1. INTRODUCTION
The release of hexavalent chromium [Cr(VI)] as a soil pollutant is increasing with the expansion of industrial production and metal processing units. Cr is an essential heavy metal having wide industrial uses. The tensile strength and anti-corrosion ability of chromium are beneficial parameters for it being used as an industrial component. The Cr-linked industrial and mining environment has witnessed the presence of Cr(VI) exceeding the threshold limits. Cr(VI) is highly toxic and expresses its toxicity in a wide range of living organisms [1]. The health of crop plants and animal husbandry is not spared from its toxic effects. Moreover, similar to other heavy metals, the persistent nature of Cr(VI) raises the risk of being transferred through the food chain, thereby leading to bioaccumulation [2].
Cr(VI) pollution is intimately connected with the disruption of the biosphere. It is related to the rise in global population and rapid urbanization [3]. Anthropogenic activities like industrialization increase the incidence of soil pollution by Cr(VI). Cr is the seventh-ranked element [4], and the sixth-ranked transition metal based on its abundance. It is available in several oxidation states ranging from 0 to +6; however, the +3 and +6 oxidation states are the two most stable forms [5] found in the soil environment.
Cr(VI) is highly toxic as compared to Cr(III) and imparts toxicity to public health when it exceeds the threshold limits. It has a very rare chance of occurring naturally; however, the formation of Cr(VI) from Cr(III) under oxidizing conditions is a possibility [6]. Cr(III) poses the chances of getting oxidized to Cr(VI) at a high pH of more than 5 [7]. The contamination of soil with Cr(VI) occurs mainly as a result of anthropogenic activities. The deposition of industrial waste is suspected to be a factor responsible for high Cr(VI) in the soil environment [8].
Cr(VI) is highly toxic and imparts more toxic effects on living organisms due to its high solubility in water [9]. It is responsible for occupational disorders and public health issues. In addition, human beings and other living organisms, like animals and plants, are not spared from its lethal effects. It expresses its lethal effects on exposed living organisms and the lethality on public health includes mutagenic, carcinogenic, and teratogenic effects. The cell cycle disturbances and genomic alterations are examples of severity of Cr(VI) toxicity [10].
Pongamia pinnata (L.) Pierre, selected for the present study, is a rapidly growing tree with spreading canopy cover and a commonly available plant in the humid and subtropical environment [11]. It grows in countries across the world like Australia, Bangladesh, China, Egypt, Fiji, India, Indonesia, Japan, Malaysia, Mauritius, Myanmar, Nepal, New Zealand, Pakistan, Philippines, Sri Lanka, Sudan, Thailand, and the United States of America [12] (Fig. 1). The presence of this plant species is also indicated at higher altitudes, even higher than 1,000 m above the sea level. These sites show a wider range of variations in rainfall and soil characteristics. Pollution of the environment due to Cr(VI) is a major concern and needs immediate attention. Biological remediation of Cr(VI)-contaminated soils using plant hyperaccumulators is preferable over other techniques for its eco-friendly approach. The current study aims to utilize P. pinnata (L.) Pierre as a tool for the remediation of Cr(VI)-contaminated soils. The study examines the ability of the plant to accumulate toxic heavy metals like Cr(VI) in its parts like roots, stems, and leaves. Roots being the primary zone of contact of plants with the contaminated soil accumulates metals in its cells. This study works on the elucidation of the impact of Cr(VI) on the structural morphology of plant roots.
2. MATERIALS AND METHODS
2.1. Selection of Target Plant Species
The plant species targeted for this study was selected on the basis of its natural cosmopolitan distribution and high importance value index (IVI). The certified seeds collected for this experiment were germinated in pots filled with soil. The water content of the soil was maintained at three-quarter its water-holding capacity. The plants were watered regularly at an interval of 24 hour. The 45-day-old seedlings were selected randomly for this experimental study.
2.2. Experimental Setup
The experiment was carried out in a randomized block design with the consideration of control plants and Cr(VI)-contaminated soils of 10 different treatment concentrations. The plants in treatment conditions and control were studied in triplicates. Besides control, the soil treatment was carried out using equivalent amounts of potassium dichromate (K2Cr2O7) as the chemical source of Cr(VI). In the 10 different soil Cr(VI) treatment conditions, the concentration of Cr(VI) was maintained between 50 and 500 μg/g with a regular concentration interval of 50 μg/g. Before plantation, each labelled pot was filled with 3 kg of Cr(VI)-treated homogenized soil of desired concentrations. Pots marked as “C” were control and contained soil without Cr(VI). The pots containing Cr(VI)-treated soil were labelled as T1 [50 μg/g Cr(VI)], T2 (100 μg/g), T3 (150 μg/g), T4 (200 μg/g) up to T10 (500 μg/g).
 | Figure 1: Cosmopolitan distribution of P. pinnata (L.) Pierre. [Click here to view] |
2.3. Assessment of Cr(VI) Accumulation in Plant Parts
Cr(VI) accumulation in vital vegetative plant parts like roots, stems, and leaves was evaluated to determine the phytoremedial potential of the plant under varied soil Cr(VI) content. Each plant sample was first cut into pieces and cleaned properly with deionized water to remove any dust and debris. The plant samples were dried at 90°C for 24 hours and then ground into fine powder. The powdered plant samples were acid digested using 0.5 M HNO3 and the Cr(VI) estimation was carried out using atomic absorption spectroscopy, following the standard methodologies of the American Public Health Association [13]. Similarly, the analysis of Cr(VI) content in acidic solution was also conducted by a UV-Vis spectrophotometer as a confirmatory test to determine the Cr(VI) concentration in different plant parts. Cr(VI) was allowed to react with 1,5-diphenylcarbazide to give a characteristic colored complex which was analyzed at 540 nm to determine the Cr(VI) concentration in plant parts.
2.4. Calculation of Biotic Index Values Using P. pinnata( L.) Pierre
The biotic index values like bioconcentration factor (BCF), translocation factor (TF), and bioaccumulation coefficient (BAC) were calculated [14] using P. pinnata (L.) Pierre to estimate the Cr(VI) pollution of the soil as follows:
BCF = CPlant/CSoil
where
CPlant = concentration of Cr(VI) in the plant and
CSoil = concentration of Cr(VI) in the soil [15,16].
TF = CShoots/CRoots
where
CShoots = concentration of Cr(VI) in the shoots or aerial parts of the plant and
CRoots = concentration of Cr(VI) in the roots [17].
BAC = CShoots/CSoil
where
CShoots = concentration of Cr(VI) in the plant shoots, and
CSoil = concentration of Cr(VI) in the soil [18].
2.5. Structural Study of Plant Roots Under Soil Cr(VI) Stress Condition
Plants subjected to various concentrations of soil comprising Cr(VI) were studied for morphological changes occurring in the roots. The roots were observed for phenotypic changes, such as diameter and development of tap root system, when compared to that of the control.
2.6. Physicochemical Analysis of Treated Soil
The physicochemical analysis of the Cr(VI)-treated soil was carried out following standard methodologies. The soil parameters tested were soil pH, soil organic carbon content, and soil residual Cr(VI).
To measure the soil pH, 10 g of soil sample was taken in a 50 ml beaker and mixed thoroughly with 20 ml of deionized water along with continuous stirring for 5 minutes. The suspension was allowed to stand for 1 hour, followed by filtration with Whatman filter paper. The aqueous filtrate was taken for measurement of pH [19].
The soil organic carbon content was analyzed following the methodology of Datta et al. [20]. 1 g of soil sample was taken and added with 10 ml of 1N K2Cr2O7 and 20 ml of concentrated H2SO4 which contained 1.25% of Ag2SO4. The solution mixture was allowed to cool and then centrifuged. The absorbance of the chromous-colored supernatant formed was measured at 660 nm against a blank solution. The percentage of organic carbon was determined from a standard curve prepared using dilutions of glucose.
The residual Cr(VI) in the individual potted soil was measured at the end of the study by spectrophotometric analysis and was compared with the initial treatment provided.
2.7. Statistical Analysis
The data obtained were statistically validated using Statistical Package for the Social Sciences version 21.0 [21] software at probability levels of 0.05 and 0.01.
3. RESULTS AND DISCUSSION
The ability of the plant P. pinnata (L.) Pierre to survive, grow, and hyperaccumulate Cr(VI) in its biomass from the Cr(VI)-contaminated soil up to 200 μg/g soil is a noteworthy outcome of this study. The hyperaccumulation of Cr(VI) in its biomass can increase the residence time of the heavy metal in the living systems. It can reduce the possibility of Cr(VI) availability in free or binding states in the open environment.
The survival and growth of P. pinnata (L.) Pierre seedlings in soil treated with Cr(VI) concentrations >200 μg/g soil and up to 500 μg/g soil, tried during this experiment, indicated a poor response. The trial with the survival and growth of seedlings on soil treated with Cr(VI) concentrations up to 200 μg/g soil and being maintained as control (0 μg/g soil) indicated an insignificant stress-induced response. It may be attributed to the ability of this plant species to resist toxicity, osmotic imbalance, reactive oxygen species, and ionic disturbances caused by the presence of Cr(VI) in the soil strata up to 200 μg/g soil. Hence, it paves the way for the study of the uptake and accumulation of Cr(VI) by P. pinnata (L.) Pierre from the soil treated with Cr(VI). The concentration of Cr(VI) varies from 0 μg/g soil (maintained as control) to 200 μg/g soil in the treated soil of this study.
3.1. Uptake of Cr(VI) and Its Differential Accumulation in Plant Parts
The success behind the use of a plant species as a hyperaccumulator up to a certain extent depends upon its root system development. P. pinnata (L.) Pierre with a well-developed tap root system having lateral roots is advantageous for being selected as an experimental species.
The analysis of variance (ANOVA) values relating to the interactions of Cr(VI) concentration used for soil treatment and mean post-treatment accumulation of Cr(VI) in soil and plant parts of P. pinnata (L.) Pierre are significant at p = 0.05 and 0.01 levels (Table 1).
The ANOVA of the recorded data revealed that significant differences exist in the post-treatment accumulation of Cr(VI) in soil and plant parts of P. pinnata (L.) Pierre under the Cr(VI) soil treatment conditions. The values of accumulation of Cr(VI) in the roots of P. pinnata (L.) Pierre are recorded as 20.444 ± 0.077, 41.422 ± 0.077, 89.822 ± 0.077, and 116.311 ± 0.077 μg/g, with a significant increase in soil Cr(VI) treatment values of 50 μg/g soil (T1), 100 μg/g soil (T2), 150 μg/g soil (T3), and 200 μg/g soil (T4), respectively (Table 1). The short residence time of Cr(VI) on the soil surface makes this element highly mobile. Due to its mobility, it retains a higher probability to be absorbed by the root system of hyperaccumulators [22]. The higher concentration of Cr in the roots is due to its low mobility within the root tissues [23].
The values of accumulation of Cr(VI) in roots of P. pinnata (L.) Pierre is higher when compared to its accumulation in leaves under all the soil Cr(VI) treatment conditions up to 200 μg/g soil; an exception to this is the soil treatment with 50 μg/g soil Cr(VI). In this exceptional condition, Cr(VI) accumulation is more in leaves when compared to roots. This may be due to a high rate of movement of Cr(VI) from roots to leaves using the healthy translocation system of plants under low stress conditions of the soil. The values of accumulation of Cr(VI) in leaves of P. pinnata (L.) Pierre were found to be 24.178 ± 0.077, 35.522 ± 0.077, 60.967 ± 0.077, and 86.767 ± 0.077 μg/g. The accumulation of the toxic metal increased significantly with the increase in soil Cr(VI) treatment values of 50 μg/g (T1), 100 μg/g (T2), 150 μg/g (T3), and 200 μg/g (T4), respectively (Table 1).
The values of accumulation of Cr(VI) in stems of P. pinnata (L.) Pierre is minimum when compared to its accumulation in roots and leaves under all the soil Cr(VI) treatment conditions up to 200 μg/g soil. The values of accumulation of Cr(VI) in the stems of P. pinnata (L.) Pierre are analyzed to be 19.178 ± 0.077, 26.300 ± 0.077, 37.000 ± 0.077, and 45.367 ± 0.077 μg/g. A notable increase in the accumulation of heavy metal in the stem is observed with the increase in soil Cr(VI) treatment values of 50, 100, 150, and 200 μg/g, respectively (Table 1).
The values of residual Cr(VI) in the soil after accumulation by P. pinnata (L.) Pierre is 38.144 ± 0.077, 65.622 ± 0.077, 99.233 ± 0.077, and 148.878 ± 0.077 μg/g, which increased markedly with the increase in soil Cr(VI) treatment values of 50, 100, 150, and 200 μg/g, respectively (Table 1).
The plant P. pinnata (L.) Pierre demonstrated an increase in accumulation of Cr(VI) in its roots, leaves, and stems biomass with the increase in soil Cr(VI) toxicity. It is supported by the findings of Chitraprabha and Sathyavathi [24]. Maximum Cr(VI) accumulation is observed in the roots biomass, followed by its accumulation in the biomass of leaves and stems. The more accumulation of Cr(VI) in roots biomass may be attributed to the accumulation of heavy metal in the root cell vacuoles as a natural defensive mechanism [25,26].
In the present study, increased accumulation of Cr(VI) in plants is observed along with the increment in soil Cr(VI) concentration. Cr(VI) is a toxic and non-essential substance for the plants and hence lacks any specific uptake mechanism. Plant uptake of Cr(VI) is an active mechanism that occurs mostly through anionic carriers like the sulfate and the phosphate carriers. A major part of Cr is mostly retained in the cortex of the plant root [27]. The xylem tissues play a major role in this regard. The xylem tissues not only deposit Cr(VI) in the roots but also translocate the heavy metal through the conducting strands to the aerial parts. Xylem-assisted transfer of Cr(VI) is mostly associated with the involvement of membrane and transport proteins. This may be attributed to the structural similarity of Cr(VI) with that of phosphate or sulfate ions. Once inside the cells, the metals react with specific ligands, thus forming complexes. These complexes are then entrapped inside the cellular vacuoles rendering it less toxic.
 | Table 1: Effect of the variations in soil Cr(VI) treatment on its accumulation in parts of P. pinnata (L.) Pierre. [Click here to view] |
3.2. Correlation Studies
The study of the correlation between the increase in soil Cr(VI) treatment and the accumulation of Cr(VI) in roots, stems, and leaves shows a significantly higher positive correlation with the coefficient of correlation (r) of 0.986, 0.983, and 0.993, respectively (Fig. 2).
A comparatively high r-value between soil Cr(VI) treatment concentration and accumulation of Cr(VI) in leaves is an indication of efficient translocation of toxic Cr(VI) metal from roots to aerial parts of the plant species. It is supported by the observations made in the previous studies. Besides being efficient accumulators of metals, hyperaccumulator plants efficiently carry out metal translocation from the underground parts to the aerial parts of the plants [28]. This supports the use of the targeted plant, P. pinnata (L.) Pierre, as a suitable hyperaccumulator for phytoextraction of Cr(VI) from contaminated industrial and mining soils.
3.3. Estimation of Biotic Index Values to Evaluate The Phytoremedial Ability of P. pinnata (L.) Pierre Under Cr(VI) Stress Conditions
The plant parts were harvested after 180 days of treatment with Cr(VI). Cr(VI) contents in the targeted plant parts were used to calculate the biotic indices such as BCF, TF, and BAC (Fig. 3). In plant T1, treated with 50 μg Cr(VI)/g soil, the TF value is highest, followed by BCF and BAC. The other three treatment conditions, namely T2 [100 μg Cr(VI)/g soil], T3 [150 μg Cr(VI)/g soil], and T4 [200 μg Cr(VI)/g soil], exhibited high BCF, followed by TF and BAC values. The reduction in the TF value of treated plants with a gradual increase in soil Cr(VI) toxicity indicates probable damage of the xylem tissues, thus impairing translocation of the heavy metal from roots to shoots. Under all the treatment conditions, plants exhibited BCF and TF values of more than 1. A high BCF and TF value indicates the suitability of a plant as an hyperaccumulator [29,30]. Plants exhibiting a BCF > 1 and TF < 1 can be used for the phytostabilization of Cr in the soil [31]. In the current study, BCF and TF value > 1 in all the conditions of treatment imply that the plant is not only able to accumulate high Cr(VI) in its root, but is also efficient in translocating the metal to its above ground parts. This strongly supports the suitability of this plant species as a potential hyperaccumulator for phytoremediation of Cr(VI)-contaminated soils.
3.4. Impact of Soil Cr(VI) Treatments on The Morphology of Accumulating Plant Roots
The study of Cr(VI) impact on the root structure plays an important role as it is the channel for the movement of Cr(VI) from contaminated soil to the biomass of the targeted plants for phytoaccumulation. The impact is pronounced more on root morphology when compared to the structure of stems and leaves of P. pinnata (L.) Pierre. The roots of the plants are adversely affected by an elevation in the soil Cr(VI) concentration from 0 μg Cr(VI)/g soil (control) to 200 μg Cr(VI)/g soil at T4. The secondary and tertiary roots are affected with an increase in soil Cr(VI) concentration when compared to the control (C). The roots under increasing soil Cr(VI) toxicity [50 μg Cr(VI)/g soil to 200 μg Cr(VI)/g soil] exhibited a gradual decrease in biomass and structure (Fig. 4). The diameter of primary roots of plants subjected to 50 μg Cr(VI)/g soil (T1) and 100 μg Cr(VI)/g soil (T2) is more when compared to the roots of the plant (T3) subjected to 150 μg Cr(VI)/g soil. The roots of the plant (T4) subjected to 200 μg Cr(VI)/g soil exhibited a sharp decline in its structure and the primary root had a lesser diameter when compared to the roots of the control and other plants under treatment.
This may be due to the damage caused to the root cell structure or inhibition of root cell division [32]. Cr has been found to adversely affect the root parameters like diameter, surface area, and root hair numbers as has been supported by the observations of Ali et al. [33]. The observations are supported by similar results from a recent study of Cr(VI) toxicity on roots of Lepidium sativum [34]. Impaired uptake of water and nutrients from the soil through the damaged root may cause metabolic and survival disturbances in plants [35,36]. Cr(VI)-induced disruption of root cells may be due to the generation of reactive oxygen species [37,38].
3.5. Post-Treatment Analysis of Soil Physicochemical Parameters
The phytoremediation of Cr(VI)-contaminated soil using P. pinnata (L.) Pierre shows variation in soil parameters like pH, organic carbon content, and residual Cr(VI) in all the four treatment conditions (T1, T2, T3, and T4) and control (C). The outcomes of this study were analyzed and post-analysis data are presented in Table 2. The pH is higher in the Cr(VI)-treated soil when compared to the control. The pH of the soil shows a positive relationship with the increasing concentration of Cr(VI), except in case of T4 where it decreased. This may be due to the release of more organic acids to the rhizospheric soil at T4. It is supported by the increase in soil organic carbon percentage from T1 to T4. The organic carbon content is minimum in the control when compared to treatment conditions. It showed an increase in the soil organic carbon percentage with the increase in soil Cr(VI) content. Similar results were obtained by Zhang and Wang [39], suggesting that high amounts of heavy metals like Cr(VI) in the soil could drastically reduce the mineralization of organic carbon present in the soil, thus increasing its percentage. Enya et al. [40] studied the effect of several heavy metals on the soil organic carbon content. They found Cr to have weak inhibitory effects on the soil organic carbon content. The group found organic carbon content in the soil to be lower in the control when compared to the treatments. Another probable reason for the increase in soil organic carbon with an increase in soil Cr(VI) treatment may be the complex formation between the heavy metal and the organic matter [41].
 | Figure 2: Correlation between soil Cr(VI) concentration and mean Cr(VI) accumulation in the (a) root, (b) stem, and (c) leaf biomass (Significant at p = 0.05 and 0.01 levels). [Click here to view] |
 | Figure 3: Biotic index values of P. pinnata (L.) Pierre under Cr(VI) soil stress conditions [T1: plant with soil Cr(VI) treatment of 50 μg g−1, T2: plant with soil Cr(VI) treatment of 100 μg g−1, T3: plant with soil Cr(VI) treatment of 150 μg g−1, and T4: plant with soil Cr(VI) treatment of 200 μg g−1]. [Click here to view] |
 | Figure 4: Effect of Cr(VI) toxicity on the structure of roots of P. pinnata (L.) Pierre [C: control plant, T1: plant with soil Cr(VI) treatment of 50 μg g−1, T2: plant with soil Cr(VI) treatment of 100 μg g−1, T3: plant with soil Cr(VI) treatment of 150 μg g−1, and T4: plant with soil Cr(VI) treatment of 200 μg g−1]. [Click here to view] |
 | Table 2: Analysis of post-treatment soil physicochemical parameters (after 180 days of treatment). [Click here to view] |
4. CONCLUSION
The results of this study are in favor of treating the plant P. pinnata (L.) Pierre as a suitable species for the remediation of soil under Cr(VI) stress up to 200 μg/g. The accumulation of Cr(VI) is more in roots of this plant species when compared to the stems and leaves, during its growth in soil contaminated with Cr(VI) ranging between 100 μg/g and 200 μg/g. The differential accumulation of Cr(VI) in plant parts of P. pinnata (L.) Pierre is highly significant at p = 0.05 and p = 0.01 levels. The mean Cr(VI) bioaccumulation in roots, stems, and leaves shows a high positive correlation with the soil Cr(VI) concentration. The targeted plant species, P. pinnata (L.) Pierre, is a possible tool for the phytoremediation of Cr(VI)-contaminated soils of industrial and mining areas.
5. ACKNOWLEDGEMENT
The authors acknowledge the support provided by Siksha 'O' Anusandhan (Deemed to be University) during the course of this research.
6. AUTHOR CONTRIBUTIONS
All authors made substantial contributions to conception and design, acquisition of data, or analysis and interpretation of data; took part in drafting the article or revising it critically for important intellectual content; agreed to submit to the current journal; gave final approval of the version to be published; and agree to be accountable for all aspects of the work. All the authors are eligible to be an author as per the international committee of medical journal editors (ICMJE) requirements/guidelines.
7. CONFLICTS OF INTEREST
The authors report no financial or any other conflicts of interest in this work.
8. ETHICAL APPROVALS
This study does not involve experiments on animals or human subjects.
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