism of honeysuckle against As toxicity.

The performed element correlation analysis provided some information on the absorption and storage relationship between elements. As shown in Figure 3, Cu, Mn, and Zn were mainly distributed in the vein, similar to the distribution characteristics of As. According to the correlation analysis of As and other elements in L. japonica leaves (see Table 3), Ca, Cu, Mn, and Zn had a significant positive correlation with As at a 0.05 level.

Table 3

Pearson coefficient (R) of correlation between As and other elements in honeysuckle leaf samples

As Ca Mn Fe Cu Zn
DMA70 0.37903* 0.38035* −0.036 0.49825* 0.25683*
Control group 0.69865* 0.76875* 0.69313* 0.84361* 0.8368*
As(iii)30 0.8457* 0.61999* 0.77104* 0.8941* 0.87616*

*Note: The correlation was significant at a 0.05 level.

Under organic As (DMA) stress, As did not correlate with Fe. Overall, there was a high correlation between Cu and As in the leaves of L. japonica. Compared with the control group, the distribution of five elements in leaves only slightly changed under inorganic and organic As stresses. Under organic As stress, the accumulation of Mn, Ca, and especially Cu in leaves increased, while those of Fe and Zn decreased, with a small accumulation of Fe at the tip of leaves. Under inorganic As stress, the accumulation of Cu in leaves increased, while contents of the other four elements, especially Fe, in leaves dropped.

Similar findings have been earlier reported for other plants. Thus, Chen et al. studied correlations between As and K, Ca, Mn, Fe, Cu, and Zn in the petiole, midvein, and feather leaves of Pteris nervosa, as a typical As-enriched plant. All these elements exhibited strong positive correlations at a level of 0.01 [25]. In contrast, Tu and Ma examined the As hyperaccumulator P. vittata L. and reported that As only correlated with Fe in the mature leaves, and there was a significant negative correlation between As and Mn (R = −0.795), while in the young leaves, Mn did not correlate with As [26]. Concerning As accumulation in rice, Hossain et al. revealed no correlation between As and Fe in rice grains but reported a significant correlation between As and Fe in rice leaves [27].

4 Conclusion

This study analyzed the absorption and transport characteristics of organic and inorganic As in L. japonica using synchrotron X-ray fluorescence spectroscopy (μ-XRF), revealing the following As transportation and distribution patterns.

  1. L. japonica plants absorbed As through roots, mainly distributed in the epidermis and cortex of roots and the central vascular column. Then, As was transmitted upward to stems through the central vascular column. The stems played the role of conduction between roots and leaves. In the presence of DMA, As was distributed evenly in the roots’ epidermis, cortex, and middle vascular column. Except for a small amount of As accumulated in the epidermis and cortex, most of As migrated to the upper plants through the middle vascular column. After reaching the stem, As became mainly distributed in the outer skin, and its content exceeded that in the cambium and xylem, indicating that the root and stem of L. japonica blocked the transport of As in the plant.

  2. Inorganic As(iii) absorption and transportation trends differed from those of organic As DMA. In the presence of As(iii), As accumulated in the epidermis and cortex in large amounts, minimizing the accumulation in the central vascular column and reducing the transportation and absorption of As by plant roots. In the stem, as the transport tissue of plants, xylem exhibited a considerable accumulation of As, implying that As had a strong transmission capacity once it entered the stem of L. japonica from the root, thus causing serious harm to the plant. The analysis of L. japonica leaves revealed that the leaves of L. japonica had a strong capacity to transfer As to the lateral vein, ensuring plant’s resistance to As toxicity and being of great significance for leaf accumulation and tolerance to As.

  3. The performed element correlation analysis revealed the following absorption and storage relationship between heavy metal elements. There was a strong correlation between As and Cu in the roots and leaves of L. japonica, and the correlation between As and Zn in the stems of L. japonica was the strongest. For future research on the influence of As pollution on plants, interference based on the above two elements can be considered.

Acknowledgment

The authors appreciate the technical assistance and guidance of Mr. Xu Bai, Institute of High Energy Physics, Chinese Academy of Sciences, Beijing, China.

  1. Funding information: This research was financially supported by the National Natural Science Foundation of China (Grant No. 11975048) and Beijing Union University Graduate Program (Grant No. YZ2020K001).

  2. Author contributions: Jiaqi Qiao and Juntong Zhou: writing – original draft, Congnan Peng, Xin Yuan, and Li Yao: investigate, Yilin Fan and Kailin Qi: validation, Dongliang Chen, Zhiying Guo, and Xiaolong Gan: supervision, Yaxuan Sun and Xueling Dai: conceptualization, and Guohao Wu and Qing Huo: project management.

  3. Conflict of interest: The authors state no conflict of interest.

  4. Ethical approval: The conducted research is not related to either human or animal use.

  5. Data availability statement: The data used to support the findings of this study are available from the corresponding author upon request.

References

[1] Zhang W, Qi LJ, Ning JY, Gao S, Li GJ. Health hazard assessment of arsenic. J Toxicol. 2021;35(5):367–72 + 378.Search in Google Scholar

[2] Stargardt T, Gonder-Frederick L, Krobot KJ, Alexander CM. Scientific opinion on arsenic in food EFSA panel on contaminants in the food chain (CONTAM). EFSA J. 2009;7(10):1351.10.2903/j.efsa.2009.1351Search in Google Scholar

[3] Ibrar M, Muhammad N, Shah W, Ullah B. Evaluation of trace and toxic heavy metals in selected crude drugs used in khyber Pukhtonkhawa, Pakistan. Pak J Botany. 2013;45(1):141–4.Search in Google Scholar

[4] Chan CS, Guo L, Shih MC. Statistic analysis of heavy metal residues in Chinese crude drugs with the international standards of Chinese Medicine-Chinese herbal medicine heavy metal limit. Sci Technol Rev. 2017;35(11):91–8. 10.1023/A:1010602031070.Search in Google Scholar

[5] Han XL, Zhang XB, Guo LP. Statistical analysis of residues of heavy metals in Chinese crude drugs. China J Chin Mater Medica. 2008;33(18):2041–8. 10.3724/SP.J.1011.2008.00534.Search in Google Scholar

[6] Tang YJ. Overview of research on heavy metals in traditional Chinese medicine. Jiangxi Univ Trad Chin Med. 2007;19(6):88–90. 10.3724/SP.J.1011.2008.00534.Search in Google Scholar

[7] Palchetti I, Mascini M, Minunni M, Bilia AR, Vincieri FF. Disposable electrochemical sensor for rapid determination of heavy metals in herbal drugs. J Pharm Biomed Anal. 2003;32(2):251–6. 10.1016/S0731-7085(03)00132-8.Search in Google Scholar

[8] International Organization for Standardization. ISO 18664: 2015 Traditional Chinese Medicine-Determination of heavy metals in herbal medicines used in Traditional Chinese Medicine; 2017. https://www.iso.org/standard/63150.html.Search in Google Scholar

[9] Meng ZY. Study on the safety of different valence arsenic in aquatic products [dissertation]. Qingdao (MI): Ocean University of China, 2005.Search in Google Scholar

[10] Yang F, Xie S, Wei C, Liu J, Zhang H, Chen T, et al. Arsenic characteristics in the terrestrial environment in the vicinity of the Shimen realgar mine, China. Sci Total Environ. 2018;626(jun.1):77–86.10.1016/j.scitotenv.2018.01.079Search in Google Scholar PubMed

[11] Luo JY, Liu H, Gu SY, Wu JJ, Yang MH. Analysis and limitation standard of mercury and arsenic elements residues in 31 animal drugs. Chin J Pharm. 2018;53(11):1879–86.Search in Google Scholar

[12] Hao CL, Zhao L, Zhuang ZX. Simultaneous analysis of various forms of arsenic in Chinese medicinal materials by HPLC-ICP/MS. Anal Lab. 2011;30(6):90–3.Search in Google Scholar

[13] Mao HL, Wu QX, Yang ZB, Luo Q. Determination of the content of arsenic and mercury in common traditional Chinese herbs in Qiannan by the method of hydride generation-atomic fluorescence spectrometer. J Qiannan Norm Coll Nationalities. 2009;29(6):7–10.Search in Google Scholar

[14] Zhang Qli, Wu Q, Xie YY, Shen LZ, Fan MW, Wang YM, et al. Arsenic in Liushen pills and realgar morphological distribution research. Chin J Pharm Sci. 2011;46(6):701–6.Search in Google Scholar

[15] Yang CZ, Cheng GF, Huang YH. Basic knowledge of synchrotron radiation lecture (No.1 principle, construction and characters of synchrotron radiation source). Phys Test Chem Anal Part A Phys Test. 2008;44(1):28–32.Search in Google Scholar

[16] Yamaguchi N, Ishikawa S, Abe T, Baba K, Arao T, Terada Y. Role of the node in controlling traffic of cadmium, zinc, and manganese in ricer. J Exp Botany. 2012;63(7):2729–37.10.1093/jxb/err455Search in Google Scholar PubMed PubMed Central

[17] Pickering IJ, Gumaelius L, Harris HH, Prince RC, Hirsch G, Banks JA, et al. Localizing the biochemical transformations of arsenate in a hyperaccumulating fern. Environ Sci Technol. 2006;40(16):5010–4.10.1021/es052559aSearch in Google Scholar PubMed

[18] Voegelin A, Weber F-A, Kretzschmar R. Distribution and speciation of arsenic around roots in a contaminated riparian floodplain soil: Micro-XRF element mapping and EXAFS spectroscopy. Geochim Cosmochim Acta. 2007;71:5804–20.10.1016/j.gca.2007.05.030Search in Google Scholar

[19] Lombi E, Zhao FJ, Fuhrmann M, Ma LQ, McGrath SP. Arsenic distribution and speciation in the fronds of the hyperaccumulator Pteris vittata. N Phytol. 2002 Nov;156(2):195–203.10.1046/j.1469-8137.2002.00512.xSearch in Google Scholar PubMed

[20] Wu T-L, Cui X-D, Cui P-X, Ata-Ul-Karim ST, Sun Q, Liu C, et al. Speciation and location of arsenic and antimony in rice samples around antimony mining area. Environ Pollut. 2019;252(Sep. Pt. B):1439–47.10.1016/j.envpol.2019.06.083Search in Google Scholar PubMed

[21] Peng C, Zhou J, Sun Y, Yin H, Chen Y, Yao L, et al. Study on the speciation of arsenic in the genuine medicinal material honeysuckle. Open Chem. 2021;19:1288–95. 10.1515/chem-2021-0120.Search in Google Scholar

[22] Qiang S, Ren HY, Hu JL, Shen XS. Phytology. 2nd edn. Beijing: Higher Education Press; 2017.Search in Google Scholar

[23] Toaspern M, Lasat M, Kochian L, Smolenski K, Bilderback D, Fontes E, et al. X-ray imaging of zinc accumulation in bioremediators. Cornell High Energy Synchrotron Source (CHESS) Newsletter. 2000;44–5.Search in Google Scholar

[24] Kitajima N, Kashiwabara T, Fukuda N, Endo S, Hokura A, Terada Y, et al. Observation of arsenic transfer in leaf tissue of hyperaccumulator fern by utilizing synchrotron radiation micro-XRF imaging. Chem Lett. 2008;37(1):32–3. 10.1246/cl.2008.32.Search in Google Scholar

[25] Chen TB, Huang ZG, Huang YY, Xie H, Liao XY. Cellular distribution of arsenic and other elements in hyperaccumulator Pteris nervosa and their relations to arsenic accumulation. Chin Sci Bull. 2003;48(15):1586–91. 10.1007/BF03183966.Search in Google Scholar

[26] Tu C, Ma LQ. Effects of arsenic on concentration and distribution of nutrients in the fronds of the arsenic hyperaccumulator Pteris vittata L. Environ Pollut. 2005;135(2):333–40. 10.1016/j.envpol.2004.03.026.Search in Google Scholar PubMed

[27] Hossain MB, Jahiruddin M, Panaullah GM, Loeppert RH, Islam MR, Duxbury JM Spatial variability of arsenic concentration in soils and plants, and its relationship with iron, manganese and phosphorus. Environ Pollut. 2008;156(3):739–44. 10.1016/j.envpol.2008.06.015.Search in Google Scholar PubMed

Received: 2022-09-01
Revised: 2023-01-04
Accepted: 2023-01-09
Published Online: 2023-01-30

© 2023 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

Downloaded on 24.2.2024 from https://www.degruyter.com/document/doi/10.1515/chem-2022-0278/html
Scroll to top button