Phytoremediation Properties of Sweet Potato for Soils Contaminated by Heavy Metals in South Kazakhstan

Abstract

Industrial waste in the form of abandoned mine tailings from a former lead plant in South Kazakhstan amounts to about 2 million tons, and this has led to environmental pollution with heavy metals (HMs) in Shymkent city. The concentrations of Pb, Zn, and Cd in the mine tailings were 1354.50, 262.90, and 61.08 mg/kg, respectively. The contamination of the adjacent soils with Pb, Zn, and Cd ranged from 7.76 to 551.49, from 8.25 to 245.74, and from 5.40 to 19.23 mg/kg, respectively. In this study, the phytoremediation properties of sweet potato on soils contaminated with HMs adjacent to mine tailings were investigated. The phytoremediation efficiency of sweet potato was assessed in terms of its capacity to biotransfer and bioaccumulate HMs. The concentrations of Pb, Zn, and Cd in sweet potato in the experimental fields were 28.70–45.10, 70.0–94.20, and 1.19–1.80 mg/kg, respectively. It was determined that the pollution class of the studied soils according to I_geo was high pollution (5.28–8.80), and the potential risk of HM accumulation according to the ecological risk index proposed by Hakanson was moderate pollution.

1. Introduction

The pollution of soil by heavy metals is a significant environmental problem all over the world. Active industrialization of the Republic of Kazakhstan in the last century was accompanied by intensive construction and operation of industrial enterprises and factories. As a consequence, there was significant pollution of the environment and growth of urbanization, with a subsequent increase in the concentrations of toxic metals. In particular, there were mine tailings from the industrial production of a lead factory located almost in the center of Shymkent city, which had operated for 70 years since 1937. These mine tailings were a source of HM pollution affecting the entire metropolis. The factory was abandoned between 2010 and 2015, and lead dust waste is still stored at the former factory site. Over 2 million tons of lead waste has accumulated over 70 years and poses a serious threat to residents living in the immediate vicinity [1].

Accumulation of certain amounts of HMs in the soil leads not only to its degradation [2], suppression of plant growth and development [3], and deterioration of its quality as a natural resource but also pollutes surface and groundwater through runoff and the vertical migration of water in the soil [4]. Unlike organic pollutants, heavy metals are not biodegradable and tend to accumulate in living organisms. Many heavy metal ions (salts) are hazardous or carcinogenic [5,6]. Major HM pollutants include cadmium (Cd), lead (Pb), copper (Cu), mercury (Hg), and arsenic (As), with densities exceeding 5 g/cm³ [7]. In particular, soils contaminated with lead (Pb) are difficult to remediate because of their low mobility, high toxicity, and high persistence [8]. HMs not only degrade the quality of the atmosphere, water, and agricultural crops [9] but also threaten the health of humans and fauna through the food chain [10,11]. HMs do not decompose, which means that they migrate from one place to another in the soil environment, causing a higher degree of pollution.

Given the wide range of dispersion of HM particles in the areas around abandoned industrial enterprises [12,13,14], it is necessary to carry out several stages of soil reclamation, including both technical treatment and biological reclamation [15]. One method of biological reclamation is phytoremediation. In this case, it is necessary to select plant species that have high phytoremediation activity and are able to grow in the recultivated soil [16].

Because of its high antioxidant activity, sweet potato (Ipomoea batatas L.) is a crop with wide ecological adaptation, drought tolerance, and high adaptability to harsh environmental conditions. In addition, it is considered a nutritionally valuable crop because it is rich in dietary fiber, potassium, minerals, and various antioxidants, including anthocyanins, carotenoids, vitamin C, and tocopherols [17,18]. Sweet potato has a high biomass ratio of both stem and tuber necessary for remediation [19]. Additionally, cultivation of sweet potato for the phytoremediation of lead-contaminated soils is possible with the subsequent production of biofuel [20].

Phytoremediation is considered to be the most environmentally friendly and economically feasible remediation technology for reducing the contamination of agricultural land. To evaluate potential ecological impact, the potential ecological risk and geoaccumulation indexes are used to assess the levels of HM concentrations in soil [21]. Fly ash from mine tailings increases HM concentrations in roots by increasing HM uptake and translocation from the root to the aerial part of the plants [22]. To evaluate the phytoremediation properties of plant species, it is also necessary to take into account the bioconcentration factor (BCF), which reflects the ability of plant parts to accumulate HMs, and the translocation factor, which reflects the movement of HMs from the root to the aerial part of the plants [23]. Determination of heavy metals in different samples is difficult due to the complex nature of the sample and the different chemical forms in which the metals can be found. Atomic absorption spectrometry with flame is a very precise, simple method to determine HM for single measurement of large samples [9,13,24,25].

This research attempted to determine the phytoremediation properties of sweet potato for the biological remediation of soils contaminated with HMs. It consists of a determination of the dynamics of HM distribution in the soil on the territory of the abandoned Shymkent lead factory and an experimental study of the phytoremediation properties of sweet potato grown on soils contaminated with HMs.

2. Materials and Methods

2.1. Site Description

The study concerned the mine tailings of the lead factory (42°18′51″ N 69°32′21″ E) and the adjacent area of Shymkent City, which has a population of over 1.1 million people [26].

The climate of the region is characterized by aridity, with a maximum annual precipitation of 600 mm in Shymkent, most of which falls in the autumn and winter (according to meteorological data from 2000 to 2022). The average annual temperature is 13 °C. The highest (47.2 °C) and lowest (−31.1 °C) temperatures were recorded in July and January, respectively. The main wind direction is east-northeast, with an average speed of 1.63 m/s per year and a maximum speed of 18 m/s [27,28].

The factory was founded in the 1940s and was originally located outside the city boundaries; however, because of the high rate of urbanization, a new district of the city was formed in 2022, and new residential buildings were constructed in the mine tailings area. Over 2 million tons of waste were generated in the form of mine tailings over the lifetime of the factory [1] (Figure 1). The factory produced mainly metallic zinc and lead.

2.2. Cultivation Methods for Sweet Potatoes

Sweet potato plants were used in the experiment. Propagation and cultivation of the sweet potato were carried out using 25–30 cm long cuttings and planting them in a boat-shaped orientation relative to the ridges at a depth of 7–10 cm [29]. Cuttings from sweet potato plants were planted in the farmsteads of local residents at 10–15 plants per 30 cm ridge. The duration of the planting period was 133 days from May to September 2022. Samples were collected on day 133 to analyze the sweet potato components for their HM concentration.

2.3. Sampling Procedures

Experimental cultivation of sweet potatoes on the land adjacent to the mine tailings was carried out at the following coordinates: Field 1, 42°18’30.6” N 69°31’60.0” E; Field 2, 42°18’29.7” N 69°31’58.1” E; Field 3, 42°18’58.4” N 69°32’42.9” E; and the control, 42°21’15.7” N 69°36’43.5” E (Figure 2). Cuttings from sweet potato plants were planted by local households in 30 cm ridges of 10–15 plants each. The sweet potato crop was harvested.

Sweet potato samples were collected from the three experimental plots, and 1–2 g of the homogenized dried sample was weighed into a 50 mL quartz crucible. The sample was placed into a cool muffle furnace, and the temperature of the oven was raised to 500–550 °C for several hours. Next, the ash was dissolved in 25 mL of 1% nitric acid and diluted to 25 mL in a volumetric flask [30].

2.4. Soil Sampling

Soil samples were taken from the three fields of private farmsteads around the mine tailings in which sweet potato crops had been planted. Soil from the control plot on a private farmstead significantly distant from the contaminated site (42°21’15.7” N 69°36’43.5” E) was also sampled.

Soil samples were taken from one or more layers using the envelope sampling method (along the diagonal). Combined samples were created by mixing five point samples taken from one sample site. The point samples were taken layer by layer from depths of 5 and 15 cm, with the mass of each sample not exceeding 200 g. The mass of the combined sample was at least 1 kg.

The soil samples were collected and sieved. A quantity of 2 g of dried soil sample was transferred into a 100 mL Erlenmeyer flask, and concentrated nitric acid was added. Then, the sample was boiled in a water bath at 80 °C for 3 h. Next, it was cooled at room temperature, 25 mL water was added, and the resulting extract was filtered on filter paper into a 25 mL volumetric flask. These clear filtrate solutions were analyzed using an atomic absorption spectrometer [31].

2.5. Ecological Risk Assessment and Geoaccumulation Index (Contamination Assessment Methodology)

The potential environmental risk index was proposed by Hakanson [21]. This method simultaneously takes into account several factors: concentration of HMs in soil, type of pollutant, and toxicity level. It comprehensively estimates the potential impact of HMs on environmental systems. It is possible to estimate the risk presented by a single factor (environmental risk coefficient, E_r) as well as the risk presented by a number of elements (potential environmental risk index, R_I). The risk is calculated using the following equations [32]:

C_f = C_sample/C_background

(1)

where C_f is the contamination factor, C_sample is the concentration of HMs in polluted soil, mg∙kg⁻¹, and C_background is the natural background concentration in the soil, mg∙kg⁻¹;

E_r = T_r × C_f

(2)

$$R_I={{\displaystyle \sum }}_{i=1}^n{E}_r$$

(3)

where R_I is the comprehensive potential ecological risk index, E_r is the individual potential ecological risk index of HM, T_r is the toxicity coefficient of the HMs (Pb–5, Zn–1, Cd–30), and C_f is the pollution coefficient of the HMs.

The value of R_I indicates the type and quantity of the pollution. The classification criteria proposed by Hakanson [21] for the R_Iand E_r values are shown in

Table 1. Interpretation of the value of the potential environmental risk indicator.

Er	Levels	RI	Levels
Er ˂ 40	Low	RI ˂ 150	Low
40 ≤ Er ˂ 80	Moderate	150 ≤ RI ˂ 300	Moderate
80 ≤ Er ˂ 160	Considerable	300 ≤ RI ˂ 600	Considerable
160 ≤ Er ˂ 320	High	RI ≥ 600	High
Er ≥ 320	Very high

R_I is the comprehensive potential ecological risk index; E_r is the individual potential ecological risk index of heavy metal.

.

Geoaccumulation Index

The geoaccumulation index, I_geo, estimates the degree of soil contamination by heavy metals, and is calculated on the basis of the concentrations of the metal present in the soil, the geochemical background value of this metal, and a coefficient of 1.5 to take possible deviations into account [33,34]:

I_geo = log₂(Cn/1.5 × Bn)

(4)

where I_geo is the geoaccumulation index of the HM, C_n is the concentration of the HM in the soil, B_n is the geochemical background value of the HM, and 1.5 is the deviation coefficient. The level of pollution is divided into 7 classes, ranging from no pollution to extremely high pollution:

I_geo ≤ 0, uncontaminated (Class 0);

0 < I_geo ≤ 1, uncontaminated to moderately contaminated (Class 1);

1 < I_geo ≤ 2, moderately contaminated (Class 2);

2 < I_geo ≤ 3, moderately to heavily contaminated (Class 3);

3 < I_geo ≤ 4, heavily contaminated (Class 4);

4 < I_geo ≤ 5, heavily to extremely contaminated (Class 5);

I_geo > 5, extremely contaminated (Class 6).

The bioconcentration factor was used to determine the phytoremediation properties of plants. According to this, if the index value of the factor is below 1, the plant is tolerant of HMs, and if it is above 1, it is a hyperaccumulator. The bioconcentration factor denotes the ability of the parts of the plant to elementally accumulate pollutants from the environment [35]:

BCF = C_plant/C_soil

(5)

where BCF is the bioconcentration factor, C_plant is the concentration of heavy metals present in the sweet potato, mg∙kg⁻¹, and C_soil is the concentration of heavy metals in the soil, mg∙kg⁻¹.

The translocation factor (TF) is the value of the metal concentration in the aerial part of the plant in relation to the concentration in the root of the plant. This value is used to estimate the ability of plants to transfer HMs to their aerial parts [35]:

TF = C_aerial/C_roots

(6)

2.6. Spatial Interpolation

The geo-ecological map based on actual data was constructed using Qgis 3.30.1. with the IDW (inverse distance weighting) method. IDW is one of the most commonly used deterministic interpolation algorithms in soil investigation, and it focuses on areas directly around the objects of study and given coordinate points. The inversion of width around the investigation objects from the interpolation point is used to determine the weighted particles of the assigned location of the conducted interpolation. Therefore, it is shaped in such a way that close points have a higher weighting (and, therefore, a greater influence) than distant points, and vice versa. The Qgis system is self-managed and does not require additional calculations during map creation [34,36].

2.7. Atomic Absorption Spectrometry

The calibration curves were prepared using lead (Pb), zinc (Zn), and cadmium (Cd) (Ecroskhim Co., Ltd., Moscow, Russia) with atomic absorption stock solutions (1.0 g/L) by making successive dilutions. A working calibration solution between 1 mg/L and 10 mg/L was prepared. For the preparation of the solutions, ultrapure water obtained from a Milli-Q system (Merck, Millipore) was used. All chemical reagents used were of standard analytical grade, including nitric acid (65%) and hydrogen peroxide (30%).

For validation of the analytical procedure, reference standard solutions were used, and the results should lay within ±1 of the certified values. The method was validated in terms of linearity and range of the calibration curves. Linearity was validated using reference standard solutions by repeating the process five times for each metal. The limit of detection (LOD) and limit of qualification (LOQ) values for each metal were calculated for each solution: 1 mg/L, 2 mg/L, 5 mg/L, and 10 mg/L concentrations for Pb, Zn, and Cd, respectively.

Pb, Zn, and Cd concentrations were determined using a flame atomic absorption spectrometer (Analytik Jena AG, novAA 350, Jena, Germany) equipped with a hollow cathode lamp and an air–acetylene flame. The wavelengths (nm) used for the determination of the analyses were Pb 283.3 nm, Zn 232.0 nm, and Cd 228.8 nm. The gas flow was 50 dm³/h, and the aspiration rate was 5 cm³/min. Single-element hollow cathode lamps (Hamamatsu Photonics K.K., Hamamatsu, Japan) of Pb, Zn, and Cd were used as light sources.

2.8. Scanning Electron Microscope

The surface morphology and topography of the mine tailings lead samples were observed using scanning electron microscopy with an energy dispersive spectrometer (SEM-EDS) (JSM-6510, JEOL/EO, Tokyo, Japan) at an accelerated voltage of 10 kV. The surface structural images were obtained using the high vacuum secondary electron detector of the microscope. Lead slag was fixed inside the instrument at a working distance of 7 mm (WD 7 mm), magnification value of 3000× (maximum), and spot size 50 (SS50).

2.9. Statistical Analysis

Pearson’s correlation coefficient was used to understand the HM concentration correlations. Principal component analysis (PCA) was used to determine the source of the HM in the soil and sweet potato plants. PCA was used to analyze the HM value after checking the suitability.

3. Results and Discussion

3.1. Validation of the Method

A quantitative analysis of the HM was carried out, and calibration curve equations were plotted between concentrations 1.0 and 100 mg/L. The calibration curves consisted of four concentrations.

Table 2. LOD and LOQ values and linear parameters for the HM calibration standards.

HM	R2	Calibration Curve Equation	Range (mg/L)	LOD (mg/L)	LOQ (mg/L)
Pb	0.9999	y = 0.9956x − 0.2264	1.0–10.0	0.06	0.18
Zn	0.9998	y = 0.9852x − 0.1013	1.0–10.0	0.10	0.31
Cd	0.9998	y = 1.2255x − 0.1155	1.0–10.0	0.09	0.26

R, correlation coefficient; LOD, limit of detection; LOQ, limit of quantification.

shows correlation coefficients, calibration curve equations, ranges, LOD, and LOQ values for each HM. The correlation coefficients were more than 99%, confirming excellent response. The LOD value was between 0.06 mg/L and 0.10 mg/L, and the LOQ values varied between 0.18 mg/L and 0.31 mg/L, which showed that the method is sensitive.

Table 3. Reference standard certified and measured values and the recovery.

HM	Certified Values (mg/L)	Measured Values (mg/L)	Recovery (%)	Mean Recovery ± SD (%)
Pb	5.0	4.98	99.6	99.6 ± 0.15
	10.0	9.97	99.7
Zn	5.0	4.95	99.0	99.4 ± 1.51
	10.0	9.98	99.8
Cd	5.0	5.01	100.0	100.5 ± 0.57
	10.0	10.05	101.0

SD, standard deviation.

shows the mean recovery and standard deviation results using reference standard solution for each HM. Results for HM were in agreement at a 95% confidence level with the certified values for each metal. Mean recovery results were between 99.6 and 100.5% for all metals.

3.2. Soil Characterization

The mine tailings had high heavy metal concentrations of 1354.50 ± 2.26, 226.90 ± 1.61, and 61.08 ± 0.20 mg/kg for Pb, Zn, and Cd, respectively. At Point 1 (50 m from the mine tailings epicenter) in the top layer (5 cm) of soil close to the mine tailings, the highest concentrations of Pb, Zn, and Cd were 551.49 ± 1.91, 245.74 ± 0.49, and 19.23 ± 0.02 mg/kg, and at a depth of 15 cm they were 368.73 ± 0.40, 216.21 ± 0.37, and 11.91 ± 0.01 mg/kg, respectively (Figure 1). At Point 2 (200 m from the epicenter of the mine tailings), the concentrations of Pb, Zn, and Cd were 12.79 ± 0.03, 48.18 ± 0.08, and 14.28 ± 0.02 mg/kg in the upper layer and 7.76 ± 0.07, 8.25 ± 0.07, and 5.40 ± 0.04 mg/kg, respectively, in the lower layer. (

Table 4. HM concentration of soil samples from mine tailing slag at different depths (5 and 15 cm).

Heavy Metals	Mine Tailings, mg/kg	Soil, mg/kg				MPC, mg/kg [37]
		Point 1		Point 2
		Depth (5 cm)	Depth (15 cm)	Depth (5 cm)	Depth (15 cm)
Pb	1354.5 ± 2.26	551.49 ± 1.91	368.73 ± 0.40	12.79 ± 0.03	7.76 ± 0.07	32.0
Zn	262.90 ± 1.61	245.74 ± 0.49	216.21 ± 0.37	48.18 ± 0.08	8.25 ± 0.07	23.0
Cd	61.08 ± 0.20	19.23 ± 0.02	11.91 ± 0.01	14.28 ± 0.02	5.40 ± 0.04	2.0

MPC, maximum permissible concentration.

). Our results were consistent with those of other researchers [1] in showing concentrations of 350.6, 54.3, and 11.8 mg/kg of Pb, Zn, and Cd, respectively, around 500 m from the mine tailings. Thus, the amount of Pb at Point 1 in the area adjacent to the factory was found to be 11.5 to 17 MPC. Zn concentration at Point 1 was 9 to 10 MPC. Cd concentrations were the highest at all sampled points in the mine tailings area at 2.5 to 20 MPC.

HM concentrations in polluted soils exceeding the MPC were determined according to the regulations. MPC values (mg/kg) for HMs were 32.0 for Pb, 23.0 for Zn, and 2.0 for Cd [37].

The territories adjacent to Shymkent City are characterized by ordinary greyzem [38]. These are soils with a low-moisture, low-humus surface, an arid moisture regime, and the absence of permafrost within 200 cm of the surface [39]. As these are alkaline soils, with a pH of 7.5–8 and absolute dominance of oxidative processes, they do not have a high capacity to accumulate Pb, Zn, or Cd directly, but Pb processing wastes, as shown in Figure 2, have contaminated the area for more than 70 years. [1]. In Figure 3, the distribution of Pb, Zn, and Cd is illustrated using color interpolation. The areas of distribution of certain HM concentrations are highlighted by isolines and displayed at the scale of the sampling points and the adjacent mine tailings territory.

3.3. SEM Analyses

SEM produced two-dimensional data, which allowed visual identification of metal slag particle surfaces without sputter coating. According to the results of SEM-EDS analysis, the slag from mine tailings mainly contained SiO2 (22.2%), oxides (46%), and carbon (17.8%), in addition to Zn (9.08%) and Pb (4.22%), as shown in Figure 4c. Figure 4a,b show SEM images at 400× and 3000× magnification, respectively.

An atomic absorption spectrometer was used to estimate the distribution of heavy metal concentration at each site. The average Pb concentration of the soil samples from the three experimental (Fields 1, 2, and 3) and control sites were 4.94 ± 0.07, 2.72 ± 0.03, 5.34 ± 0.06, and 2.20 ± 0.03 mg/kg, respectively (

Table 5. HM concentrations of mine tailings, soils, and sweet potatoes.

HM	Mine Tailings, mg/kg	Depth (cm)	Soil, mg/kg				Tuber, mg/kg				Leaves, mg/kg
			Field 1	Field 2	Field 3	C	Field 1	Field 2	Field 3	C	Field 1	Field 2	Field 3	C
Pb	1354.5 ± 2.26	5	5.52 ± 0.07	22.13 ± 0.09	15.31 ± 0.06	3.29 ± 0.01	28.7 ± 0.07	45.1 ± 0.09	34.0 ± 0.03	0.96 ± 0.01	2.34 ± 0.06	10.1 ± 0.07	32.5 ± 0.09	1.09 ± 0.02
		15	4.94 ± 0.07	2.72 ± 0.03	5.34 ± 0.06	2.20 ± 0.03
Zn	262.90 ± 1.61	5	31.22 ± 0.1	47.99 ± 0.01	150.50 ± 0.05	25.83 ± 0.05	70.0 ± 0.05	94.1 ± 0.09	94.2 ± 0.07	38.5 ± 0.07	8.24 ± 0.06	14.1 ± 0.01	59.4 ± 0.01	7.6 ± 0.01
		15	3.87 ± 0.02	24.63 ± 0.02	109.69 ± 0.03	3.70 ± 0.03
Cd	61.08 ± 0.20	5	7.69 ± 0.01	6.69 ± 0.02	20.52 ± 0.01	6.44 ± 0.01	nd	1.80 ± 0.02	1.19 ± 0.03	nd	nd	nd	2.75 ± 0.01	nd
		15	4.04 ± 0.01	5.97 ± 0.02	14.56 ± 0.04	3.18 ± 0.01

C, control; nd, not detected.

). These data showed that Pb concentrations were different at the three sites and varied by as much as 51%. The mean Zn concentrations at the sites were 3.87 ± 0.02, 24.63 ± 0.02, 109.69 ± 0.03, and 3.70 ± 0.03 mg/kg, respectively. Zn concentrations were very different at the three sites. In addition, the Cd concentrations were 4.04 ± 0.01, 5.97 ± 0.04, 14.56 ± 0.04, and 3.18 ± 0.01 mg/kg, respectively (Table 5).

3.4. Heavy Metal Concentration in Sweet Potato Samples

The concentrations of Pb, Zn, and Cd in the sweet potato samples are presented in Table 5, which shows that the HM concentrations of tubers and leaves differed significantly. The HM concentrations were significantly higher in the sweet potato samples than in the control samples. The highest HM concentrations were found in Field 3, in which the Pb, Zn, and Cd concentrations in tubers were 34.0 ± 0.03, 94.2 ± 0.07, and 1.19 ± 0.03 mg/kg and in leaves were 32.5 ± 0.09, 59.4 ± 0.01, and 2.75 ± 0.01, respectively. Furthermore, in the experimental sites Field 1 and Field 2, the Pb, Zn, and Cd concentrations in tubers varied from 28.7 ± 0.07 to 45.1 ± 0.09, 70.0 ± 0.05 to 94.1 ± 0.09, and 0 to 1.80 ± 0.02 mg/kg, respectively. At the control site, the tubers showed 0.96 (Pb), 38.5 (Zn), and Cd was not detected. Thus, in the control samples, the Pb and Zn values were 31 and 2.14 times lower.

The concentrations of Pb, Zn, and Cd in leaves from Field 3 showed very high values of 32.5 ± 0.09, 59.4 ± 0.01, and 2.75 ± 0.01 mg/kg, respectively. Cd was detected in the sweet potatoes grown at the Field 3 experimental site. Pb concentrations in Field 1 and Field 2 were 2.34 ± 0.06 and 10.1 ± 0.07 mg/kg, respectively, whereas at the control site, it was 1.09 ± 0.02 mg/kg. Additionally, Zn concentrations in Field 1 and Field 2 were 8.24 ± 0.06 and 14.1 ± 0.01 mg/kg, respectively, whereas the control sample measured 7.6 ± 0.01 mg/kg. According to the results in Table 5, Pb concentration was highest in mine tailings and lower in soil and sweet potatoes. However, Zn concentrations were lower in lead slag samples but showed higher concentrations in soil and sweet potatoes than other HMs. Different behaviors were reported for Zn concentration. For example, high Zn concentration accumulated in control and contaminated sites [40]. HM (Pb, Zn, Cd, Cu) in soil samples transferred in grains, but Zn concentration was not predicted by total HM in soil [41]. The results of other researchers highlighted different absorption levels of HM, where sweet potatoes cultivated from contaminated mine tailings soils and sweet potato cultivars influenced accumulation properties [42].

According to data presented by other researchers involving 14 sweet potato varieties, the tendency for Cd and Pb to accumulate in tubers was consistently proved, but a lower index was indicated in shoots and roots [43]. Pb accumulation in roots was found to be characteristic of rapeseed (Brassica napus), mustard (Brassica carinata) [44], red amaranth (Amaranthus gangeticus) [45], and water spinach (Ipomoea aquatica Forsk) [46]. Maize (Zea mays L.) accumulated Cd in its leaves [47], and lettuce was characterized by Cd accumulation in its roots [48]. Other studies considered Zn accumulation. Compared with these results, low concentrations of Zn were found in radish [49]. On the other hand, high concentrations were reported for leek, paddy rice (Oryza sativa L.) [50], and maize [47].

According to our data, there was a clear trend of HM accumulation in tubers (Table 5). Such stability and accumulation of HMs in the plant root system were characteristic of some hyperaccumulator ecotypes [51], in which HMs were predominantly accumulated in the plant roots or root walls [52]. It was proved that in T. caerulescens, the main part of Cd was stored in the root apoplast [53], and other studies showed that Cd retention after root uptake occurred in the root cell walls [54]. Pb also accumulated in the root walls or in the vacuole [55]. The accumulation of pollutants in separate parts of the plant cell is referred to as compartmentalization, and its purpose is to move HMs into vacuoles, trichomes, and hydropotes in order to prevent cellular destruction [56].

3.5. Heavy Metal Accumulation and Ecological Risk Assessment

The contamination factor, geoaccumulation index, and environmental risk for Pb, Zn, and Cd are presented in

Table 6. HM concentrations of mine tailings, soils, and sweet potatoes.

Field	Depth (cm)	Pb			Zn			Cd
		Cf	Igeo	Er	Cf	Igeo	Er	Cf	Igeo	Er
1	5	2.05	7.32	10.25	1.22	9.05	1.22	0.95	5.37	28.59
	15	0.46	5.15	2.29	0.15	6.04	0.15	0.50	4.44	15.02
2	5	0.51	5.31	2.56	1.88	9.67	1.88	0.83	5.17	24.87
	15	0.25	4.28	1.25	0.97	8.71	0.97	0.74	5.01	22.19
3	5	1.42	6.78	7.09	5.90	11.32	5.90	2.54	6.79	76.28
	15	0.49	5.26	2.47	4.30	10.86	4.30	1.80	6.29	54.13
control	5	0.30	4.57	1.52	1.01	8.78	1.01	0.80	5.11	23.94
	15	0.20	3.99	1.02	0.15	5.97	0.15	0.39	4.10	11.82

C_f, contamination factor; I_geo, geoaccumulation index of HM; and E_r, individual potential ecological risk index of HM.

. According to the contamination coefficients [21] for the soils containing Pb, higher figures were noted for samples taken at a depth of 5 cm, with six samples being characterized by a low level of contamination, and the only samples shown as moderately contaminated were those taken from a depth of 5 cm for Point 1 (which was on the leeward side) and Field 3 (the closest site to the mine tailings). The results for Cd contamination showed a similar trend, with the samples from the fields characterized by moderate contamination. For Zn, there was a significant degree of contamination in the field samples and a predominance of moderate contamination among the other soil samples.

The geoaccumulation index proposed by Muller [33] was used to identify and determine the metal contamination of soil. The HM geoaccumulation factor indicated high levels for all metals at all sampling points. The highest index was 11.32 units for Zn in Field 3 at a depth of 5 cm and was characterized as extreme Zn contamination. This was also seen in the other soil samples with values of 3.2 and 2.26 (as shown in

Table 7. Comparison of the ecological assessment in soil samples with other studies from industry sites.

Location	Igeo			Er			References
	Pb	Zn	Cd	Pb	Zn	Cd
Belgrade, Serbia	3.3	3.2	1.8	4	2	63	Radomirovic et al. [57]
Southeast Coast, Jamaica	−0.05	−1.70	nd	0.4	0.6	nd	Williams et al. [59]
Guangzhou, China	0.46	2.26	2.70	8.60	10.70	200.48	Liu et al. [58]
Drama district, northern Greece	0.70	−0.30	1.10	31.50	1.90	139.29	Sofianska et al. [60]
Central Andes, Peru	−0.56	−0.53	−2.47	8.25	1.08	8.14	Mendoza et. al. [61]
Konya, Turkey	−0.30	−1.05	−0.41	5.29	0.98	24.32	Horasan et al. [24]
Shymkent, Kazakhstan	5.33	8.80	5.28	3.55	1.94	32.10	This study

I_geo is the HM geoaccumulation index; E_r, individual HM potential ecological risk index.

), which are higher than those identified by other authors [57,58]. Extreme Pb contamination was noted in Fields 1 and 3, for which the indices were 5.26 and 7.32, respectively, also higher concentrations than those reported by other authors [58,59,60]. Excessive concentrations of Cd were also found in Field 3. The environmental risk values associated with Pb and Zn showed a low level of risk. However, the values for Cd in Field 3 were described as a moderate level of risk, consistent with the findings of other researchers [24,61].

3.6. Bioconcentration and Translocation Factors

The bioconcentration factor is one of the main indicators of the phytoremediation efficiency of a plant; it is an indicator of the ability of the plant to accumulate HMs from the soil [62].

Table 8. Bioconcentration and translocation factors in sweet potato.

		Field	Pb	Zn	Cd
Bioconcentration factor	Tuber	Field 1	10.50	18.08	nd
		Field 2	9.12	35.77	0.30
		Field 3	6.36	0.85	0.081
	Aerial parts (leaves)	Field 1	1.70	12.18	nd
		Field 2	4.22	17.72	nd
		Field 3	6.01	1.34	0.33
Translocation coefficient	Aerial parts/roots	Field 1	0.08	0.11	nd
		Field 2	0.22	0.14	nd
		Field 3	0.95	0.63	2.31

nd, not detected.

provides the BCF calculation results for sweet potato grown in three contaminated fields. The sweet potato tuber BCFs for Zn in Fields 1, 2, and 3 were 18.08, 35.77, and 0.85, respectively. This correlated with the results for the leaf BCF, which were 12.18, 17.72, and 1.34, respectively. A lower absorption of Zn was observed for Field 3 and higher for Fields 1 and 2. Brown rice used as a food plant in South Korea showed a low BCF [63], but plants such as Corchorus olitorius and Solanum nigrum had a Zn BCF greater than 1 [64]. BCF and TF also depended on sweet potato varieties, where authors showed the effectiveness of phytoremediation properties of sweet potatoes lead removal efficiencies by kg/ha. Also, the process has been accelerated with the addition of fertilizer to obtain more yields, correspondingly more accumulation of HM. HM accumulation and transfer mechanisms at the whole plant level in these plants depend on several processes: tuber metal uptake, translocation between roots and aerial parts, transport to deciduous organs or less active tissues or cell types, and transfer to seeds [44].

The BCFs for Cd were 0.3 and 0.08 for Fields 2 and 3, respectively. These values indicated low HM accumulation. However, there was a clear correlation between the decrease in the BCF and the increase in the TIF of the plant. There were high values for Cd in the leaves compared with the tuber, with a TF of 2.31 indicating active movement of metal ions in the plant, and similar dynamics were observed in four species of Brassica [44]. The opposite dynamic was observed in a study of Virginia fanpetals [65].

Pb values for Fields 1, 2, and 3 were 10.5, 9.12, and 6.36, and for leaves 1.7, 4.22, and 6.01, respectively. Previous studies by Dinçer et al. concerning Carthamus tinctorius L. [66] and Parthenium hysterophorus [25] observed the same correlation between Pb concentration in soil, BCF, and TF.

The ability of sweet potato to accumulate metals was as follows: Zn > Pb > Cd. With the exception of Cd with BCF < 1, this indicator was >1 for Zn and Pb, from which we can conclude that sweet potato has great potential for use in phytoremediation.

3.7. Correlation and Principal Component Analysis

Pearson’s correlation analysis of soil heavy metals (

Table 9. Pearson’s correlation coefficient (r) between HMs in soil.

	Pb (5 cm)	Zn (5 cm)	Cd (5 cm)	Pb (15 cm)	Zn (15 cm)	Cd (15 cm)
Pb (5 cm)	1.0000	0.8616	0.5221	0.9995	0.8880	0.4793
Zn (5 cm)		1.0000	0.8372	0.8571	0.9960	0.8564
Cd (5 cm)			1.0000	0.5224	0.7857	0.9049
Pb (15 cm)				1.0000	0.8830	0.4697
Zn (15 cm)					1.0000	0.8241
Cd (15 cm)						1.0000

) showed statistically significant strong positive correlations >0.90 between Pb at 5 cm and 15 cm, Zn at 5 cm and 15 cm, and Cd at 5 cm and 15 cm. A strong correlation was observed between metals at different depths. However, the variation in the heavy metal concentrations in the investigated soil samples was correlated in each field. There were also strong correlations between Zn (5 and 15 cm), Pb (5 and 15 cm), and Cd (5 and 15 cm), with the correlation coefficients ranging from 0.78 to 0.85.

Pearson’s correlation analysis of the different parts of the sweet potato plants is shown in

Table 10. Pearson’s correlation coefficient (r) between parts of sweet potato plants.

	Pb (Tuber)	Zn (Tuber)	Cd (Tuber)	Pb (Leaves)	Zn (Leaves)	Cd (Leaves)
Pb (tuber)	1.0000	0.9574	0.7973	0.4602	0.3355	0.2418
Zn (tuber)		1.0000	0.8385	0.6966	0.5904	0.5054
Cd (tuber)			1.0000	0.5724	0.4367	0.3284
Pb (leaves)				1.0000	0.9873	0.9618
Zn (leaves)					1.0000	0.9931
Cd (leaves)						1.0000

. There were significant positive correlations between the Pb (tuber) and Zn (tuber) at 0.95, Pb (tuber) and Cd (tuber) at 0.79, Zn (tuber) and Cd (tuber) at 0.83, Zn (leaves) and Cd (leaves) at 0.99, Pb (leaves) and Cd (leaves) at 0.96, and Pb (leaves) and Cd (leaves) at 0.98. Strong correlations between the different parts of the sweet potato plants were noted.

In our research, PCA was used to conduct a multidimensional analysis of the influence of the concentration of heavy metals as dependent variables. In Figure 5, PCA explained 98.46% of the total variation, with p1 for 90.71% and p2 for 7.75%. The PCA plot revealed several groups, with six dependent variables distinguishing each group. Point 1 and Field 3 soils were close together because of their higher Zn concentration. The control, Point 2, and Fields 1 and 2 had lower concentrations of HMs. The mine tailings sample was dependent on higher concentrations of Pb and Cd. In the PCA results in Figure 5, the scores for the sweet potato tubers were mainly related to higher concentrations of metals. The results indicated that factors extracted 50.97% from the soils and 49.88% from the sweet potatoes of the total variances. In addition, the loadings showed that Pb (5 cm), Pb (15 cm), Pb (leaves), Zn (leaves), and Cd (leaves) were higher, at 96%, 96%, 92%, 97%, and 99%, respectively.

4. Conclusions

The mine tailings of the former lead factory in Shymkent City represent a serious threat to the surrounding urban environment. In our study, it was determined that soils from adjacent territories were heavily polluted with HMs, with Pb, Zn, and Cd concentrations of 7.76–551.49, 8.25–245.74, and 5.40–19.23 mg/kg, respectively, whereas at the control site (in the city area), the concentrations of Pb, Zn, and Cd were 2.20, 3.70, and 3.18 mg/kg, respectively.

It was found that sweet potato plants accumulated HMs in their aerial and root parts. According to the data obtained, concentrations in the roots (tubers) were higher than those in the aerial parts (leaves). In addition, Pb and Zn concentrations in plants were high, whereas Cd was found only in tubers from Field 3.

According to the contamination coefficients obtained for HM concentrations, the soil in the experimental plots was moderately contaminated. It was found that sweet potato is a hyperaccumulative plant for two heavy metals, Pb and Zn.