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Article

Physiological Responses and Phytoremediation Abilities of Cucumber (Cucumis sativus L.) under Cesium and Strontium Contaminated Soils

by
Shahzaib Ali
1,2,3,
Dan Wang
1,*,
Abdul Rasheed Kaleri
1,
Sadia Babar Baloch
3,
Martin Brtnicky
4,5,
Jiri Kucerik
5 and
Adnan Mustafa
4,5,6,*
1
College of Life Science and Engineering, Southwest University of Science and Technology, Mianyang 621010, China
2
Key Defense Laboratory of the Nuclear Waste and Environmental Security, Mianyang 621010, China
3
Department of Agroecosystems, University of South Bohemia, 370 05 Ceske Budejovice, Czech Republic
4
Department of Agrochemistry, Soil Science, Microbiology and Plant Nutrition, Faculty of AgriSciences, Mendel University in Brno, 61300 Brno, Czech Republic
5
Institute of Chemistry and Technology of Environmental Protection, Faculty of Chemistry, Brno University of Technology, 61200 Brno, Czech Republic
6
Institute for Environmental Studies, Faculty of Science, Charles University in Prague, 12800 Prague, Czech Republic
*
Authors to whom correspondence should be addressed.
Agronomy 2022, 12(6), 1311; https://doi.org/10.3390/agronomy12061311
Submission received: 19 April 2022 / Revised: 26 May 2022 / Accepted: 26 May 2022 / Published: 30 May 2022
(This article belongs to the Special Issue Resilience to Biotic and Environmental Stresses in Horticultural Crops)
Browse Figures
Versions Notes

Abstract

:
Soils contaminated with radionuclides pose a long-term radiation hazard to human health through food chain exposure and other pathways. The uptake, accumulation, and distribution of 133Cs, individual 88Sr, and combined 88Sr + 133Cs, with their physiological and biochemical responses in greenhouse-potted soil-based cucumber (Cucumis sativus L.), were studied. The results from the present study revealed that the uptake, accumulation, TF, and BCF ability of cucumber for 88Sr + 133Cs were greater than for 133Cs and 88Sr while the concentration was the same in the soil (10, 20, 40, 80, and 160 mg kg−1). The highest 88Sr + 133Cs accumulation was 2128.5 µg g−1dw, and the highest accumulation values of 133Cs and 88Sr were 1738.4 µg g−1dw and 1818.2 µg g−1dw (in 160 mg kg−1), respectively. The lowest 88Sr + 133Cs, 133Cs, and 88Sr accumulation values were 416.37 µg g−1dw, 268.90 µg g−1dw, and 354.28 µg g−1dw (10 mg kg−1), respectively. MDA content was higher under 88Sr and 133Cs stress than under 88Sr + 133Cs stress. Chlorophyll content increased at 10 and 20 mg kg−1; however, it decreased with increasing concentrations (40, 80, and 160 mg kg−1). Proline content and the activities of CAT, POD, and SOD were lower under 133Cs and 88Sr than 88Sr + 133Cs stress. The 88Sr, 133Cs, and 88Sr + 133Cs treatment concentrations sequentially induced some enzymes over 60 days of exposure, suggesting that this complex of antioxidant enzymes—CAT, POD, and SOD—works in combination to reduce the impact of toxicity of 88Sr, 133Cs, and 88Sr + 133Cs, especially in young leaves. It is concluded that cucumber reveals considerable phytoremediation capabilities due to unique growth potential in contaminated substrate and is suitable for the bioreclamation of degraded soils. The plant is especially applicable for efficient phytoextraction of 88Sr + 133Cs contamination.

1. Introduction

Soil contaminated with radionuclides due to anthropogenic activities, nuclear weapons testing, pollution of the nuclear power plants, accidents such as the Chernobyl disaster, and dumping of nuclear waste create significant challenges to the ecosystem [1,2]. The long life expectancy of radionuclides and their extensive presence instigate severe pollution of the soil, including agriculture and farmland [1,3]. Human beings are directly or indirectly exposed to these pollutants in soil and waste streams through different ways, such as eating contaminated food crops or drinking contaminated water, which may cause serious harms to human health. In this regard, 133Cs and 88Sr are transferred to plants due to absorption by roots from the liquid phase of the soil [4,5]. The availability of radionuclides in soil solutions is influenced by a variety of factors, including climate, soil variables (such as organic matter, pH, CEC, and soil microbes), and plant characteristics such as taxonomy, morphology, and physiology [6,7,8]. Although Sr and Cs do not have known functions to perform in the plant body, being chemically similar to essential Ca and K, they are believed to enter into the plant body using Ca and K transporters in the cell membrane. Therefore, they compete with K and Ca ions, causing the significant reduction in their transport to the cytoplasm and an ultimate deficiency of these essential elements in plant [9,10,11] where they cause potential metabolic interference and growth and productivity loss [12]. Moreover, the ability of plants to absorb stable isotopes 88Sr and 134Cs from the soil is similar to their ability to absorb radioactive 90Sr and 137Cs; according to certain research, the transport and dispersion of 137Cs and 90Sr in the plant soil system can be very well simulated using 133Cs and 88Sr [13,14].
In recent years, the role of phytoremediation in the restoration of contaminated areas of 90Sr and 137Cs has become the focus of research [15,16,17]. Phytoextraction is considered as an alternate to existing physical and chemical reduction methods. The amount of soil to be treated has decreased by nearly 100 times, but this process takes time and leads to the absorption of radionuclide biomass [18,19]. Phytoextraction is suitable for those hyperaccumulator plants that have huge biomass, quick growth periods, and that move toxic pollutants from the soil to harvestable parts (leaf and stem) of the plants. However, the efficiency of plants for accumulating these toxic pollutants from the soil and transporting them to their aboveground parts depends upon the plant species, growth conditions, and soil types [20]. There has been a sparse amount of literature reporting the ability of horticultural crops for the phytoextraction of 90Sr and 137Cs from contaminated sites.
In the past, it has been reported that leafy vegetables, e.g., komatsuna (Brassica rapa var. perviridis) and mustard (Brassica juncea), which possess large root volumes and root surface areas, had a higher 137Cs transfer value than the root vegetables radish (Raphanus sativus) and turnip (Brassica rapa var. glaba) [2]. Moreover, in the phytoremediation of Cs-polluted soil, oilseed rape and New Zealand spinach were found to be promising plant species, as were pumpkin and sunflower for Sr-polluted soil [1]. However, for the phytoremediation of Cs- and Sr-polluted soil, not only the absorption ability but also the characteristics of the species used should be considered and evaluated [1]. Therefore, we assumed that cucumber plants used in the present study would have high Sr and Cs absorption and transport ability owing to their rapid growth, extensive root system, and high survival and tolerance to excessive concentrations of heavy metals. Moreover, concern may arise for its end-use, and for this purpose we would like to recommend that contaminated residual biomass can be utilized for bioenergy production in addition to its safe disposal options, e.g., in a landfill [21,22,23]. Thus, integrating phytoremediation with valuable material and bioenergy production can make the process economically viable. Thus, in the present study, cucumber plants were utilized to assess their efficacy to tolerate combined 90Sr and 137Cs stress. The specific objectives of the present study were to evaluate the bioaccumulation, transportation, and distribution of individual 133Cs and 88Sr and combined 88Sr + 133Cs and to assess the physiological and biochemical responses of cucumber (Cucumis sativus L.) grown in greenhouse-potted soil. In addition, we analyzed the phytoextraction efficiency in the plants in order to assess whether the cucumber plants can grow and remediate the 88Sr, 133Cs, and 88Sr + 133Cs in contaminated soils.

2. Materials and Methods

2.1. Soil Collection and Seedling Growth

The soil was collected from the nursery garden center of the Southwest University of Science and Technology, Mianyang, China. Firstly, collected soil samples were air dried and then grinded and passed through a 2 mm sieve. The pH values of soil in water (H2O) and potassium chloride (KCl) were determined using a pH meter, and soil organic matter (SOM) was determined according to the Walkley–Black method. Deionized water (5 mL) was mixed with 1 g of grinded and sieved soil, and the soil’s electrical conductivity was measured. The primary physical and chemical characteristics of the soil were pH H2O = 7.0, pH KCl = 6.22, soil organic matter percentage = 1.24, and electrical conductivity (mS/cm) = 1.12. Cucumber plant seeds were purchased from the Mianyang seed company, the nutritional soil was filled with small bags of polyethylene for seedlings, and seeds were planted approximately 1 cm deep in uncontaminated soil (one seed in each bag).

2.2. Treatment and Experimental Design

The pot experiment was carried out in the greenhouse of Southwest University of Science and Technology in Mianyang, China (E = 104°41′, N = 31°32′). The sieved soil was kept on a waterproof sheet and mixed with 88Sr (NO3)2,133CsCl, and 88Sr (NO3)2 + 133CsCl solutions to obtain appropriate concentrations in soil (Table 1). The soil was then allowed to stabilize for at least 30 days. Uncontaminated soil was used as a control. Each pot (25 cm in diameter, 20 cm in height) was filled with 4.5 kg of concentrated soils. Three uniform 15 day-old seedlings were transferred into each pot, and three pots of each treatment and three replicates were used in a randomized complete block design (RCBD). Plants were irrigated with tap water up to 100% for their field potential to maintain 41.9% soil moisture. Every pot was kept on the plastic dishes to collect leachates, which were applied periodically to the pot soil to minimize treatment loss. After transport of the seedlings, the pot trial lasted for 60 days.

2.3. Growth Measurements

The growth of the whole plant was measured after the harvest. Stainless steel scissors were used to cut the plant specimens into two parts, namely shoot and root, after rinsing with distilled water. Specimens were first measured using a scale to determine shoot height (cm), root length (cm), and leaf area (cm2), and after that they were air dried in a natural cool environment and well-ventilated location, and then oven-dried for 24 h at (68 °C ± 2 °C). The dry weight (g plant–1) of each part was weighed to calculate the biomass.

2.4. Assessing the 88Sr, 133Cs, and 88Sr + 133Cs Accumulation

Inductively coupled plasma-optical emission spectrometry (ICP-MS; version 715-ES ICP-MS; version, Palo Alto, CA, USA) with the acid digestion method was used to assess the plant concentrations of 88Sr, 133Cs, and 88Sr + 133Cs in shoot and root, as stated by [24]. In brief, 15 mL HNO3 and HClO4 (3:1 v/v) were used to acid digest 0.5 g of dried shoot tissue and 0.3 g of dry root tissue. The digestive vessels of the specimens were kept for 15 min in a microwave-assisted digestion system (MDS-6G) between 120 and 190 °C, for 15 and min at 190 °C for 30 min at 190 °C. Finally, the digested specimens were diluted with deionized water to a final volume of 50 mL for individual 88Sr, 133Cs, and 88Sr + 133Cs determinations. The concentrations and accumulations of 88Sr, 133Cs, and 88Sr + 133Cs in the plants′ roots and shoots were calculated according to [25].

2.5. Phytoextraction Potential

The plant extraction capacity was determined by measuring the biological concentration factor (BCF) and transfer factor (TF) of the nuclide. BCF is the ratio of nuclide concentration in the aboveground part of the whole plant to nuclide concentration in the soil, and TF is the ratio of the nuclide concentration in the aboveground part of the plant to the root of the plant [26].
BCF and TF were calculated by these formulas:
BCF = Cshoot (mg kg−1 dw)/Csoil (mg kg−1 dw)
TF = Cshoot (mg kg−1 dw)/Croot (mg kg−1dw)
where Cshoot, Croot, and Csoil, respectively, are concentrations of nuclides in shoot, root, and soil.

2.6. Assessing the Physiological and Biochemical Indexes

The contents of chlorophyll content, malondialdehyde (MDA), proline, superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT) were measured from the plant leaves. Total chlorophyll content was calculated using the Li technique and quantified at 652 nm using the 95% ethanol colorimetric method [27]. The content of MDA was determined by total bile acid colorimetry, as in [27]. The content of the proline was determined by the Bates method [28]. The activity of SOD and POD was determined by Li’s method, and SOD activity was assayed based on the reduction of NBT (nitroblue tetrazolium). This reaction was conducted in sodium phosphate buffer (50 mM, pH 7.8) containing 100 µL of enzyme extract, 2 µM riboflavin, 65 µM NBT, 13 µM methionine, and 1 µM ethylenediamine tetraacetic sodium. The 3 mL reaction mixture was initialed by illumination for 2 min at 25 °C, and the absorbance of blue formazan was measured with a spectrophotometer (UV-3802, Unico, Shanghai, China) at 560 nm. One unit of SOD activity (U) was defined as the amount of enzyme that caused 50% inhibition of NBT reduction. POD activity was determined by measuring the absorbance changes at 470 nm and 25 °C. The reaction was performed in a 3 mL solution. A 10 µL volume of enzyme solution was added to 2.99 mL of sodium phosphate buffer (50 mM, pH 6.0) containing 18.2 mM guaiacol and 4.4 mM H2O2 as substrates. POD activity was defined as the amount of enzyme that caused an increase in absorbance at 470 nm of 0.001 per minute. CAT activity was measured by monitoring the decrease of H2O2 at 240 nm for 1 min at 25 °C. The 3 mL reaction mixture contained 100 µL of enzyme extract and 2.9 mL of sodium phosphate buffer (50 mM, pH 6.0) containing 10 mM H2O2. CAT activity was calculated as the amount of enzyme that caused a reduction in absorbance at 240 nm of 0.01 per minute [27]. The experimental results are the average of three replicates.

2.7. Statistical Analysis

The data were tested for normalities and variance homogeneity, and they were log-transformed to correct the deviations from those assumptions when necessary. Treatment means were compared using a two-way analysis of variance. All measurements were checked by Microsoft Excel 2013, IBM SPSS Statistics V22.0, and the Origin Pro 8.0 mapping software.

3. Results

3.1. Growth Characteristics of Cucumber under 88Sr, 133Cs, and 88Sr + 133Cs Stress

Plant growth is a primary stress indicator, and its response to any stress can predict the level of toxicity in the environment. In this context, the measuring growth response of cucumber to 133Cs, 88Sr, and 88Sr + 133Cs was one of the primary objectives of this study. The growth in the form of shoot height, root length, and leaf area (Figure 1) was not significantly reduced by 88Sr and 133Cs individual treatments or 88Sr + 133Cs in combination. The applications of 88Sr, 133Cs, and 88Sr + 133Cs (at 10 mg kg−1) significantly decreased shoot height, root length, and leaf area in comparison to the control, but higher concentrations (20, 40, 80, 160 mg kg–1) did not cause any further significant decrease in plant growth characteristics. 133Cs and 88Sr individually and in combination produced non-significant stress even at the lowest concentration of 10 mg kg−1 and reduced shoot length, root length, and leaf area. This suggested the degree of toxicity produced by the two nuclides. Higher shoot height, root length, and leaf area of 88Sr (99.93 cm, 13.23 cm, 93.62 cm2, respectively), 133Cs (80.40 cm, 16.46 cm, 76.82 cm2, respectively), and 88Sr + 133Cs (105.36 cm, 17.5 cm, 99.09 cm2, respectively) were recorded at 10 mg kg−1 concentrations. However, lower shoot height, root length, and leaf area of 88Sr (78.3 cm, 11.56 cm, 48.28 cm2, respectively), 133Cs (62.23 cm, 12.43 cm, 27.80 cm2, respectively), and 88Sr + 133Cs (83.33 cm, 12.83 cm, 52.52 cm2, respectively) were recorded at 160 mg kg−1 concentrations. The individual 133Cs, at its highest concentration, showed the significantly highest shoot height, root length, and leaf area reduction compared to 88Sr and 88Sr + 133Cs, proving itself to be more toxic.

3.2. Effect of 88Sr, 133Cs, and 88Sr + 133Cs on the Biomass Distribution of Cucumber

The effects of 88Sr and 133Cs individually and 88Sr + 133Cs combined on the shoot and root dry biomass showed (Table 2) that the shoot and root biomass in 88Sr-, 133Cs-, and 88Sr + 133Cs-treated plants were significantly lower compared to their controls. It was observed that the 88Sr + 133Cs treatment had lower effects and produced higher shoot biomass of 6.297 ± 0.18 g dw plant−1 at the 10 mg kg−1 level than did the 88Sr + 133Cs treatments, while minimum shoot biomass was recorded at the 160 mg kg−1 level of 133Cs (2.054 ± 0.18 g dw plant−1). The maximum root biomass (1.499 ± 0.06 g dw plant−1) produced by 88Sr + 133Cs at a 10 mg kg−1 concentration was significantly the highest biomass value among all treatments except for the control (Table 2). It was interesting that this treatment showed non-significant variation in root biomass up to 40 mg kg−1 levels and declined significantly at 80 and 160 mg kg−1 levels.

3.3. 88Sr, 133Cs, and 88Sr + 133Cs Bio-Accumulation in Plant and Phytoextraction Potential

The 88Sr + 133Cs accumulation in total plants was shown to be significantly higher than that of 88Sr and 133Cs among all treatment concentrations (Table 3); however, accumulation in shoot and root was significant with 88Sr and 133Cs at the 160 mg kg−1 level. Similarly, at treatment concentrations of 10, 20, and 40 mg kg−1, the 88Sr + 133Cs accumulation in both root and shoot were non-significant; the highest accumulation in the shoot part was 1514.4 ± 240.1 µg g−1dw detected in 88Sr + 133Cs followed by 1196.8 ± 47.78 µg g−1dw in 88Sr at 160 mg kg−1 treatment concentrations. However, the 88Sr and 133Cs, individually and combined, showed significant accumulation in root, namely 621.37 ± 65.5a µg g−1 dw for 88Sr, 606.16 ± 95.6 µg g−1 dw for 133Cs, and 614.12 ± 37.3 µg g−1 dw for 88Sr + 133Cs. The highest total plant accumulation was observed (2128.5 ± 219.2 µg g−1dw) at 88Sr + 133Cs, while the lowest total plant accumulation was observed (1738.4 ± 178.9 µg g−1dw) at 133Cs (160 mg kg−1) treatment concentrations. This revealed that the most important factor affecting the content of 88Sr + 133Cs in cucumber plants was the concentration of 88Sr + 133Cs in the soil.
The total plant BCF of 88Sr + 133Cs was significantly higher than that of 88Sr and Cs. However, shoot BCF was significantly the highest in 88Sr + 133Cs among all treatments (Table 3). The highest total plant values of BCF for 88Sr (35.42), 133Cs (26.89), and 88Sr + 133Cs (41.63) were recorded at 10 mg kg−1 treatment concentrations. Moreover, the 88Sr + 133Cs was found to have the highest TF values (2.78 and 2.51 at 80 and 160 mg kg−1 concentrations, respectively), while values of 88Sr and 133Cs were found to be significant (1.97, 1.93) at 160 mg kg−1 treatment concentrations.

3.4. The Effect of 88Sr, 133Cs, and 88Sr + 133Cs Extraction Efficiency on Cucumber

The extraction productivity of cucumber in 88Sr, 133Cs, and 88Sr + 133Cs was determined, and the findings are summarized in Table 4. The results showed that the concentrations of 88Sr, 133Cs, and 88Sr + 133Cs in the soil; plant attentiveness; and the amount of plants and pots in the soil steadily rose as the concentration in the soil increased. However, the total plant biomass and the ratio of plant/content in the pot (%) decreased gradually. In the 10 mg kg−1 treatments, the contents of 88Sr, 133Cs, and 88Sr + 133Cs were highest among plants with contents in pots, which was 7.06, 3.74, and 10.80% for 88Sr, 133Cs, and 88Sr + 133Cs, respectively. In the 160 mg kg−1 treatment, the ratio was lowest, i.e., 1.63%, 0.91%, and 2.11% for 88Sr, 133Cs, and 88Sr + 133Cs, respectively.

3.5. Physiological and Biochemical Response of Cucumber to 88Sr, 133Cs, and 88Sr + 133Cs Stress

The chlorophyll, MDA, and proline contents of cucumber are shown in Figure 2. The results reveal that the chlorophyll content of 88Sr + 133Cs was observed to be high at each concentration as compared to 88Sr and 133Cs. There were non-significant differences detected at 10, 40, and 80 mg kg−1 concentrations of 88Sr and 133Cs. The chlorophyll content was observed to be high at low concentrations; however, it decreased as the concentration of 88Sr, 133Cs, and 88Sr + 133Cs increased in the soil. The chlorophyll content was detected to be higher in the control (80.30) followed by 70.84, 64.97, and 75.34 mg g−1FW at 10 mg kg−1 of 88Sr, 133Cs, and 88Sr + 133Cs, respectively. Similarly, the lowest chlorophyll content was detected (35.25, 34.23 mg g−1FW) at (160 mg kg−1) of 88Sr and 133Cs, respectively. It was also observed, as seen in Figure 2, that the MDA content of the cucumber plant was increased by increasing the 88Sr, 133Cs, and 88Sr + 133Cs concentrations in soil. The maximum MDA content was detected for 88Sr at all concentrations; compared with 133Cs and 88Sr + 133Cs, the highest MDA content (0.333 µmol g−1FW, 0.301 µmol g−1FW, and 0.256 µmol g−1FW) were observed at 160 mg kg−1 treatment concentrations of 88Sr, 133Cs, and 88Sr + 133Cs, respectively. Similarly, the lowest MDA were observed at 10 mg kg−1 of 88Sr, 133Cs, and 88Sr + 133Cs. The MDA content of the cucumber plant was increased at different concentrations of 88Sr, 133Cs, and 88Sr + 133Cs compared with the control. Figure 2 demonstrate that the proline content of cucumber leaves under 88Sr, 133Cs, and 88Sr + 133Cs stress was increased as the concentration increased in the soil. Similarly, variable proline contents were detected in the 88Sr and 88Sr + 133Cs at concentrations of 10, 40, and 80 mg kg−1 compared to 133Cs. The highest proline content of 39.81 µg g−1FW 88Sr was observed at the 40 mg kg−1 treatment, and 39.54 µg g−1FW and 41.10 µg g−1FW were detected with treatment of 160 mg kg−1 of 133Cs and 88Sr + 133Cs, respectively, with significant values (p < 0.001). Under the stress of 88Sr, 133Cs, and 88Sr + 133Cs, the rapid accumulation of proline was observed in cucumber as compared to their controls.
The effect of 88Sr, 133Cs, and 88Sr + 133Cs stress on the CAT, POD, and SOD activity of cucumber plants are presented in Figure 3. The results demonstrated that the CAT activity increased with increases in the 88Sr and 88Sr + 133Cs concentrations in soil. The highest CAT activities were 72.47 µg min−1), 62.64 µg min−1, and 102.49 µg min−1 detected at 160 mg kg−1 concentration of 88Sr, 133Cs, and 88Sr + 133Cs treatments, respectively, with significant values (p < 0.001). The activity of CAT in the 88Sr + 133Cs treatment was higher than the activity of CAT in the treatments of 88Sr and 133Cs. It could be concluded from the results that 88Sr, 133Cs, and 88Sr + 133Cs had positive influences on the activity of CAT at high concentrations. The results from Figure 3 demonstrated that the POD activity was increased as 88Sr, 133Cs, and 88Sr + 133Cs treatment concentrations increased. The maximum POD activity was observed (109.78 µg min−1) for the 88Sr + 133Cs treatment at 160 mg kg−1 concentration. However, the lower POD activity was observed at 10 mg kg−1 of 88Sr, 133Cs, and 88Sr + 133Cs treatments. The results of SOD activity significantly increased as the concentration of 88Sr, 133Cs, and 88Sr + 133Cs increased compared with the control. The highest SOD activities (136.79 µg min−1, 93.66 µg min−1, and 158.49 µg min−1) were recorded at the 160 mg kg−1 concentration of 88Sr, 133Cs, and 88Sr + 133Cs treatments, while, the lowest SOD activity was 58.40 µg min−1, 45.90 µg min−1, and 114.45 µg min−1 for 88Sr, 133Cs, and 88Sr + 133Cs, respectively.

4. Discussion

4.1. Growth Characteristics of Cucumber under 88Sr, 133Cs, and 88Sr + 133Cs Stress

The role of 88Sr and 133Cs in plant nutrition is unclear. According to several scientists, low concentrations of heavy metal ions in the soil solution can enhance plant growth, while a high concentration of metals such as cesium and chromium in the soil can be toxic to plants and restrict plant growth [29,30]. Plants have different abilities to absorb, transfer, and isolate radionuclides, and it is a well-known fact that Cs does not have any important role in plant growth and metabolism, and hence its higher accumulation in plant biomass may create toxic effects. 133Cs also reduced root length at lower and higher concentrations as compared to 88Sr alone and 88Sr + 133Cs. Our findings confirm the observations of [5], who found the same growth effects of Cs on Plantago major. The reduction in growth is a result of physiological and metabolic impairment caused by metal stress. Since metal stress triggers oxidative stress in plant cells [31], which is obvious from the hyper-regulation of anti-oxidative defense genes against Cs stress [32], a reduction in growth could therefore be the result of such metabolism. Another possible cause of growth reduction can be traced to Cs competitiveness with K. The authors in [33] concluded that Cs uses K channels during its uptake, which causes K deficiencies in the cells. The authors in [32] also showed that Cs enhances oxidative stress when applied in a K-deficient medium. Due to such metabolic and physiologically adverse effects, Cs causes significant losses to growth in many sensitive plants.
Different concentrations of 88Sr, when applied individually, also significantly reduced cucumber growth (Figure 1), but as described earlier, its effects were less than those of 133Cs. Like Cs, Sr also does not have important functions in the plant body. Therefore, Sr has also been reported as a toxic heavy metal with its stable isotopes. The Sr toxicity effects on growth from hydroponic experiments have been reported in other plants such as Oryza sativa [34], Brassica juncea [35], Arabidopsis thaliana [36], Solanum tuberosum [37], and Plantago major [5]. Such findings confirm the toxic effects of 88Sr on plant growth. The results of 88Sr + 133Cs combined application, at all concentrations, were statistically similar with Sr, although it produced the lowest reduction in shoot length, root length, and leaf area. This suggests that both nuclides when combined masked much of the toxic effects of each other.

4.2. Effect of 88Sr, 133Cs, and 88Sr + 133Cs on the Biomass Distribution of Cucumber

Since shoot and root biomass are directly proportional to each other, shoot length and root length results thus coincide with them and prove 133Cs to be more toxic than all other treatments, particularly at higher concentration levels. It is reported that heavy metal ions, even at low concentrations in a soil solution, may decrease plant growth, while their excessive or higher concentrations can be toxic to plants and therefore limit plant growth dangerously [38,39]. This pattern shows that the nuclides when combined can reduce the toxic effects on the growth of plants. Although the mechanism behind this is yet not understood, but can nevertheless open new insights of research, it is documented [40] that plants show cross-protection, a reaction against stress in which one stress may protect the plant against others. 133Cs alone showed significantly high deleterious effects on root biomass from its lowest to highest concentrations compared to all other treatments. However, its effects were non-significant from 10 to 40 mg kg−1 applied concentrations in soil. The 88Sr showed non-significant effects to those of 133Cs on root biomass at 10 and 20 mg kg−1, while it produced significantly higher root biomass at concentrations of 20 mg kg−1 an onward than did 133Cs. The findings of [5,34,41] suggest that root growth was not decreased in Triticum aestivum, Glycine max, and Plantago major at low concentrations; however, our results vary from these findings and suggest that even at lowest concentrations (10 mg kg−1), the reduction effects were significant. The authors in [42], while studying the effects on Amaranthus mangostanus, found that lower concentrations of 133Cs and 88Sr did not affect the above ground and below ground biomass. They also found that 88Sr was a more hazardous to reduce crop biomass than 133Cs. These results are antagonistic to our findings. The effects of 88Sr and 88Sr + 133Cs treatments were statistically similar on the shoot and root biomass of cucumber as compared to 133Cs; statistically, it was shown that 88Sr + 133Cs treatment had a lower impact on the biomass of cucumber than did 88Sr and 133Cs alone. This suggests that 88Sr, when applied in combination with 133Cs, has some mitigation properties to the adverse effects of 133Cs, which resembles a phenomenon of cross-protection in plants.

4.3. Sr, 133Cs, and 88Sr + 133Cs Bio-Accumulation in Plant and Phytoextraction Potential

It can be seen from Table 3 that a slight increase in 88Sr + 133Cs concentration in the soil does not affect its bioaccumulation in the root and shoot of cucumber. Similar results have been reported in Arabidopsis thaliana [32], Pennisetum purpureum (up to 3 mM; [43]), Calla palustris (0.5 and 1 mM; [44]), and Ocimum basilicum (up to 0.4 mM; [33]). Earlier findings suggest that the uptake and distribution of nuclides in plants are dependent on nutrient metabolism, especially K and Ca [29]. The lower accumulation of 133Cs can be attributed to the levels of K uptake and regulation. The authors in [5] suggested that K uptake was not affected by low concentrations of Cs in the external medium in Plantago major. However, increasing concentrations decreased the uptake of K significantly [5], which may influence the higher accumulation of Cs in shoots and roots. The bioaccumulation of nuclides in the root at the highest (160 mg_ concentration was non-significant among all treatments, suggesting statistically similar effects. The increased bioaccumulation of 88Sr has been suggested in many previous studies [5,32,45,46], but they suggested its hyper-accumulation over 133Cs. In contrast, our results suggest that bioaccumulation of 88Sr + 133Cs was higher in shoot, while in root the 88Sr accumulation was higher than the 133Cs. Since the results of 88Sr + 133Cs were non-significant to those of 88Sr in root, it can therefore be concluded that both produced similar results in their root bioaccumulation (Table 2). The authors in [45] suggested that total (in the whole plant) bioaccumulation of Cs is higher than that of Sr in Amaranthus mangostanus. They also concluded that A. mangostanus has more Cs absorption and accumulation ability. This suggests that there are some selective mechanisms in different plants for the uptake and accumulation of Sr and Cs.
The values of BCF > 1 indicate that the plant is an accumulator, while the values of BCF > 10 indicate that the plant has the potential to be a hyper-accumulator, while the value of TF of each nuclide is used to evaluate the capacity of a plant to transfer a nuclide from the root to the shoot. This value is defined as the ratio of the metal concentration in the shoot to that in the root of plants. The value of TF > 1 indicates that the plant is effective in the translocation of metal from its root to shoot. The TF values increased with an increase in concentration levels in all treatments [47,48]. Notably, BCF and TF of 88Sr and 133Cs found in our study were high compared to those reported for other species such as Amaranthus mangostanus L. [45], Raphanus sativus L. [42], and Gypsophila paniculata [49]. Table 4 indicates that when the intensity of 88Sr, 133Cs, and 88Sr + 133Cs in the soil was high, it was more difficult to uptake88Sr, 133Cs, and 88Sr + 133Cs from the soil, and it would take additional time to apply cucumber to remediate the high concentrations of 88Sr, 133Cs, and 88Sr + 133Cs from contaminated soil. In this test, when the concentration in the soil of 88Sr, 133Cs, and 88Sr + 133Cs was 10 mg kg−1, it needed to grow cucumber plants two seasons in a year for 88Sr approximately 14 times, which needed 7 years, followed by 133Cs 26 times, which needed 13 years, and 88Sr + 133Cs 10 times, which needed 5 years, theoretically, to uptake all the 88Sr, 133Cs, and 88Sr + 133Cs from the soil, respectively; when the 88Sr, 133Cs, and 88Sr + 133Cs, concentration in the soil was 160 mg kg−1, it needed to grow cucumber plants two seasons in a year for 88Sr approximately 62 times, which needed 31 years, followed by 133Cs 110 times, which needed 55 years, and 88Sr + 133Cs 48 times, which need 24 years, theoretically, to uptake all the 88Sr, 133Cs, and 88Sr + 133Cs from the soil. Similar results were recorded in [45].

4.4. Physiological and Biochemical Response of Cucumber to 88Sr, 133Cs, and 88Sr + 133Cs Stress

These results corroborate those reported by other studies [42,50]. Decreased chlorophyll contents with heavy metal stress may be due to the inhibition of enzymes responsible for chlorophyll biosynthesis and a strong production of reactive oxygen species [50]. Chlorophyll content was increased at 10 and 20 mg (Figure 2); however, it was reduced by increasing the concentrations of treatments. This phenomenon is due to excessive 88Sr and 133Cs, which significantly reduced the chlorophyll content compared to 88Sr + 133Cs. Similar results were obtained by other researchers who studied the impact of Sr on oilseed rape [46], Amaranthus caudatus Linn [51], maize [6], Amaranthus mangostanus L. [45], and Raphanus sativus L [42]; and the impact of Cs on Nitella pseudoflabellata [52], Salix paraplesia [53], Spinacia oleracea [54], Amaranthus mangostanus L. [45], and Raphanus sativus L. [42]. MDA is an important product of membrane lipid peroxidation, and it can indirectly reflect the degree of damage to the plant membrane system. In this experiment, MDA content slightly decreased at low 88Sr, 133Cs, and 88Sr + 133Cs concentrations (10 and 20 mg kg−1) and then increased at high concentrations (40, 80, and 160 mg kg−1); this change trend indicated that low concentrations of 88Sr, 133Cs, and 88Sr + 133Cs had little destructive effects on cucumber membrane function, while the high 88Sr concentration treatments led to impairment of cucumber membrane function. These MDA changes were similar to those found by [42,45]. The increased activity of antioxidant enzyme activities (CAT, POD, and SOD) indicated the activation of defense mechanisms against the 88Sr, 133Cs, and 88Sr + 133Cs that induced oxidative stress in cucumber. In the present study, the activity of CAT, POD, and SOD increased gradually with increasing 88Sr, 133Cs, and 88Sr + 133Cs concentrations from (10 to 160 mg) (Figure 3). Similarly, the Sr and Cs application resulted in the increased activity of CAT, POD, and SOD in Amaranthus mangostanus L. [45,51], the activities of CAT and POD in Amaranthus caudatus L. [45], and CAT, POD, and SOD in Raphanus sativus L. [42].

5. Conclusions

The Sr and Cs contamination threats to the soil environment hence are liable to be removed. Phytoremediation is an effective tool to combat the hyper-accumulation of radionuclides and heavy metals in soil. The cucumber plant showed significantly lower growth under various concentrations of individual 88Sr and 133Cs treatments than did 88Sr + 133Cs combined. 133Cs produced more loss in terms of growth and biomass production. The 88Sr + 133Cs when applied in combination showed significantly better results, indicating some mitigating effects. Shoot accumulation was high for 88Sr + 133Cs, while root accumulation was higher for 88Sr than for 133Cs. Similarly, the bioaccumulation and translocation of 88Sr + 133Cs was higher than of 88Sr and 133Cs treatments. This shows that 88Sr + 133Cs combined are absorbed and translocated at high levels and at the same concentrations and enhance growth and biomass production. It is well known that radionuclides and heavy metals will directly or indirectly cause molecular damage to plant cells through the outbreak of reactive oxygen species (ROS), and ROS will react with fatty acids, leading to lipid peroxidation and damage to biofilms [55,56]. One of the responses of plants to ROS is an increase in antioxidant enzyme activity, thereby protecting them from oxidative damage induced by various stresses [55]. Some plants’ tolerance to heavy metal stress is related to the higher activity of antioxidant enzymes [57,58,59]. The 88Sr, 133Cs, and 88Sr + 133Cs treatment concentrations sequentially induced some enzymes over 60 days of exposure, suggesting that this complex of antioxidant enzymes (CAT, POD, and SOD) work in combination to reduce the impact of toxicity of 88Sr, 133Cs, and 88Sr + 133Cs, especially in young leaves. It is concluded that cucumber reveals considerable phytoremediation capabilities due to the unique growth potential in contaminated substrate and is suitable for bioreclamation of degraded soils. The plant is especially applicable for efficient phytoextraction of 88Sr + 133Cs-contamination.

Author Contributions

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

Funding

This research was financially supported by National Defense Foundation of China (Grant No. 16ZG6101).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare that there is no conflict of interest either financially or otherwise.

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Agronomy 12 01311 g001 550
Figure 1. Shoot height, root length, and leaf area responses of cucumber to various concentrations (0 to 160 mg kg−1) of 88Sr, 133Cs, and 88Sr + 133Cs treatments. The columns sharing different letters are significantly different at p < 0.05. The error bars indicate standard deviation.
Figure 1. Shoot height, root length, and leaf area responses of cucumber to various concentrations (0 to 160 mg kg−1) of 88Sr, 133Cs, and 88Sr + 133Cs treatments. The columns sharing different letters are significantly different at p < 0.05. The error bars indicate standard deviation.
Agronomy 12 01311 g001
Agronomy 12 01311 g002 550
Figure 2. The effect of 88Sr, 133Cs, and 88Sr + 133Cs stress on the chlorophyll, MDA, and proline content of cucumber to various concentrations (0 to 160 mg kg−1) of 88Sr, 133Cs, and 88Sr + 133Cs treatments. The columns sharing different letters are significantly different at p < 0.05.
Figure 2. The effect of 88Sr, 133Cs, and 88Sr + 133Cs stress on the chlorophyll, MDA, and proline content of cucumber to various concentrations (0 to 160 mg kg−1) of 88Sr, 133Cs, and 88Sr + 133Cs treatments. The columns sharing different letters are significantly different at p < 0.05.
Agronomy 12 01311 g002
Agronomy 12 01311 g003 550
Figure 3. The effect of 88Sr, 133Cs, and 88Sr + 133Cs stress on the activity of antioxidant enzymes of CAT, POD, and SOD of cucumber to various concentrations (0 to 160 mg kg−1) of 88Sr, 133Cs, and 88Sr + 133Cs treatments. The columns sharing different letters are significantly different at p < 0.05. The error bars indicate standard deviation.
Figure 3. The effect of 88Sr, 133Cs, and 88Sr + 133Cs stress on the activity of antioxidant enzymes of CAT, POD, and SOD of cucumber to various concentrations (0 to 160 mg kg−1) of 88Sr, 133Cs, and 88Sr + 133Cs treatments. The columns sharing different letters are significantly different at p < 0.05. The error bars indicate standard deviation.
Agronomy 12 01311 g003
Table
Table 1. Concentration of 88Sr, 133Cs, and 88Sr + 133Cs applied in soils.
Table 1. Concentration of 88Sr, 133Cs, and 88Sr + 133Cs applied in soils.
Treatment
(mg/kg−1)		Treatment
0 (ck)12345
88Sr010204080160
133Cs010204080160
88Sr + 133Cs (1:1)010 + 1020 + 2040 + 4080 + 80160 + 160
Note: 0 is the control, each treatment is repeated three times.
Table
Table 2. Effect of 88Sr, 133Cs, and 88Sr + 133Cs on the biomass distribution of cucumber.
Table 2. Effect of 88Sr, 133Cs, and 88Sr + 133Cs on the biomass distribution of cucumber.
Concentration
(mg kg−1)		Plant Biomass (g dw Plant−1)
ShootRootTotal
88Sr09.443a2.362a11.80a
104.848bc1.133cd5.981bcd
204.431bc1.040de5.472bcd
404.321bc0.995de5.316bcd
804.193bc0.966de5.160bcd
1603.501bc0.815ef4.317bcd
Treatment mean for 88Sr5.122AB1.218AB6.341AB
133Cs09.443a2.362a11.80a
103.373bc0.815ef4.188bcd
203.266bc0.787ef4.054bcd
403.217bc0.610fg3.828cd
802.838bc0.592fg3.431cd
1602.054c0.470g2.525d
Treatment mean for 88Sr4.031B0.939B4.971B
88Sr + 133Cs09.443a2.362a11.80a
106.297ab1.499b7.797b
205.709bc1.378bc7.087bc
405.083bc1.209bcd6.293bcd
804.392bc1.068de5.460bcd
1603.836bc0.925de4.762bc
Treatment mean for 88Sr 133Cs5.793A1.406A7.199A
Treatment × concentration interactionNSNSNS
Note. Different lowercase letters, in a single column, show significant differences among concentration means at p < 0.05, while different upper case letters, in a single column, show significant differences among the treatment means at p < 0.05. NS = non-significant.
Table
Table 3. The effect of 88Sr, 133Cs, and 88Sr + 133Cs on the bio-accumulation of plants and phytoextraction potential.
Table 3. The effect of 88Sr, 133Cs, and 88Sr + 133Cs on the bio-accumulation of plants and phytoextraction potential.
Accumulation
(µg. g dw−1)		TFBCFBCF
TreatmentsConcentrationsShootRootTotal PlantShootShootTotal Plant
88Sr0------
10156.23fg198.05f354.280.79e15.62bcd35.42ab
20226.95fg341.52cde568.46de0.67de11.34cd28.42bc
40448.64efg457.91abc906.55cd0.98d11.21cd22.66bcd
80962.44bcd579.07ab1541.51bc1.65c12.03bcd19.26cde
1601196.84abc621.38a1818.221.97b7.48d11.36ed
Treatment mean for 88Sr598.22B439.58A1037.80AB1.212B11.5323.42AB
133Cs0------
10125.79g143.12f268.90f0.88e12.57bcd26.89bcd
20204.27fg217.48ef421.74ef0.94d10.21cd21.08bcd
40449.02efg240.05def689.06d1.87c11.22cd17.22cde
80838.6cde426.96abc1265.5c1.97b10.48cd15.81def
1601132.27abc606.16a1738.4b1.93b7.07d10.86ef
Treatment mean for 133Cs549.99B326.75B876.72B1.518B 18.37B
88Sr + 133Cs0------
10257.65fg158.72f416.37ef1.61c25.76a41.63a
20422.69efg241.39def664.08de1.73b21.13ab33.20ab
40648.1def401.38bcd1049.4cd1.59c16.20bcd26.23cde
801365.01ab488.59abc1853.5ab2.78a17.06bc23.16cde
1601514.45a614.13a2128.5a2.51ab9.46cd13.30ef
Treatment mean for 88Sr + 133Cs841.58A380.84AB1222.37A2.044A22.45A27.505A
Treatment × concentration interactionNSNSNSNSNSNS
Note. Different lowercase letters, in a single column, show significant differences among concentration means at p < 0.05, while different upper case letters, in a single column, show significant differences among the treatment means at p < 0.05. NS = non-significant.
Table
Table 4. The effect of 88Sr, 133Cs, and 88Sr + 133Cs extraction efficiency of cucumber.
Table 4. The effect of 88Sr, 133Cs, and 88Sr + 133Cs extraction efficiency of cucumber.
88Sr Treatment
Concentration in Soil (mg/kg)Concentration in Plant (mg kg−1 DW)Biomass of Total Plant (g /Plant)Contents in Plant (mg/Plant)Contents in Pot (mg/Pot)Ratio b/w Contents in
the plant\Contents in
a Pot (%)
0-11.80--
10177.145.981.059457.06
20284.235.471.554905.18
40453.275.312.4061804.01
80770.755.163.9773603.31
160909.104.313.9187201.63
133Cs treatment
0-11.80--
10134.454.180.562001453.74
20210.874.050.854024902.84
40344.533.821.3161051802.19
80632.773.432.1704013601.80
160869.212.522.1904097200.91
88Sr + 133Cs treatment
0-11.80--
10208.187.791.6214510.80
20332.047.082.350907.83
40524.746.293.3001805.5
80926.795.465.0603604.21
1601064.24.765.0657202.11
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Ali, S.; Wang, D.; Kaleri, A.R.; Baloch, S.B.; Brtnicky, M.; Kucerik, J.; Mustafa, A. Physiological Responses and Phytoremediation Abilities of Cucumber (Cucumis sativus L.) under Cesium and Strontium Contaminated Soils. Agronomy 2022, 12, 1311. https://doi.org/10.3390/agronomy12061311

AMA Style

Ali S, Wang D, Kaleri AR, Baloch SB, Brtnicky M, Kucerik J, Mustafa A. Physiological Responses and Phytoremediation Abilities of Cucumber (Cucumis sativus L.) under Cesium and Strontium Contaminated Soils. Agronomy. 2022; 12(6):1311. https://doi.org/10.3390/agronomy12061311

Chicago/Turabian Style

Ali, Shahzaib, Dan Wang, Abdul Rasheed Kaleri, Sadia Babar Baloch, Martin Brtnicky, Jiri Kucerik, and Adnan Mustafa. 2022. "Physiological Responses and Phytoremediation Abilities of Cucumber (Cucumis sativus L.) under Cesium and Strontium Contaminated Soils" Agronomy 12, no. 6: 1311. https://doi.org/10.3390/agronomy12061311

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