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Article

Differential Response of Brassica Cultivars to Potentially Toxic Elements and Their Distribution in Different Plant Parts Irrigated with Metal-Contaminated Water

by
Saad Dahlawi
1,
Muhammad Sadiq
2,
Muhammad Sabir
2,*,
Zia Ur Rahman Farooqi
2,
Saifullah
2,
Ayesha Abdul Qadir
2 and
Turki Kh Faraj
3
1
Department of Environmental Health, College of Public Health, Imam Abdulrahman Bin Faisal University (IAU), P.O. Box 1982, Dammam 31441, Saudi Arabia
2
Institute of Soil and Environmental Sciences, University of Agriculture, Faisalabad 38040, Pakistan
3
Department of Soil Science, College of Food and Agriculture Sciences, King Saud University, P.O. Box 145111, Riyadh 11362, Saudi Arabia
*
Author to whom correspondence should be addressed.
Sustainability 2023, 15(3), 1966; https://doi.org/10.3390/su15031966
Submission received: 6 December 2022 / Revised: 3 January 2023 / Accepted: 10 January 2023 / Published: 19 January 2023
Browse Figures
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Abstract

:
The increasing concentration of potentially toxic elements (PTEs) in agricultural soils has greatly disturbed the quality and productivity of soils. In this study, we investigated the uptake and distribution of cadmium (Cd), lead (Pb), and nickel (Ni) by two Brassica cultivars (Khanpur raya and Sandal canola) grown on soil irrigated with metal-contaminated water. Distilled water was spiked with salts to prepare irrigation water with various levels of metals (Ni application at 90, Cd at 20, Pb at 500, Ni + Pb at 20 + 500, Ni + Cd at 90 + 20, Cd + Pb at 20 + 500, and Ni + Cd + Pb at 90 + 20 + 500 mg L−1). These treatments were compared with water without the addition of any salt. The results indicated that compared to the control treatment, increasing metal concentrations decreased the shoot weight (44.25%, 29.03%), root length (33.33%, 12.74%), and shoot length (19.73%, 11.06%) in Khanpur raya and Sandal canola, respectively. Compared to the control treatment, irrigation with contaminated water decreased the photosynthesis rate (98.42%, 99.34%), chlorophyll content (18.27%, 13.73%), respiration rate (7.97%, 6.47%), and transpiration rate (9.90%, 33.33%) in both varieties, respectively. Notably, the concentrations of Ni (0.01 and 0.003), Cd (0.01 and 0.012), and Pb (0.03 and 0.05%) in the seeds were increased, as well as in Khanpur raya and Sandal canola, respectively, compared to the controls. Furthermore, the PTE accumulation in different components was recorded, with the order of soil > root > shoot > seed. It was observed that brassica cultivars differed significantly in their response to the growth and accumulation of PTEs in edible parts. It was concluded that Khanpur raya did not exhibit a decline in growth due to PTEs in irrigation water and prevented the translocation of PTEs towards edible parts compared to Sandal canola and thus can be safely grown in soils receiving PTE-contaminated water.

1. Introduction

Shortages of good quality irrigation water in arid/semi-arid regions are prompting the use of raw city effluent for irrigating crops, especially in peri-urban areas that supply a large proportion of vegetables and fodder to urban dwellers. The high amounts of plant nutrients in raw city effluent and its continued supply are important factors necessitating its use for irrigation purposes in peri-urban areas [1]. However, raw city effluent contains potentially toxic elements (PTEs), viz. cadmium (Cd), nickel (Ni), mercury (Hg), copper (Cu), manganese (Mn), zinc (Zn), and lead (Pb), which are causing serious threats to public and ecosystem health [2]. Potentially toxic elements particularly Cd, Ni, and Pb are abundant in raw city effluent due to the mixing of industrial wastewater with raw city effluent. While PTEs are naturally present in soils, the continuous irrigation of soils with raw city effluent results in the accumulation of PTEs in such soils [3]. The dynamics of PTEs in the water–soil–plant continuum lead to the potential threat of food chain contamination, which has human and ecosystem health implications. PTE accumulation in soils can lead to the contamination of surface and sub-surface water resources through run-off and leaching, respectively, thereby threatening public and ecosystem health [2]. The absorption of PTEs by growing crops and vegetables irrigated with PTE-contaminated raw city effluent is a key cause of contamination to the food chain, causing serious health consequences in humans [2]. Different mechanisms are adopted by different plants to absorb, translocate, and distribute PTEs within the plant body, and the study of these is of great importance in determining their environmental fate and potential health risks [4].
With increasing awareness about food quality, PTE contamination is now considered an important, primary indicator of food quality [5]. The ingestion of PTE-contaminated food by humans causes serious health hazards due to its depletion of certain essential elements, leading to the impairment of immunological defenses, the failure or retardation of intrauterine growth, psychosocial disorders, and the occurrence of upper gastrointestinal cancer [6]. PTEs can build up in the body’s essential organs, leading to a variety of severe medical conditions, including the infamous itai-itai sickness [7].
Researchers have used different indices to study the level of health risks posed by PTEs accumulated in plants due to contaminated irrigation water. In agricultural practices, the evaluation of the soil enrichment of trace metals can be carried out by using the pollution load index (PLI), which measures the number of times in which metals in a soil surpass the critical level, providing a summative sign of the general level of metal harmfulness in a specific sample [8].
Brassica is a hyper-accumulator crop used for the phytoremediation of PTE-contaminated soil. The elements which have potentially hazardous effects on crops and human health include Pb, Cd, Zn, and Ni [9]. For the remediation of PTEs, the use of mustard (Brassica juncea) species is one of the many possible options for cleaning PTE-contaminated soils. Different cultivars were grown to identify tolerant cultivars capable of growing with PTE-contaminated raw city effluent. Depending upon the species, Brassica can produce high biomass under a variety of climatic and growing circumstances, allowing for significant PTE uptake, removal, and/or accumulation. Through a variety of processes, such as the activation of the antioxidant defense system, chelation, the compartmentation of Cd into metabolically inactive regions, the accumulation of total amino acids, and osmo-protectants, several crop species can withstand PTE stress [10]. In this study, we applied PTE-contaminated (Cd, Ni, and Pb) water to two brassica cultivars to study their differential growth responses, the distribution of PTEs in the different plant parts, and the accumulation of PTEs in the soil. These PTEs were selected due to their presence in raw city effluent.

2. Materials and Methods

2.1. Soil Collection, Preparation, and Analysis

The soil was collected in bulk from the agricultural field that had not received metal-contaminated water or amendment previously. The soil was air-dried, crushed, and passed through a 2-mm sieve to remove extraneous material. Physico-chemical properties of soil were determined using standard methods, i.e., EC and pH were measured using EC and pH meters (Hanna HI-83141 and Lovibond SensoDirect con200) after their calibration [11], soil organic matter was determined using the Walkley and Black Method [12], and soluble anion and cations were determined using the methods described by US Salinity Lab Staff [11] (Table 1).

2.2. Spiking of Irrigation Water with Potentially Toxic Elements

Cadmium chloride, nickel nitrate, and lead nitrate (Analytical grade) were used as sources for Cd, Ni, and Pb, respectively. These salts were dissolved in distilled water to prepare the required concentrations of Cd (20 mg L−1), Ni (90 mg L−1), and Pb (500 mg L−1). These levels were selected on the basis of threshold levels of these metals in irrigation water. After their preparation, these solutions were applied to Brassica cultivars through irrigation water in splits.

2.3. Treatment Setup and Crop Husbandry

Brassica cultivars (Khanpur raya and Sandal canola) were grown in pots filled with 5 kg soil, with three replications being performed. The experimental pots were arranged according to a completely randomized design (Table 2). Treatments were T0 (un-amended control), T1 (Ni 90 mg L−1), T2 (Cd 20 mg L−1), T3 (Pb 500 mg L−1), and their combination, i.e., T4 (Ni + Pb), T5 (Ni + Cd), T6 (Cd + Pb), T7 (Cd + Pb + Ni). A total of 68 pots (2 cultivars × 8 treatments × 3 replications) were placed in the middle of a glasshouse according to a completely randomized arrangement in which all the pots received equal sunlight. Seed sowing in these filled pots was accomplished and recommended doses of NPK (60:60:40 kg ha−1) were applied using urea, di-ammonium phosphate (DAP), and sulfate of potash (SOP), respectively. After germination, four seedlings per pot were maintained. The irrigations were applied at regular intervals, and appropriate plant protection measures were followed. After two months, two plants from each pot were harvested, and their fresh and dry weights were recorded. At harvest, data regarding agronomic, chemical, and physiological parameters were recorded.

2.4. Recording of Crop Physiological Attributes

A chlorophyll meter (SPAD-502 Plus) was used to measure the SPAD values of healthy, fully expanded leaves. The second leaf of each treatment was selected. Data were recorded from three different points of each leaf by placing the leaf on the sensor of a meter, and the average was calculated. Transpiration, photosynthesis, and respiration rates were determined using Infrared Gas Analyzer (IRGA, LCA-4, Analytical Development, Hoddesdon, UK).

2.5. Determination of Potentially Toxic Element Concentrations in Soil and Plant Samples

Root, shoot, and seed samples were digested using HNO3 and HClO4. Conical flasks containing 0.5 g plant samples were taken, and 10 mL of a mixture of 70% HNO3 and 65% HClO4 (5:1) was added to samples for digestion at 150 °C until the clear material was obtained. The final volume of digested samples was increased to 25 mL using distilled water. After filtration, the dilution of digested transparent samples was carried out and analyzed using a flame atomic absorption spectrophotometer (Solaar S-100, CiSA).
For PTE determination in soil, 10 g air-dried soil samples in 100 mL volumetric tubes were taken. A 20 mL extracting reagent AB-DTPA (Ammonium bicarbonate Diethylene-triamine Acetic Acid) was added to the samples. After 5 min of shaking, the samples were filtered, and the filtrates were collected. Potentially toxic elements were determined from filtrates using an atomic absorption spectrophotometer.

2.6. Calculation of Translocation and Bioaccumulation Factors

The translocation factors (TF) for PTEs were calculated using Equation (1) [13]:
TF = Cs/Cr
where Cs and Cr are the metal concentrations (µg kg−1) in the shoot and roots, respectively. A TF > 1 indicates that the plant translocated PTEs effectively from root to shoot.
The bioaccumulation factors (BAF) for PTEs were calculated using Equation (2) [13]:
BAF = Cplant/Csoil
where Csoil and Cplant are the metal concentrations (μg kg−1) in the soil and plant, respectively.
The enrichment factor (EF) was calculated using the following formula (Equation (3)):
EF = (C_n/C_ref)/(B_n/B_ref)
where Cn and Bn are the concentration of metals in soil and the concentration of reference PTE in soil (mg kg−1), respectively. Cref and Bref are PTE concentration in the earth’s crust and concentration of reference metal in the earth’s crust (mg kg−1), respectively.
The pollution load index was calculated using Equation (4):
PLI = √(n & CF1 × CF2 × CF3 × … × 〖CF〗_n
where CF is the contamination factor and n is the number of PTEs.

2.7. Statistical Analysis

Two-way analysis of variance (ANOVA) was used to analyze the recorded data using the Statistix (v8.1) software. The Least Significant Difference (LSD) test was applied for the comparison of means.

3. Results

3.1. Agronomic Parameters

3.1.1. Shoot Fresh and Dry Weight (First Harvest)

For the shoot fresh and dry weight (SFW and SDW), a significant (p < 0.05) main effect of the varieties on the SFW was found, but a non-significant effect of the treatments and their interactions was also found. The SFW of Sandal canola ranged between 6.66 and 9.33 g plant−1. The maximum SFW (9.33 mg plant−1) was recorded for the control, while the minimum SFW was recorded for T7 (6.66 g plant−1 or 29.03% less than the respective control (Figure 1a). The SDW of Khanpur raya ranged between 2.83 and 5.33 g plant−1, while 2.50–4.33 g plant−1 was recorded for sandal canola. The SFW of Khanpur raya ranged between 6.33 and 11.33 g plant−1. The maximum SFW (11.33 g plant−1) was recorded for the control, while the minimum SFW was recorded for T7 (6.33 g plant-1 or 44.25% less than the respective control). The maximum SDW values (5.33 and 4.33 mg plant−1) were recorded for the controls of both varieties, while the minimum SDW values were recorded for T7 (2.83 and 2.50 g plant−1), showing 47.17 and 41.86% (2.5 g) less than their respective controls. Therefore, it can be concluded that Khanpur raya produced better SFW and SDW values than sandal canola up to the first harvest, and there was a gradual decrease in the SFW and SDW values with the increases in the Ni, Cd, and Pb concentrations (Figure 1a).

3.1.2. Shoot Fresh and Dry Weight (Second Harvest)

The SFW and SDW values of the second harvest are given in Figure 1b. There was a significant (p < 0.05) main effect of the varieties on the SFW but a non-significant effect of the treatments and their interactions. The SFW values of Khanpur raya and Sandal canola ranged between 24.33 and 37.33 and 30.16 and 50.66 g plant−1, respectively. The maximum SFW values (50.66 and 37.33 mg plant−1) were recorded for the control, while the minimum SFW values were recorded for T7 (24.33 and 30.16 g plant−1 or 34.85 and 40.51% less than their respective controls). The varieties had a non-significant main effect on the SDW, but the treatments and their interactions had a significant effect. The SDW values of Khanpur raya and sandal canola ranged between 14 and 17.16 and 8.33 and 20.66 g plant−1, with the maximum SDW values (17.16 and 20.66 mg plant−1) obtained for the controls and the minimum for T7 (14 and 8.33 g plant−1). The application of metals decreased the SDW values of both varieties by up to 18.41 and 59.68% less than their respective controls. Therefore, it can be concluded that Khanpur raya showed better performance than Sandal canola.

3.1.3. Shoot Length

The data regarding the shoot length are given in Figure 1c. There was a significant (p < 0.05) main effect of the varieties and treatments and their interactions on the shoot length. The shoot length values of Khanpur raya and Sandal canola ranged between (80 and 99.66 and 71.0 and 79.83 cm). The maximum shoot length (99.66 vs. 79.83 cm) was obtained for the control and the minimum for T7 (80 vs. 71.0 cm), which were 19.73 and 11.06% less, respectively, than their respective controls.

3.1.4. Root Length and Fresh and Dry Weight

There was a significant (p < 0.05) main effect of the varieties, treatments, and their interactions on the root fresh and dry weight (RFW and RDW) (Figure 2a). The RFW values of Khanpur raya and Sandal canola ranged between 6.45 and 13.50 and 9.01 and 19.63 g, with the maximum value obtained for the control and the minimum for T7 for both varieties, which were 52.22 and 54.10% less, respectively, than their respective controls. The RDW values of Khanpur raya and Sandal canola ranged between 4.42 and 7.14 and 2.11 and 5.16, respectively, indicating that the maximum production was obtained for the control and the minimum for T7. The maximum decrease in RDW was recorded at 38.10% for Khanpur raya and 59.11% for Sandal canola when compared with their respective controls (Figure 2a).
The data regarding the root length is given in Figure 2b. There was a significant (p < 0.05) main effect of the varieties on the root length but a non-significant effect of the treatments and their interactions. The root length values of Khanpur raya and Sandal canola ranged between 8.92 and 13.38 and 9.45 and 10.83 cm, respectively. The maximum root length was recorded for the control, while the minimum root length was recorded for T7 for both varieties, which were 33.33 and 12.74% less, respectively, than their respective controls.

3.2. Physiological Parameters

3.2.1. Chlorophyll Content (SPAD)

The data regarding the chlorophyll content are given in Figure 3. There was a significant (p < 0.05) main effect of the varieties and treatments on the chlorophyll content but a non-significant effect of the treatments’ interactions. The SPAD values of Khanpur raya and Sandal canola ranged between 30.16 and 36.90 and 37.06 and 42.96, respectively, with the maximum SPAD values of 36.90 and 42.96 obtained for the control and the minimum (30.16 and 37.06) for T7, which were 30.16 and 13.73% less, respectively, compared to their respective controls (Figure 3a).

3.2.2. Photosynthetic Rate

The photosynthesis rate (Ph) values are given in Figure 3b. There was a significant (p < 0.05) main effect of the varieties and treatments on the Ph, but a non-significant effect of the treatments’ interactions. The Ph values of Khanpur raya and Sandal canola ranged between (0.36 and 5.68 and 0.02 and 3.01 plant-1), with the maximum values obtained for the control and the minimum for T7. These were 98.42 and 99.34% less, respectively, compared to their respective controls.

3.2.3. Respiration Rate

The data regarding the respiration rate is given in Figure 3c. There was a non-significant main effect of the varieties, treatments, and the treatments’ interactions on the respiration rate. The respiration rate values of Khanpur raya and Sandal canola ranged between (169.60 and 184.27 and 168.70 and 180.37 µmol CO2 hr−1), with the maximum respiration rate obtained for the controls and the minimum for T7, which were 7.93 and 6.47% less, respectively, compared to their respective controls.

3.2.4. Transpiration Rate

The data regarding the transpiration rate is given in Figure 3d. The transpiration rate values of Khanpur raya and Sandal canola ranged between (33.66 and 37.36 and 22.0 and 33.0), with the maximum values (37.36 and 33.0) obtained for the controls and the minimum (33.66 and 33.0) for T7, which were 9.92 and 33.33% less, respectively, than their respective controls.

3.3. Chemical Parameters

3.3.1. Ni Concentrations in Roots, Shoots, and Seeds

The data regarding the nickel (Ni) concentration in the roots, shoots, and seeds are given in Figure 4. There was a significant (p < 0.05) main effect of the treatments, varieties, and their interactions on Ni accumulation in the plant tissues. The maximum Ni concentrations were recorded for T7, while the minimum was recorded for the control (0.0021 mg kg−1) for both varieties. There was up to 5.30 and 5.99% more Ni in the roots and shoots compared to the controls for Khanpur raya, and 18.27 and 13.73% more Ni in the seeds of T7 compared to the control for Sandal canola.

3.3.2. Cd Concentrations in Roots, Shoots, and Seeds

The data on the cadmium (Cd) concentrations in the roots, shoots, and seeds are presented in Figure 5. The maximum Cd concentrations in the roots were found for T7, which surpassed the control by 9.90 and 13.45%, the maximum concentrations in the shoots were found for T5, which surpassed the control by 326.09 and 258.80%, and the maximum concentrations in the seeds were found for T3, which surpassed the control by 95 and 93%.

3.3.3. Pb concentrations in Roots, Shoots, and Seeds

The data regarding the lead (Pb) concentrations in the roots, shoots, and seeds are presented in Figure 6. The Pb values of the plant tissues of Khanpur raya and Sandal canola surpassed the control values by 10- and 2.3-fold in the roots of T3, 37- and 85-fold in the shoots of T7, and 8-fold each in T7 and T3.

3.3.4. Ni, Cd, and Pb Concentrations (mg kg−1) in soil

The Ni, Cd, and Pb concentrations in the soil are given in Figure 7. In the soil where Khanpur raya and Sandal canola were grown, the Ni concentrations were 9.90 and 33.33% more for T7, the Cd concentrations were 70.83 and 66.10% more for T2, and the Pb concentrations were 22- and 13-fold more for T7 compared to their respective control treatments.

3.3.5. Soil Quality and Contamination Indices

Bioaccumulation in plants is the process whereby PTEs from the surrounding environment are accumulated within the plant tissues. It is calculated as the ratio of the studied PTE concentration in the root tissues of the plant to the PTE concentration in the source, i.e., the water or soil. As presented in Table 3, the maximum TF values of Ni for the applied treatments were 685 and 139 for Khanpur raya and Sandal canola, respectively. Further, the maximum TF values of Cd were 1.48 and 44.20, and the maximum TF values of Pb were 2.88 and 1045 for Khanpur raya and Sandal canola, respectively. The maximum BAF values of Ni, Cd, and Pb were 21.41 and 3.17, 2.0 and 3.64, and 3.34 and 2.0, respectively, for Khanpur raya and Sandal canola, respectively. The maximum EF values of Ni, Cd, and Pb were 0.06, 0.60, and 0.06 for Khanpur raya, respectively, while they were 0.05, 0.27, and 0.03 for Sandal canola, respectively (Table 3).

3.3.6. Correlation Analysis

Correlation analysis (Figure 8) showed that the plant growth, plant yield, and heavy metal concentrations in the roots, shoot, grains, and soil were significantly correlated with each other. The dry matter and PTE concentrations were negatively correlated. However, a negative but significant association was found between the PTE concentrations and plant growth and physiological parameters. There was a highly significant positive association between the PTE translocation in the roots and shoots but a non-significant correlation between the PTEs in the seeds (Figure 8).

4. Discussion

4.1. Plant Growth, Plant Yield, and Physiological Attributes

The plant growth and yield attributes were significantly decreased in the pots receiving contaminated water compared to the control (Figure 1 and Figure 2). The results reported in this study are in agreement with already published data [14,15,16] reporting that plant growth and biomass decreased under PTE-amended treatments due to their induction of stress in plants. These results are thus in agreement with Sheetal et al. [17], who also reported a 20% reduction in the shoot biomass of Brassica Juncea L. under Cd stress. A decrease in biomass production due to PTEs was also reported by Bhardwaj et al. [18], who found an up to 82% decline in plant dry matter due to applied Cd. The reasons behind this reduction in plant biomass were the decreased plant metabolism and the production of reactive oxygen species (ROS) [19].
Similarly, in this study, the exposure of Brassica campestris species to PTEs significantly reduced their fresh root and dry weights compared to controls. Lugon-Moulin et al. [20] reported an up to 60% decrease in root dry matter production after the application of PTEs. Similar results were obtained by Ha et al. [21], who concluded that Cd application decreased tobacco plant growth due to disruption to the plant’s nutrient uptake. Further, plant physiological processes have been found to be impacted due to disruption to Zn transporters by Cd accumulation, disruption to nutrient homeostasis, DNA, and membrane damage, which leads to reduced plant growth [22]. In the present study, there was an up to 33% reduction in the root lengths of Brassica campestris species. These results were similar to those of Cornu et al. [23], who reported a reduction in the root lengths of sunflower under 50–100 μM Cd stress and a 20% reduction in their root dry biomass. These reductions may take place due to the sequestration of PTEs in a plant’s roots, indicating the remediation and accumulation mechanism is involved, as seen in this study for Brassica campestris L. Increased PTE stress has been linked to short, thick, and twisted roots, as well as fewer lateral roots and apparent root deformity [24]. Because the cells at taproot development sites are so sensitive to contaminants, PTE stress may prevent root cell division, resulting in fewer secondary roots [25]. As a result, it can cause significant changes in root length and growth, as depicted in our findings, which showed reduced root lengths [26,27].

4.2. Physiological Parameters

Plant physiology is severely affected by external stress factors such as PTEs and PTEs containing water. Chlorophyll is a green pigment found in plants that helps in photosynthesis. In this study, the T7 treatment resulted in the maximum reduction (30%) in the chlorophyll content in the leaves of Brassica campestris L. (Figure 2a). PTEs may accumulate in mesophyll cell walls, limiting chlorophyll production in rape leaves. Exogenous stress factors such as PTEs have been found to alter chlorophyll content and plant growth [28]. Similar results were obtained in this study, where chlorophyll content decreased due to the application of PTE-contaminated water. Khan and Bano [29] found that 0.12 mg kg−1 Cd in ryegrass (Lolium multiflorum L.) reduced its chlorophyll content by up to 50%. Similar results were also found by Ebbs and Uchil [30] for Brassica napus, where relative to a control, the application of Cd (20 mg kg−1) significantly reduced its chlorophyll content and several other growth parameters. In the present study, the maximum chlorophyll content (42.93) was found in the control treatment of Sandal canola. This was due to the non-application of stressing factors to this treatment, i.e., PTEs [31]. The higher SPAD value obtained for this treatment may also have been due to the effect of the leaf thickness or specific leaf weight and the accumulation of more chlorophyll content [32].
In this study, the chlorophyll content decreased in the Brassica campestris species studied, which also caused reduced photosynthetic activity. These results resemble those of the study of Jiang et al. [33]. The possible mechanism underlying this phenomenon is that PTE application alters the normal structure of the catalytic enzymes of chlorophyll production and damages intercellular membranes [34]. A number of researchers have reported that PTEs combined with nucleic acids, proteins, and enzymes cause the inhibition of respiration, metabolism, photosynthetic activity, and cell division [35,36]. In this study, along with the maximum chlorophyll content and photosynthetic activity values, the maximum respiration rate was obtained for the control rather than the PTE-applied treatments. This was due to the PTE-induced toxicity in the latter treatments, which caused a mechanism that altered mineral nutrient uptake in the samples in these groups. PTE-induced toxicity has also been found to severely affect root morphology and growth, causing oxidative stress in vegetables by producing ROS, which damaged the antioxidant enzyme system, affecting the respiration and transpiration rates of the plants [37].

4.3. Ni, Cd, and Pb Contents in Soil and Plant Tissues

In this study, the postharvest soil and plant tissue PTE concentrations showed significant differences compared to the controls. PTE uptake by plants depend on the concentration and solubility of the PTE present in soil. Predominantly, PTEs are transported from roots to shoots and then to leaves and edible parts through xylem vessels during transpiration flow. Further, PTEs are highly mobile naturally and can be translocated from the older to younger leaves of a plant [38].
In this study, metal concentrations in the roots, shoots, and seeds increased with exogenous PTE application (Figure 4, Figure 5, Figure 6 and Figure 7). However, PTE concentrations significantly decreased in the seeds, while the maximum PTE accumulations were in the roots and shoots, as indicated by the translocation and bioaccumulation factors (Table 3). A previous study on wheat seedlings also reported the accelerated translocation of PTEs to shoots when they were applied in excess [39]. Similar results were also reported by He et al. [40] for Mn uptake by Macleaya cordata and concluded that accumulation followed the trend leaf > root > stem, and transport efficiency decreased with the increase of Mn concentration.

4.4. Phytoremediation and Soil Metal Quality Indices

Among the PTEs, the maximum BAF value was obtained for Pb in Khanpur raya, while the lowest was obtained for the control and Cd treatment for Khanpur raya. The food chain (environment–plant–human) is mainly known as one of the major pathways for the exposure of humans to environmental contaminants. Environment-to-plant transfer is one of the key processes of human exposure to toxic heavy metals through the food chain [41]. According to Takarina and Pin [42], when CF < 1 or BAF = 1, this denotes that a plant only absorbs PTEs; the PTEs are not accumulated. When BCF > 1, this indicates that the plant effectively accumulates the PTEs. In the present study, among the estimated PTEs, the maximum enrichment was found for Cd in Khanpur raya. According to a previous study [43], EF values greater than 1 indicate the higher availability and distribution of PTEs in contaminated soils, subsequently increasing PTE accumulation in plant species. Therefore, we propose that Khanpur raya could be considered an accumulator or hyper-accumulator for phytoremediation, since it generally recorded in this study higher metal concentrations in its shoot tissues rather than in its root tissues. The same plant variety’s TF values were also high, indicating effective PTE translocation took place from its roots to its shoots.

5. Conclusions

The results of this study indicate that irrigation with metal-contaminated water may increase the levels of PTEs in plants. It can be concluded that Khanpur raya performed the best in the study due to the fact that (1) its growth was not hampered due to the presence of metals in water; thus, it can be considered to be tolerant to high levels of PTEs; (2) it accumulated large amounts of metals in its non-edible parts, thus suggesting that it can be grown safely in soils receiving contaminated irrigation water. Further field studies are needed to confirm the ability of this cultivar to be a good candidate for contaminated soils and water.

Author Contributions

Conceptualization, S.; Methodology, A.A.Q.; Formal analysis, Z.U.R.F.; Resources, S.D. and T.K.F.; Data curation, M.S. (Muhammad Sadiq); Writing—review & editing, M.S. (Muhammad Sabir). All authors have read and agreed to the published version of the manuscript.

Funding

We extend our appreciation to the Researchers Supporting Project at King Saud University, Riyadh, Saudi Arabia, for funding this research project, (Fund no. RSP2023R487).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data is contained within the article.

Conflicts of Interest

The authors declare no conflict of interest.

References

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Figure 1. Effect of applied treatments on (a) shoot fresh and dry weight of canola varieties after two months harvest, (b) shoot fresh and dry weight after harvest, and (c) shoot length. Error bars show the standard error of three replications. Different letters show levels of significance at p < 0.05.
Figure 1. Effect of applied treatments on (a) shoot fresh and dry weight of canola varieties after two months harvest, (b) shoot fresh and dry weight after harvest, and (c) shoot length. Error bars show the standard error of three replications. Different letters show levels of significance at p < 0.05.
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Figure 2. Effect of applied treatments on (a) root fresh and dry weight and (b) root length of canola varieties. Error bars show the standard error of three replications. Different letters show levels of significance at p < 0.05.
Figure 2. Effect of applied treatments on (a) root fresh and dry weight and (b) root length of canola varieties. Error bars show the standard error of three replications. Different letters show levels of significance at p < 0.05.
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Figure 3. Effect of applied treatments on (a) chlorophyll content, (b) photosynthesis rate, (c) respiration rate, and (d) transpiration rate of canola varieties. Error bars show the standard error of three replications. Different letters show levels of significance at p < 0.05.
Figure 3. Effect of applied treatments on (a) chlorophyll content, (b) photosynthesis rate, (c) respiration rate, and (d) transpiration rate of canola varieties. Error bars show the standard error of three replications. Different letters show levels of significance at p < 0.05.
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Figure 4. Effect of different treatments on Ni accumulation in (a) roots, (b) shoots, and (c) seed of canola varieties. Error bars show the standard error of three replications. Different letters show levels of significance at p < 0.05.
Figure 4. Effect of different treatments on Ni accumulation in (a) roots, (b) shoots, and (c) seed of canola varieties. Error bars show the standard error of three replications. Different letters show levels of significance at p < 0.05.
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Figure 5. Effect of different treatments on Cd accumulation in (a) roots, (b) shoots, and (c) seed of canola varieties. Error bars show the standard error of three replications. Different letters show levels of significance at p < 0.05.
Figure 5. Effect of different treatments on Cd accumulation in (a) roots, (b) shoots, and (c) seed of canola varieties. Error bars show the standard error of three replications. Different letters show levels of significance at p < 0.05.
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Figure 6. Effect of different treatments on Pb accumulation in (a) roots, (b) shoots, and (c) seed of canola varieties. Error bars show standard error of three replication. Different letters show level of significance at p < 0.05.
Figure 6. Effect of different treatments on Pb accumulation in (a) roots, (b) shoots, and (c) seed of canola varieties. Error bars show standard error of three replication. Different letters show level of significance at p < 0.05.
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Figure 7. Effect of different treatments on (a) Ni, (b) Cd, and (c) Pb concentration in soil under two different canola varieties. Error bars show the standard error of three replications. Different letters show levels of significance at p < 0.05.
Figure 7. Effect of different treatments on (a) Ni, (b) Cd, and (c) Pb concentration in soil under two different canola varieties. Error bars show the standard error of three replications. Different letters show levels of significance at p < 0.05.
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Figure 8. Correlation between the studied parameters and the applied treatments. Values with steric are statistically significant at p < 0.05.
Figure 8. Correlation between the studied parameters and the applied treatments. Values with steric are statistically significant at p < 0.05.
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Table
Table 1. Physico-chemical properties of experimental soil.
Table 1. Physico-chemical properties of experimental soil.
Soil PropertiesUnitsValues
soil texture-Sandy Clay loam
Sand%61.01
Silt%18.70
Clay%20.29
Saturation percentage (SP)%32.50
pHs-7.30
EcedS m−13.42
TSSmmolcL−134.2
CO32−mmolcL−11.00
HCO3−mmolcL−17.20
Cl-mmolcL−113.0
Ca2++Mg2+mmolcL−123.0
SO42−mmolcL−114.0
Na+mmolcL−112.2
SAR(mmolcL−1)1/212.0
Table
Table 2. Treatment plan and salts used for the PTE treatments for experiments.
Table 2. Treatment plan and salts used for the PTE treatments for experiments.
SymbolDescription
T0Control
T1Ni (Nickel nitrate) 90 mg kg−1
T2Cd (Cadmium chloride) 20 mg kg−1
T3Pb (Lead nitrate) 500 mg kg−1
T4Ni + Pb (90 + 500) mg kg−1
T5Ni + Cd (90 + 20) mg kg−1
T6Cd + Pb (20 + 500) mg kg−1
T7Cd + Pb + Ni (20 + 500 + 90) mg kg−1
Table
Table 3. Translocation and bioaccumulation factors of Ni, Cd, and Pb in applied treatments.
Table 3. Translocation and bioaccumulation factors of Ni, Cd, and Pb in applied treatments.
TF
TreatmentsKhanpur RayaSandal Canola
NiCdPbNiCdPb
Control11.000.750.003.671.330.00
Ni0.751.462.890.990.331.07
Cd684.830.184.520.020.031.04
Pb0.521.000.15139.050.030.24
Ni + Pb2.290.001.850.431.181.64
Ni + Cd0.860.574.650.661.430.08
Cd + Pb0.681.480.970.001.201.98
Ni + Cd + Pb3.840.031.580.7044.200.99
BAF
TreatmentsKhanpur RayaSandal Canola
NiCdPbNiCdPb
Control0.061.820.000.030.020.00
Ni1.130.260.051.010.171.73
Cd1.130.780.000.420.740.36
Pb21.410.023.340.060.001.35
Ni + Pb0.730.391.051.683.641.21
Ni + Cd1.411.200.611.630.740.27
Cd + Pb0.032.001.383.170.262.01
Ni + Cd + Pb0.481.871.821.240.931.62
EF
TreatmentsKhanpur RayaSandal Canola
NiCdPbNiCdPb
Control0.000.000.000.000.000.00
Ni0.010.000.000.030.010.00
Cd0.000.190.020.010.270.03
Pb0.000.000.010.010.000.02
Ni + Pb0.000.050.020.020.010.02
Ni + Cd0.030.210.000.020.160.00
Cd + Pb0.010.100.010.030.170.01
Ni + Cd + Pb0.060.160.060.050.060.02
PLI
TreatmentsKhanpur RayaSandal Canola
Control1.10839 × 10−80
Ni1.95927 × 10−81.4 × 10−6
Cd3.47222 × 10−70.000113
Pb01.14 × 10−7
Ni + Pb5.24237 × 10−77.31 × 10−6
Ni + Cd2.6328 × 10−59.36 × 10−6
Cd + Pb2.19014 × 10−50.000125
Ni + Cd + Pb0.0008578420.000108
TF = translocation factor, BAF = bioaccumulation factor, EF = enrichment factor, PLI = pollution load index.
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Dahlawi, S.; Sadiq, M.; Sabir, M.; Farooqi, Z.U.R.; Saifullah; Qadir, A.A.; Faraj, T.K. Differential Response of Brassica Cultivars to Potentially Toxic Elements and Their Distribution in Different Plant Parts Irrigated with Metal-Contaminated Water. Sustainability 2023, 15, 1966. https://doi.org/10.3390/su15031966

AMA Style

Dahlawi S, Sadiq M, Sabir M, Farooqi ZUR, Saifullah, Qadir AA, Faraj TK. Differential Response of Brassica Cultivars to Potentially Toxic Elements and Their Distribution in Different Plant Parts Irrigated with Metal-Contaminated Water. Sustainability. 2023; 15(3):1966. https://doi.org/10.3390/su15031966

Chicago/Turabian Style

Dahlawi, Saad, Muhammad Sadiq, Muhammad Sabir, Zia Ur Rahman Farooqi, Saifullah, Ayesha Abdul Qadir, and Turki Kh Faraj. 2023. "Differential Response of Brassica Cultivars to Potentially Toxic Elements and Their Distribution in Different Plant Parts Irrigated with Metal-Contaminated Water" Sustainability 15, no. 3: 1966. https://doi.org/10.3390/su15031966

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