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Article

Metal Accumulation and Tolerance in Artemisia indica var. maximowiczii (Nakai) H. Hara. and Fallopia sachalinensis (F.Schmidt) Ronse Decr., a Naturally Growing Plant Species at Mine Site

by
Xingyan Lu
1,
Keiko Yamaji
1,*,
Toshikatsu Haruma
2,3,
Mitsuki Yachi
1,
Kohei Doyama
1 and
Shingo Tomiyama
3
1
Graduate School of Life and Environmental Sciences, University of Tsukuba, 1-1-1, Tennodai, Tsukuba 305-8587, Japan
2
Advanced Science Research Center, Japan Atomic Energy Agency, 2-4, Shirakata, Tokai, Naka, Ibaraki 319-1195, Japan
3
Division of Sustainable Resources Engineering, Faculty of Engineering, Hokkaido University, Sapporo 060-8628, Japan
*
Author to whom correspondence should be addressed.
Minerals 2021, 11(8), 806; https://doi.org/10.3390/min11080806
Submission received: 27 May 2021 / Revised: 15 July 2021 / Accepted: 23 July 2021 / Published: 26 July 2021
(This article belongs to the Special Issue Potentially Toxic Elements in Soils Affected by Metal Mining and Processing)
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Abstract

:
For growing plants at mine sites, plant species that accumulate metals in tissues and are tolerant to high metal concentrations should be selected from the perspective of phytostabilization. However, the eco-chemical or elemental information of the plant species at the mine sites is limited. The purpose of this study was to identify plants that can adapt to natural growth at mine sites, via: (1) vegetation survey, (2) elemental analysis in soil and plants, and (3) detoxicant detection in plant cells. Our vegetation survey indicated that plants growing at our study site are consistent with plant species confirmed at other mine sites in previous reports. A. indica var. maximowiczii and F. sachalinensis, present at the mine site, highly accumulated Fe, Al, and Cu in the roots, indicating their metal tolerance. Furthermore, A. indica var. maximowiczii produced detoxicants such as chlorogenic acid and 3,5-dicaffeoylquinic acid in the roots, which exhibited high antioxidative activity that would play an important role in metal tolerance in A. indica var. maximowiczii. This study will be effective in providing fundamental information on phytostabilization at mine sites.

1. Introduction

During Japan’s period of rapid economic growth after World War II, many mines were operating to refine metals from ores; nowadays, most mines are closed. At several areas in mine sites, the soil still contains high concentrations of metals, showing acidity; therefore, plants cannot grow easily due to high concentrations of bioavailable metals, which can damage plant growth [1]. In order to grow plants at mine sites, it would be beneficial to consider “phytostabilization”, which is a type of phytoremediation method that uses plants [2,3,4]. For phytostabilization, the following plant characteristics would be useful: plants that are capable of accumulating metals in the roots or the rhizosphere, and do not cause soil run off from the mine sites [3,5]. Therefore, plant species that can accumulate metals in the tissues and tolerate high concentrations of metals should be selected; however, there is limited eco-chemical and elemental information on the plant species suitable for phytostabilization at mine sites.
Apparently, plants that naturally grow on soil concentrated with metal have evolved their diverse metal-tolerant abilities [6,7]. Generally, metal tolerance mechanisms in plants are explained as follows [8]: (a) inhibition of metal ions entry into the cell by binding to the cell wall, (b) reduction in metal ions across the plasma membrane, (c) production of phyto-chelatins, organic acids, and amino acids to chelate metals in the cytosol; (d) sequestration of metal-chelating complex into the vacuole; and (e) active exclusion of metal ions from the cell. Recently, several studies have emphasized that excess heavy metals cause oxidative injury in plants due to free radicals, thereby stimulating antioxidant defense of plants via antioxidant chemicals and enzymes, such as ascorbate, carotenoids, glutathione, superoxide dismutase, and catalases [9,10,11]. Therefore, it is important to identify the metal tolerance of plant species growing naturally at mine sites for phytostabilization.
The purpose of this study was to confirm plants that can adapt to natural growth at mine sites from the viewpoint of ecology in combination with phytochemistry via: (1) vegetation survey, (2) elemental analysis in soils and plants, and (3) detoxicant detection in plant cells. Based on the results of preliminary elemental analysis in plants, we selected Artemisia indica var. maximowiczii, and Fallopia sachalinensis as the target plants. Moreover, according to the results of elemental analysis, we selected A. indica var. maximowiczii to analyze the detoxicants in its roots. In addition, we discuss the importance of A. indica var. maximowiczii, and its effectiveness in phytostabilization at mine sites.

2. Materials and Methods

2.1. Study Site and Vegetation Survey

Our study site was located at a gold, silver, and copper mine, an abandoned area after ore mining in Akita Prefecture, in the northern part of Japan. The study site (north–south: 15 m, east–west: 20 m) is located at a flat area in an abandoned concentrator including an old chimney, which is surrounded by several small mountains (Figure 1). Several plant species grow naturally. In July 2020, a vegetation survey was conducted using the line transect method. Three lines 1, 2, and 3 were set up, considering the micro-topographical differences; therefore, each length differed. Line 1 (11 m in length) and line 2 (12 m in length) were separately set up in the same horizontal area near an abandoned chimney (the space between the lines was 5 m), and line 3 (15 m in length) was set up along a brook, showing acidity. There were old artifacts, such as steps in the middle of the study site, and the brook flows from the east to the west. Along each line, the plant cover of each species in a quadrat (1 m × 1 m) was recorded. The number of quadrats in lines 1, 2, and 3 were 11, 12, and 15, respectively. The average plant cover rates of species detected in each line were calculated.

2.2. Sampling and Analysis of Root-Zone Soil and Plant Tissues and Calculations of Translocation Factor and Bioconcentration Factor

According to the vegetation survey results and preliminary analysis of element concentrations in five plant species (Miscanthus sinensis, Artemisia indica var. maximowiczii, Fallopia sachalinensis, Pinus densiflora, and Trifolium repens) (unpublished data), we selected F. sachalinensis and A. indica var. maximowiczii for further analyses, because F. sachalinensis exhibited a high cover rate at the study site, and A. indica var. maximowiczii accumulated high concentrations of Al, Fe, and Pb in the tissues. In July 2020, which is the the best growing season for the plants at our study site, 5 individuals of F. sachalinensis were collected near lines 1 and 2, and 5 individuals of A. indica var. maximowiczii were sampled near line 3 in the study area; the numbers of plants collected from mine sites were decided according to [12,13]. We collected our plant species out of the vegetation survey area because we will continue to observe the vegetation in a future study. Simultaneously, root-zone soil was collected. The root-zone soil for F. sachalinensis was collected from an area of 200 mm × 200 mm × 100 mm deep, and for A. indica var. maximowiczii, root-zone soil was collected from an area of 100 mm × 100 mm × 50 mm deep.
After the confirmation of damages in plant tissues caused by high concentrations of metals [14,15], the plant roots and root-zone soil were carefully separated, and the root-zone soil was air-dried under the shade at room temperature (23–25 °C). The air-dried soil was passed through a 2 mm sieve. The soil pH (H2O) was determined using a pH meter (F-71, HORIBA, Kyoto, Japan) with a water to soil ratio of 2.5:1. The air-dried root-zone soil was acid-digested using concentrated perchloric and nitric acids (HClO4-HNO3) in a volume ratio of 4:1, and the total concentrations of elements (Al, Fe, Cu, Zn, Pb, and Cd) in the root-zone soil were measured using inductively coupled plasma optical emission spectroscopy (ICP-OES; Agilent 5100, Agilent Technologies, Santa Clara, CA, USA).
The plants were carefully washed with tap water followed by Millipore water. A. indica var. maximowiczii (5 individuals) was divided into three parts: roots, stems, and leaves, and F. sachalinensis (5 individuals) was separated into four parts: roots, rhizomes, stems, and leaves. The cleaned plant tissues were dried at 80 °C for 48 h and each plant tissue was ground to a powder using an electric mill (IFM-650D, Iwatani, Tokyo, Japan), and the plant powder was re-dried at 80 °C overnight before digestion. The dried plant powder was weighed and pyrolyzed using concentrated HNO3. The concentrations of elements (Al, Fe, Cu, Zn, Pb, and Cd) in each plant tissue were measured using ICP-OES. The calibration curve for quantification was prepared using a series of corresponding metal standards at concentrations ranging from 0.03 mg/L to 4.00 mg/L. The results of the 5 replications were averaged, and standard errors (SEs) were calculated.
We calculated translocation factors (TFs) and bioconcentration factors (BCFs) using elements concentrations in each plant tissue and in root-zone soil collected from each plant individual via each formula according to [5,16] as follows;
TF = Elemental   concentration   of   stems   or   leaves   ( mg   kg − 1 ) Elemental   concentration   of   roots   ( mg   kg − 1 )
  BCF   = Elemental   concentration   of   particular   plant   organs   ( mg   kg − 1 )   Total   elemental   concentration   in   soil   ( mg   kg − 1 )
The results of the 5 replications were averaged, and standard errors (SEs) were calculated.

2.3. Analysis of Phenolic Compounds in Roots of A. indica var. maximowiczii

Fresh roots of A. indica var. maximowiczii were used for phenolic analyses. The fresh roots were weighed and cut into several small sections in a methanol solution for extraction of phenolic compounds. Samples were extracted for 5 d in the dark at room temperature (23–25 °C). The root extract solution was filtered and concentrated in vacuo at 35–40 °C. The concentrated sample was dissolved in 1 mL of 50% methanol and analyzed using a high-performance liquid chromatography (HPLC; Prominence UFLC series, Shimadzu, Kyoto, Japan), and spectral characteristics were analyzed using a diode array detector (DAD; SPD-M20A, Shimadzu, Kyoto, Japan). The gradient eluent solvents used were methanol, and 1.5% tetrahydrofuran and 0.25% phosphoric acid in Millipore water. The HPLC conditions were as described by Yamaji and Ichihara [17]. For the identification of chemicals in the root extracts, the spectral characteristics from 220 to 400 nm, and the retention times of chlorogenic acid (MP Biomedicals LLC., Santa Ana, CA, USA) and 3,5-dicaffeoylquinic acid (Cayman Chemical Company, Ann Arbor, CA, USA) were compared with those of the peaks in the root extracts. Further identification was performed using a liquid chromatograph-mass spectrometer (LCMS-2020; Shimadzu, Kyoto, Japan) equipped with an electrospray ionization (ESI) source. The conditions for mass detection were as follows: total ion counting (TIC) in the negative mode, 100–1000 m/z; nebulizer gas (N2), 1.5 L/min; drying gas, 15 L/min; interface voltage, −4.5 kV; interface temperature, 350 °C; dissolving line (DL) temperature, 200 °C; and heat block temperature, 200 °C. The MS spectra of the target peaks in the root extracts were compared with those of the standard chemicals as described above.
For quantification of chemicals, standard curves were prepared as follows: chlorogenic acid (25, 50, 100, 200, and 400 μg in 1 mL of 50% methanol) and 3,5-dicaffeoylquinic acid (50, 100, 200, and 400 μg in 1 mL of 50% methanol), were analyzed thrice per concentration at 320 nm using HPLC-DAD as described above, and the values were averaged. The quantification results of the root extracts of the five species were averaged, and SEs were calculated.

2.4. Statistical Analysis

The results were analyzed using SPSS Statistics software (ver. 25.0, IBM, Armonk, NY, USA). The differences between the concentrations of elements (Al, Fe, Zn, Cu, and Pb) in each plant tissue were evaluated by a one-factorial analysis of variance (one-factorial ANOVA) with the non-parametric Scheffé post hoc test. The differences in TFs or BCFs between plant species were evaluated by Student’s t-test. Differences were considered significant at p < 0.05.

3. Results

3.1. The Vegetation Survey

The results are summarized in Table 1. The average cover rates of M. sinensis and T. repens were high (over 20% in line 1), followed by F. sachalinensis (6.0% cover rate). In line 2, P. densiflora and M. sinensis exhibited high cover rates at 20.0% and 14.3%, respectively, and F. sachalinensis presented the fourth highest cover at 3.3%. In line 3, near a brook, Phragmites australis was the dominant species with a 10% cover rate. A. indica var. maximowiczii growing at the study site, revealed a similar cover rate in lines 1 and 3, with 3.9% and 4.7%, respectively.

3.2. pH and Total Element Concentrations in Root-Zone Soil

The pH (H2O) values of root-zone soil were 7.51 ± 0.15 and 6.56 ± 0.43 for F. sachalinensis and A. indica var. maximowiczii, respectively. The total concentrations of elements in the root-zone soils are listed in Table 2. The data of total Cd concentrations in root-zone soil were not shown in the Table 2 because total Cd concentrations were under the detection limit. Compared to the levels in general soil [8], the total concentrations of Fe in the root-zone soil of F. sachalinensis were higher. In addition, both F. sachalinensis and A. indica var. maximowiczii root-zone soils contained much higher concentrations of Zn, Cu, and Pb compared to the levels in general soil.

3.3. Element Concentrations in the Target Plant Tissues

Compared to the non-toxicity concentration levels in plants [1,19] (Al, around 200 mg/kg dry weight (DW); Fe, less than 229 mg/kg DW; Cu, less than 20 mg/kg DW), F. sachalinensis and A. indica var. maximowiczii accumulated high concentrations of Al, Fe, and Cu in the roots (Figure 2). The data of Cd concentrations in plant tissues are not shown in Figure 2 because they were under the detection limit. Plant tissues were not damaged due to the toxicity caused by high concentrations of metals; damages caused by metal toxicity, such as chlorosis of leaves and necrosis of roots [14,15], were not observed.

3.4. Translocation Factors (TFs) and Bioconcentration Factors (BCFs)

The results are listed in Table 3 and Table 4. Metals TFs and BCFs in A. indica var. maximowiczii and F. sachalinensis were lower than 1, except for leaves/roots TF of Zn in F. sachalinensis (Table 3) and Zn BCF of roots in A. indica var. maximowiczii (Table 4). In addition, leaves/roots TF of Cu in F. sachalinensis was significantly higher than those in A. indica var. maximowiczii. For Zn, stems/roots TF, and BCFs of roots and leaves in A. indica var. maximowiczii were higher than those in F. sachalinensis. On the contrary, Al BCF in F. sachalinensis was higher than A. indica var. maximowiczii.

3.5. Phenolic Compounds in the Roots of A. indica var. maximowiczii

Based on the HPLC-DAD, three peaks (peak 1, 2 and 3) were mainly found in the root extract (Figure 3A). Peaks 1 and 2 from the HPLC-DAD results were identified as chlorogenic acid and 3,5-dicaffeoylquinic acid, respectively, according to the retention times (Rt) and UV spectra (220–400 nm) (Figure 3) of the corresponding standard compounds (chlorogenic acid, Rt = 10.01 min, λmax = 218, 236 and 326 nm, λmin = 230 and 263 nm; 3,5-dicaffeoylquinic acid, Rt = 16.53 min, λmax = 219, 242 and 328 nm; λmin = 230 and 264 nm). In the negative mode of MS detection, peak 1 showed an [M-H]− ion at m/z 353 and peak 2 showed an [M-H]− ion at m/z 515; similar ions were detected in the respective standard compounds. From the quantification results, the concentrations of chlorogenic acid and 3,5-dicaffeoylquinic acid were 1.01 ± 0.13 mg/g fresh weight (FW) and 2.31 ± 0.52 mg/g FW, respectively. Peak 3 might be a chlorogenic acid derivative due to UV spectrum, however, it was not identified via the comparison of standard chemicals of chlorogenic acid derivatives.

4. Discussion

In general, distinctive vegetation has been established on a heavy metal-concentrated soil [20,21]. In fact, previous reports [22,23] conducted surveys at several mines in Japan and observed common vegetation, such as M. sinensis, Fallopia japonica, and F. sachalinensis. M. sinensis and F. sachalinensis were also observed in high frequency in our vegetation survey. In addition, at our study site, high incidences of T. repens and P. densiflora were confirmed. M. sinensis that grows at the mine site is recognized as a metal-tolerant perennial herb, which can accumulate high concentrations of Al in the roots via production of detoxicants and cell-wall adsorption of Al, thus inhibiting its entry into the cytosol [24]. In a previous study [25], T. repens growing in metal-concentrated soil accumulated high concentrations of Cd, Pb, and Zn in the roots than in the shoots. In a pot experiment using metal-concentrated soil, P. densiflora seedlings accumulated Cd, Cu, Pb, and Zn in the roots [26]. In addition, Phragmites australis, which is the main aquatic plant species located along a brook, is also known to accumulate metals in the roots and is used in rhizofiltration [27,28]. According to our survey results and previous reports [22,23], plant species mainly discovered at our study site would be categorized as heavy metal-tolerant species.
From the preliminary elemental analysis of five plant species, including M. sinensis, T. repens, P. densiflora, F. sachalinensis, and A. indica var. maximowiczii, we selected A. indica var. maximowiczii and F. sachalinensis as the target plants, because both plants accumulated higher concentrations of Al and Fe in the roots compared to the others. In the analysis of root-zone soil, which was collected simultaneously with A. indica var. maximowiczii or F. sachalinensis, each soil contained high total concentrations of Zn, Cu, and Pb, exhibiting neutral pH, compared to the average total concentrations of soil suggested by [8]. Elemental analysis of A. indica var. maximowiczii and F. sachalinensis showed higher accumulations of Fe, Al, and Cu in the roots compared to the acceptable concentration range in plants [1,19]. A. indica var. maximowiczii (synonyms: Artemisia princeps Pamp.) is a plant species distributed from Japan and China to Korea. According to Morishita and Boratynski [12], and Kim et al. [29], A. indica var. maximowiczii growing at metal smelters and mining areas contained high concentrations of heavy metals, such as Cu, Pb and Cd in the roots, and accumulated a high Zn concentration in the roots and shoots. In addition, several studies also reported that other Artemisia species growing in heavy metal-concentrated sites accumulated Zn, Pb, and Cd in the roots and Zn in the aboveground portion [30,31,32]. However, there was not previous research showing the metal tolerance mechanism in A. indica var. maximowiczii. For F. sachalinensis, it also accumulated Fe, Al, and Cu in the roots compared to the acceptable concentration range in the plant [1,19]. F. sachalinensis belongs to the Asian weed of the Fallopia genus, and its congener F. japonica accumulates Cu, Cd, Zn, and Pb in the roots [33,34]; in particular, Cu bound to the cell wall enhances metal tolerance in F. japonica [33]. TF and BCF are the value of measuring the ability of plant species for phytoremediation [35]. The TFs and BCFs in A. indica var. maximowiczii and F. sachalinensis were lower than 1, except for leaves/roots TF of Zn in F. sachalinensis (Table 3) and Zn BCF of roots in A. indica var. maximowiczii (Table 4). Even though the TF and BCF of roots values in A. indica var. maximowiczii and F. sachalinensis were low, both plants accumulated high concentration of metals Al, Fe and Cu in the roots compared to normal plants [1,19]. Mendez and Maier [36] indicated that shoots/roots TFs of metals or BCFs of shoots should be less than 1 for plants selection in phytostabilization. The results suggested that both plants would be possible candidates for phytostabilization at our study site. From the results of our elemental analysis and calculations of TFs and BCFs, A. indica var. maximowiczii was selected to confirm one of the heavy metal tolerance mechanisms, that is, detoxicant production in the roots, because the metal tolerance mechanism of A. indica var. maximowiczii is not clarified yet.
A. indica var. maximowiczii produces several types of chlorogenic acid derivatives [37,38,39]. According to our HPLC and LC/MS analyses, the main phenolic compounds in A. indica var. maximowiczii roots were identified as chlorogenic acid and 3,5-dicaffeoylquinic acid (Figure 3). Chlorogenic acid and 3,5-dicaffeoylquinic acid have been identified in the leaves of A. indica var. maximowiczii [39], and these chemicals show high antioxidative activities [40], which can eliminate reactive radicals released under heavy metal stress in plant cells [9]. High concentrations of metals cause damage to plants, resulting in growth inhibitions [1,11]; this has been attributed to toxic reactive radicals [11]. Therefore, chlorogenic acid and 3,5-dicaffeoylquinic acid are related to metal tolerance in A. indica var. maximowiczii.
In conclusion, our vegetation survey revealed that plants growing at our study site are consistent with plant species confirmed at other mine sites [22,23]. Naturally growing plant species under the soil including high concentrations of metals have evolved their diverse metal-tolerant abilities [6,7]. In addition, A. indica var. maximowiczii and F. sachalinensis accumulated Fe, Al, and Cu present in the heavy metal-concentrated soil at the mine site in the roots, indicating their metal tolerance. Furthermore, A. indica var. maximowiczii produced detoxicants in the roots, such as chlorogenic acid and 3,5-dicaffeoylquinic acid, which exhibited high antioxidative activities; this plays an important role in metal tolerance in A. indica var. maximowiczii. Our results would increase the value of A. indica var. maximowiczii for phytostabilization because A. indica var. maximowiczii is an endemic plant species that has been used in slope revegetation in Japan [41,42]. Recently, it has been observed that root endophytic microbes can enhance metal tolerance in several plants [24,43,44,45,46]; therefore, in future studies, we will elucidate the effects of root endophytes on metal tolerance in A. indica var. maximowiczii via the isolation and identification of microbes. Fundamental knowledge of metal tolerance in A. indica var. maximowiczii will signify the importance of this plant for phytostabilization at mine sites.

Author Contributions

Conceptualization, X.L., K.Y. and K.D.; methodology, X.L., T.H. and M.Y.; software, X.L. and M.Y.; validation, X.L., K.Y., K.D. and S.T.; formal analysis, T.H.; investigation, X.L., K.Y., T.H., M.Y., K.D. and S.T.; resources, S.T.; data curation, X.L., K.Y. and M.Y.; writing—original draft preparation, X.L. and K.Y.; writing—review and editing, K.Y., K.D., T.H. and S.T.; visualization, K.D.; supervision, K.Y. and S.T.; project administration, K.Y. and S.T.; funding acquisition, K.Y. All authors have read and agreed to the published version of the manuscript.

Funding

This work was funded by Grants-in-Aid for Scientific Research (KAKENHI), grant numbers 19H01161 and 19K22151, and Mitsubishi Materials Corporation.

Data Availability Statement

The data are not publicly available due to privacy.

Acknowledgments

We acknowledge the suggestions provided by Mitsubishi Materials Corporation and support for the field survey provided by the Eco-Management Corporation.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study.

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Minerals 11 00806 g001 550
Figure 1. Schematic diagram for vegetation survey at our study site located in the abandoned concentrator.
Figure 1. Schematic diagram for vegetation survey at our study site located in the abandoned concentrator.
Minerals 11 00806 g001
Minerals 11 00806 g002 550
Figure 2. Element concentrations in plant tissues. (A) Element concentrations in plant tissues of A. indica var. maximowiczii and (B) element concentrations in plant tissues of F. sachalinensis. The results are expressed as means ± SEs (n = 5). The differences between the concentrations of elements (Al, Fe, Zn, Cu, and Pb) in each plant tissue were evaluated by one-factorial ANOVA with Scheffé test. Differences were considered significant at p < 0.05, and different letters indicate a statistically significant difference among the tissues.
Figure 2. Element concentrations in plant tissues. (A) Element concentrations in plant tissues of A. indica var. maximowiczii and (B) element concentrations in plant tissues of F. sachalinensis. The results are expressed as means ± SEs (n = 5). The differences between the concentrations of elements (Al, Fe, Zn, Cu, and Pb) in each plant tissue were evaluated by one-factorial ANOVA with Scheffé test. Differences were considered significant at p < 0.05, and different letters indicate a statistically significant difference among the tissues.
Minerals 11 00806 g002
Minerals 11 00806 g003 550
Figure 3. HPLC-DAD results of A. indica var. maximowiczii root extract. (A) HPLC chromatogram at 320 nm of root extracts of A. indica var. maximowiczii.; retention times of peaks 1, 2 and 3 are 9.86 min, 16.52 min and 22.83 min, respectively; (B) chemical structure of chlorogenic acid; (C) chemical structure of 3,5-dicaffeoylquinic acid.
Figure 3. HPLC-DAD results of A. indica var. maximowiczii root extract. (A) HPLC chromatogram at 320 nm of root extracts of A. indica var. maximowiczii.; retention times of peaks 1, 2 and 3 are 9.86 min, 16.52 min and 22.83 min, respectively; (B) chemical structure of chlorogenic acid; (C) chemical structure of 3,5-dicaffeoylquinic acid.
Minerals 11 00806 g003
Table
Table 1. Vegetation survey results in the study site.
Table 1. Vegetation survey results in the study site.
Plant Species 1Average Cover Rate (%)
Miscanthus sinensis22.5
Trifolium repens20.7
Fallopia sachalinensis6.0
Robinia pseudoacacia5.2
Euonymus spp.4.4
Artemisia indica var. maximowiczii3.9
Quercus crispula1.8
Pinus densiflora1.5
Salix spp.1.2
Plantago asiatica1.0
Plant Species 2Average Cover Rate (%)
Pinus densiflora20.0
Miscanthus sinensis14.3
Euonymus spp.7.1
Fallopia sachalinensis3.3
Weigela hortensis2.5
Salix chaenomeloides2.5
Populus tremula var. sieboldii1.9
Toxicodendron trichocarpum1.3
Acer rufinerve0.4
Tripterospermum japonicum0.4
Trifolium repens0.4
Plant Species 3Average Cover Rate (%)
Phragmites australis10.0
Fallopia sachalinensis7.1
Miscanthus sinensis5.3
Artemisia indica var. maximowiczii4.7
Trifolium repens3.4
Typha latifolia2.8
Equisetum arvense2.5
Carex spp.1.7
Eragrostis ferruginea0.5
Salix spp.0.3
1 shows result of line 1; 2 shows result of line 2; 3 shows result of line 3.
Table
Table 2. Total element concentrations in root-zone soils of the target plants.
Table 2. Total element concentrations in root-zone soils of the target plants.
ElementsRoot-Zone SoilUnpolluted Soil in Japan *General Soil **
A. indica var. maximowicziiF. sachalinensis
Fe30,616.1 ± 904.046,640.9 ± 11,356.1–40,000
Al8699.5 ± 564.78490.1 ± 862.5–70,000
Zn226.4 ± 15.1624.3 ± 165.76090
Cu390.5 ± 21.11291.5 ± 263.21930
Pb209.6 ± 31.81367.5 ± 523.21730
The results are expressed as mean (mg/kg) ± SE (n = 5). * Unpolluted soil data in Japan were obtained from [18]. ** General soil data were obtained from [8]. – indicates no data were shown in the reference.
Table
Table 3. Translocation factors (TFs) of elements in A. indica var. maximowiczii and F. sachalinensis.
Table 3. Translocation factors (TFs) of elements in A. indica var. maximowiczii and F. sachalinensis.
ElementsStems/RootsLeaves/Roots
A. indica var. maximowicziiF. sachalinensisA. indica var. maximowicziiF. sachalinensis
Al0.08 ± 0.010.07 ± 0.010.56 ± 0.100.31 ± 0.08
Fe0.07 ± 0.010.04 ± 0.010.36 ± 0.010.26 ± 0.05
Zn0.66 ± 0.16 *0.38 ± 0.070.70 ± 0.151.19 ± 0.22
Cu0.21 ± 0.060.23 ± 0.030.21 ± 0.030.39 ± 0.10 *
Pb0.07 ± 0.00–0.19 ± 0.03–
The results expressed as means ± SEs (n = 5). – indicates TF values could not be calculated because the element concentrations in stems and leaves were under the detection limit. * p < 0.05. Differences between plant species were evaluated by Student’s t-test.
Table
Table 4. Bioconcentration factors (BCFs) of elements in A. indica var. maximowiczii and F. sachalinensis.
Table 4. Bioconcentration factors (BCFs) of elements in A. indica var. maximowiczii and F. sachalinensis.
ElementsRootsStemsLeaves
A. indica var. maximowicziiF. sachalinensisA. indica var. maximowicziiF. sachalinensisA. indica var. maximowicziiF. sachalinensis
Al0.10 ± 0.010.27 ± 0.04 *0.01 ± 0.000.02 ± 0.000.05 ± 0.010.08 ± 0.02
Fe0.13 ± 0.060.09 ± 0.010.01 ± 0.000.00 ± 0.000.03 ± 0.010.02 ± 0.00
Zn1.26 ± 0.24 *0.37 ± 0.060.72 ± 0.140.13 ± 0.030.71 ± 0.06 *0.45 ± 0.12
Cu0.58 ± 0.080.25 ± 0.050.11 ± 0.020.06 ± 0.020.12 ± 0.010.08 ± 0.03
Pb0.35 ± 0.07–0.02 ± 0.00–0.06 ± 0.01–
The results expressed as means ± SEs (n = 5). – indicates TF values could not be calculated because the element concentrations in roots, stems and leaves were under the detection limit. * p < 0.05. Differences between plant species were evaluated by Student’s t-test.
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Lu, X.; Yamaji, K.; Haruma, T.; Yachi, M.; Doyama, K.; Tomiyama, S. Metal Accumulation and Tolerance in Artemisia indica var. maximowiczii (Nakai) H. Hara. and Fallopia sachalinensis (F.Schmidt) Ronse Decr., a Naturally Growing Plant Species at Mine Site. Minerals 2021, 11, 806. https://doi.org/10.3390/min11080806

AMA Style

Lu X, Yamaji K, Haruma T, Yachi M, Doyama K, Tomiyama S. Metal Accumulation and Tolerance in Artemisia indica var. maximowiczii (Nakai) H. Hara. and Fallopia sachalinensis (F.Schmidt) Ronse Decr., a Naturally Growing Plant Species at Mine Site. Minerals. 2021; 11(8):806. https://doi.org/10.3390/min11080806

Chicago/Turabian Style

Lu, Xingyan, Keiko Yamaji, Toshikatsu Haruma, Mitsuki Yachi, Kohei Doyama, and Shingo Tomiyama. 2021. "Metal Accumulation and Tolerance in Artemisia indica var. maximowiczii (Nakai) H. Hara. and Fallopia sachalinensis (F.Schmidt) Ronse Decr., a Naturally Growing Plant Species at Mine Site" Minerals 11, no. 8: 806. https://doi.org/10.3390/min11080806

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