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Article

Deciphering Whether Illite, a Natural Clay Mineral, Alleviates Cadmium Stress in Glycine max Plants via Modulation of Phytohormones and Endogenous Antioxidant Defense System

by
Sang-Mo Kang
1,2,
Shifa Shaffique
1,
Md. Injamum-Ul-Hoque
1,
Ho-Jun Gam
1,
Ji-In Woo
1,
Jin Ryeol Jeon
1,
Da-Sol Lee
1,
In-Jung Lee
1 and
Bong-Gyu Mun
2,3,*
1
Department of Applied Biosciences, College of Agriculture and Life Sciences, Kyungpook National University, Daegu 41566, Republic of Korea
2
Institute of Agricultural Science and Technology, Kyungpook National University, Daegu 41566, Republic of Korea
3
Department of Environmental and Biological Chemistry, Chungbuk National University, Cheongju 28644, Republic of Korea
*
Author to whom correspondence should be addressed.
Sustainability 2024, 16(22), 10039; https://doi.org/10.3390/su162210039
Submission received: 7 October 2024 / Revised: 11 November 2024 / Accepted: 13 November 2024 / Published: 18 November 2024
(This article belongs to the Special Issue Sustainable Agriculture and Restoration of Agroecosystem Affected by Climate Change)
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Abstract

:
Globally, cadmium (Cd) stress dramatically reduces agricultural yield. Illite, a natural clay mineral, is a low-cost, environmentally acceptable, new promising method of reducing the heavy metal (HM) stress of cereal crops. In research statistics, there is little research on stress tolerance behavior of Illite (IL) on an experimental soybean plant. In the present study, we took IL and examined it for tolerance to Cd, as well as for other plant-growth-promoting (PGP) characteristics in Glycine max (soybean). The results showed that applying clay minerals in different concentrations enhanced the level of SA (defense hormone) and reduced the level of ABA (stress hormone). Cd 1 mM significantly reduces plant growth by altering their morphological characteristics. However, the application of IL significantly enhanced the seedling characteristics, such as root length (RL), 29.6%, shoot length (SL), 14.5%, shoot fresh biomass (SFW), 10.8%, and root fresh biomass (RFB), 6.4%, in comparison with the negative control group. Interestingly, IL 1% also enhanced the chlorophyll content (C.C), 15.5%, and relative water content (RWC), 12.5%, in all treated plants. Moreover, it resulted in an increase in the amount of superoxide dismutase (SOD), phenolics, and flavonoids in soybean plants, while lowering the levels of peroxidase (POD) and H2O2. Furthermore, compared to control plants, soybean plants treated with the Illite exhibited increased Si absorption and lower Cd levels, according to inductively coupled plasma mass spectrometry (ICP-MS). Thus, the IL can operate as an environmentally beneficial biofertilizer and sustainable approach under Cd stress by promoting plant development by activating signaling events.

1. Introduction

Heavy metals (HMs) naturally occur in trace quantities or remain sequestered in geological formations until industrial processes render them accessible, utilized, and accumulated. HMs accumulate in soils due to anthropogenic activities, including drilling, radiation, sewage pollution, and the utilization of metalloids. Plants may find soil toxic if heavy metal concentrations exceed a certain threshold [1,2]. Over the past few decades, heavy metal contamination in agricultural systems has increased globally, and its scope and extent are somewhat correlated with each nation’s level of environmental protection awareness [3]. Cadmium (Cd) lacks a distinct transporter protein and typically enters the roots via specialized transporter proteins, subsequently moving to the xylem or phloem tubes through either plastid or coplanar pathways [4,5]. Stressed plants exhibit [6] various signs and symptoms, including reduced germination metrics, stunted growth, chlorosis, necrosis, and root abnormalities. These traits are caused by extreme HMs interfering with plant growth, development, and reproduction, even though plant tolerance to these metals varies [7,8,9,10,11]. HMs have antagonistic effects on plant physiological and biochemical processes. They cause plant intracellular enzymes to become inactive and denatured, alter protein structures, and disturb membrane integrity. These effects then have an impact on plant growth. Furthermore, introducing toxic HMs into plant tissues causes a rise in reactive oxygen species (ROS), which upsets the redox balance [12,13]. As a result, an increase in superoxide anion (O2−) and hydrogen peroxide (H2O2) leads to additional membrane damage, biological macromolecule degradation, a significant increase in unsaturated fatty acid induction, and the death of oxidative cells [14,15]. Plants possess a certain resilience in response to the intrusion of toxic HMs. These responses primarily involve the removal of ROS caused by HMS, chelation using metallothionein and/or photoheating, compartmentalization in cell walls and intracellular vesicles, and inhibition of ion uptake from soil. Regretfully, much like all living things, plants can only control HMS to a limited extent before their defense mechanisms are overwhelmed [16,17].
Among all the HMs, Cd is more toxic, causing restricted plant growth and development. However, several established methods are being carried out to reduce Cd stress, such as genetic engineering, agrochemical manifestations or growth regulators, and beneficial microbes [18]. Now, researchers are giving more attention to eco-friendly techniques that do not interfere with the normal physiological function of plants [19,20,21].
Illite (IL) is a phyllosilicate, a type of clay mineral. Illite minerals have a chemical formula (K1–1.5A14[Si7–6.5A11–1.5O20] (OH4)) with a 2:1 layer structure with an interlayer assembly. Monovalent cations, usually K+, occupy interlayer sites to balance the negative charge created by Al3+ occupying 25% of the tetrahedral sites [22,23,24]. IL’s multilayered structure combines the characteristics of dispersible and swelling clays. Because of these special qualities, it is difficult to stabilize IL clays. IL has an uneven shape with lengthy spines or granules. There are only a few studies present on IL and its bioactive potential to mitigate HMs [25].
Soybean (Glycine max) is an important cereal crop that has been cultivated all over the world due to its nutrient composition. It contains several important phytonutrients that make it more valuable. However, soybean, like other plants, is sessile and must contend with HM stress throughout its life cycle [26,27]. In the present study, IL was used as a treatment option at 1% and 2% concentrations to reduce the Cd stress in the experimental soybean plant.

2. Methodology

2.1. Pot Experiment

The present experiment was conducted at the crop physiology lab, at Kyungpook National University, Daegu, South Korea. The soybean seeds were purchased from the National Resource Center of Korea and the surface of the seeds was sanitized with 70% ethanol and sowed for germination. After 5 days, the uniform seedlings were taken and transplanted into a pot 10 cm × 9 cm long (0.5 L volume). After 10 days, the seedlings were placed in a new pot environment and the plant was categorized into 4 groups: normal control group that received 50 mL water only, a negative control group that received Cd (1 mM) for three days (50 mL/day), and the treatment groups that received the Illite 1% or 2%. After 10 days of the treatment, the plants were harvested and immediately put into liquid nitrogen for further analysis. After that, plant samples were freeze-dried for further analysis. The process of the plant experiment was followed as described by [15], with slight modification.

2.2. Measurement of Seedling Characteristics and Chlorophyll Content with SPAD

Immediately after the harvesting, the seedling characteristics were noted down, such as root SL, RL, and SFB, and C.C as SPAD values were calculated with a SPAD-502 chlorophyll meter (Konica Minolta, Tokyo, Japan) by following the method. Moreover, the technical fluorescent and energy flux parameters were calculated by portable infrared gas analyzer for photosynthesis (LCproT, ADC, Herts, UK) [28].

2.3. Estimation of Relative Water Content (RWC)

The RWC of plant leaves was determined by following the protocol [6]. Briefly, every third leaf’s fresh weight (FW) was noted and then water-logged in distilled water for 8 h. After 8 h, the turgid weight (TW) was assessed. After that, the leaf was placed in an oven to dry at 75–80 °C for 8 h to find out the dry weight (DW). The RWC was calculated using the following equation
Relative water contents = Fresh weight − dry weight/turgid weight − dry weight × 100

2.4. Phytohormone Analysis (ABA and SA)

Endogenous ABA was extracted and quantified using established methods [29]. The ABA standard [(±)−3,5,5,7,7,7-d6] was introduced during the sample extraction process to detect and compare peak values. The quantification was carried out using an Agilent, Santa Clara, CA, USA, 6890 N Gas Chromatograph. A software program called ThermoQuset (MD800), Manchester, UK, was used to calculate the reaction to ions [m/e of 162 and 190 for Me-ABA and 166 and 194 for Me-(2H6)-ABA] (Supplementary Table S1).
Endogenous SA was calculated using established methods [29]. In brief, 100% methanol was used for the extraction process. Filtration, drying, concentration, and partitioning by ethyl acetate/cyclopentane/isopropanol (100:99:1, v/v) were then carried out. A C18 reverse-phase HPLC column (HP hypersil ODS, particle size 5 μm, pore size 120 Å, Waters; size 3.9 × 300 mm) (Supplementary Table S2) was used to analyze the resultant solution at a flow rate of 1.0 mL/min.

2.5. Amino Acid Evaluation

As previously mentioned, measurements of essential amino acids were carried out on control and treated soybean plants. A heat block was used to re-suspend roughly 0.1 g of dried plant powder in 1 mL hydrochloric acid (6 N HCl) for 24 h at 120 °C. The samples were then evaporated at 80 °C for a further 24 h. The material underwent additional vertexing using 1 mL of 0.02 N HCl, dilution with distilled water, and filtration using a 0.22 µm syringe filter from StarLab, Hamburg, Germany following the method [30]. An amino acid analyzer (L-8900 Hitachi, Osaka, Japan) was used to test the amino acid composition, and the results were compared to standards (Sigma-Aldrich, Darmstadt, Germany).

2.6. Analysis of Ions by ICP

The silicon (Si), aluminum (Al), and Cd2+ levels were determined using ICP-MS analyses in both controls and treated plants (ICP-MS. Optima 7900DV, PerkinElmer, Waltham, MA, USA). On a heating block, powdered dried samples (0.05 g) were reconstituted in 1.5 mL of 70% HNO3 and heated to 110 °C for 1.5 h. The samples were directly used for ICP analysis after being diluted in deionized water to obtain a final volume of 20 mL and then filtered using 0.22 µm syringe filters from StarLab, Germany. The entire protocol was followed [31].

2.7. Antioxidant Analysis

The activity of CAT was analyzed following previously published protocols [29], which utilized the method of calculating H2O2 absorption at 240 nm. There was 50 mM potassium phosphate buffer (pH 7.0) and 15 mM hydrogen peroxide in the reaction buffer. Briefly, the reaction was commenced by adding 100 μL of the enzyme extract to the reaction mixture. After one minute, the reaction mixture’s H2O2 level was determined using the CAT enzyme activity-indicating extinction coefficient of 40 mM−1 cm−1. Next, 100 mg of the plant sample was extracted for APX activity using 1 mL of 50 mM phosphate buffer (pH 7.0), which contained 1 mM EDTA and 1 mM ascorbic acid. The homogenized material was centrifuged for 15 min at 4830× g (4 °C). The supernatant was combined with 0.3 mM H2O2, 15 mM ascorbic acid, and phosphate buffer solution (pH 7.0). At 290 nm, the reaction mixture’s absorbance was measured. We employed the procedure outlined to measure SOD activity, which entailed measuring the inhibitory capacity of SOD to reduce nitro blue tetrazolium (NBT) photochemically. The quantity of enzyme required to produce a 50% inhibition of the reduction of NBT, as measured at 560 nm, was calculated using SOD activity units. To measure POD and PPO activity, 0.1 mL of the supernatant was added to the reaction mixture along with 1.0 mL of 2% H2O2, 2.9 mL of 50 mM phosphate buffer (pH 5.5), and 1.0 mL of 50 mM guaiacol. Enzyme-free phosphate buffer served as the control. POD activity was computed as a unit change per minute after the absorbance was measured for three minutes at 470 nm. An approach that has been thoroughly explained earlier was employed to ascertain the decrease in GSH content. In summary, 3 mL of 5% trichloroacetic acid was used to homogenize 0.3 g of fresh soybean leaves, and then the mixture was centrifuged at 10,000× g for 15 min. After transferring 100 μL of the obtained supernatant to a fresh tube that already had 500 μL of 5,5′-dithiobis (2-nitrobenoic acid, 75.3 mg in 30 mL of 100 mM phosphate buffer, pH 6.8) and 3 mL of 150 mM NaH2PO4, the mixture was incubated for five minutes at 30 °C. Three duplicate measurements of the absorbance were made at 412 nm, as described in [32].

2.8. Statistical Analysis

The experiment employed a completely randomized design (CRD) with three replicates. Means were analyzed by one-way ANOVA using Duncan’s Multiple Range Test (DMRT) at p  ≤  0.05. Data were visualized using GraphPad Prism (v.8.1) software, with error bars representing the mean  ±  standard error (SEM) among the replicates.

3. Results

3.1. Effect of IL on Morphological Characteristics Under Cd Stress

The application of IL1 and IL2 enhanced all growth metrics compared to the NT conditions. Cd stress significantly decreased SL, RL, SFW, and RFW by 22.1%, 28.6%,41.4%, and 19.07%, respectively, compared to the NT conditions. The application of IL1 under Cd stress enhanced SL, RL, SFW, and RFW by 14.5%, 29.6%, 10.8%, and 6.4%, respectively, compared to only Cd-stressed plants. Similarly, IL2 application under stress conditions significantly improved SL, RL, SFW, and RFW by 30.0%, 24.7%, 22.9%, and 6.4%, respectively, compared to untreated Cd-stressed plants (Table 1). These findings demonstrate the substantial efficacy of IL2 application in alleviating the deleterious impacts of Cd stress and significantly augmenting the morphological features of soybean plants (Figure 1).
Significant differences between the treatments groups at p ≤ 0.05 are indicated by different lowercase letters on top of the bars. The standard error of the mean (SEM) between the replicates is shown by the error bar.

3.2. Effect of Illite on RWC and Chlorophyll

Cd stress significantly reduced soybean plants’ chlorophyll content and RWC. The application of IL significantly enhanced the chlorophyll and RWC in the plant. The present study suggests that in comparison with the negative group, it enhanced the relative water content in the IL1 and IL2 groups by 15.5 and 22.4%, respectively. Moreover, it also increases the level of chlorophyll content. No significant differences were seen when the comparison was made between the normal control and positive control. Interestingly, when comparisons were made between the Cd group and IL1 and IL2, results showed that it enhanced the chlorophyll content by 12.5% and 17.4%, respectively. The results are given in Figure 2.

3.3. Phytohormonal Analysis

Two phytohormones from the plant sample were quantified. The present study indicates that Cd stress significantly increased the level of ABA, while applying IL to plants lowered the level of ABA. Interestingly, when Cd stress was applied to plants, there was a significant reduction in the level of salicylic acid, but the application of IL augmented the levels of SA. More significantly, it is observed that IL2 enhanced the level of SA as compared to IL1, as shown in Figure 3.

3.4. Determination of Antioxidant Analysis

When the antioxidant parameters of the IL treatment were computed, the results were significant. The results suggest that although no considerable differences were seen in the non-treated and positive control groups, almost all the parameters showed the significance of the treatment. In Cd stress, the level of SOD was higher. But when IL1 and IL2 were applied, a reduction in the level of SOD was observed. Similarly, H2O2 is an oxidative burst marker. The level of H2O2 was higher but the application of treatment reduced the level of hydrogen peroxide and enhanced the level of flavonoids and polyphenols. POD and polyphenols were more significant dominant scavenging free radicals in 1% and 2% IL treatment, while flavonoid was only significant in 2%. The results are shown in Figure 4.

3.5. Results of the Technical Fluorescent and Energy Flux

The results reveal that the treatment of the IL1 and IL2 under Cd-induced stress significantly modulated the level of the technical fluorescence, specific energy flux, and quantum yield of all the treatment groups. The results are shown in Figure 5.

3.6. Findings of the Amino Acids

The amino acid determination is important in the determination of the effectiveness of the treatment. All the groups were analyzed for the evaluation of different levels of amino acids and the results show that Cd stress significantly impaired the level of all essential amino acids but the treatment with IL augmented their levels, as shown in Figure 6. Amino acid cluster comparisons were made to show the significance of treatment.

3.7. ICP Analysis

ICP analysis was computed to see the level of the ions Cd, silicon, and aluminum. The results showed that Cd stress enhanced the level of the Cd ions in the plant samples, but IL treatment lowered the level of Cd ions in all treated groups. Similarly, it lowered the level of aluminum by 12.2%, as shown in Figure 7.

4. Discussion

Plants are sessile, so they must be exposed to constant environmental stress throughout their life [33]. Ecological stress, both biotic and abiotic, reduces plant production [34,35]. Among the abiotic stress, HMs are an important abiotic limiting stress that lower crop production [36]. Cd is a hazardous metal that not only reduces crop production, but also enters the food chain as a lethal agent. It is the need of the hour to eliminate such a hazardous material from the food chain by an eco-friendly approach [37,38].
In this study, soybeans were used as an experimental plant to see the effectiveness of IL under Cd stress. This study used soybean because it is a cereal crop that is very sensitive to Cd stress. Soybean seedlings were exposed to Cd stress and IL was applied to them to see the effectiveness of IL.
After exposure to stress and treatment, several physiological and biochemical indicators of the plant were recorded to see the effectiveness of the treatment. Morphological characteristics are important to ascertain the significance of the treatment [39]. When IL was applied under Cd-induced stress, there was a substantial enhancement in RL, SL, SFW, and RFW. The results show that in comparison with the negative control, application of clay minerals enhanced the seedling characteristics of soybeans. Our results agree that it is a natural eco-friendly clay mineral that tends to modulate the seedling characteristics of plants. Several previous studies reported that IL has positive effects on plant prediction and stress tolerance [25,40,41]. C.C are important markers of the plant’s photosynthesis [42,43]. The results were favorable when C.C was compared between the not stressed plant and the two different concentrations of IL, where a non-significant difference was noted. However, when we applied IL2, there was little enhancement in chlorophyll content and leaf area. When comparisons were made between the negative control group and the treatment group, the results were significant and the results showed that IL application not only enhanced the leaf’s RWC but also enhanced the chlorophyll content, which ultimately showed that it enhanced the photosynthesis and reserved the water for the plant.
Phytohormones are an important biological precursor in plant cell modulation. In the present study, the two phytohormones ABA and SA levels were monitored [44,45,46]. The results show that although no significant differences were seen between the normal control and IL treatment when the Cd was applied, it enhanced the level of the ABA, which acted as a signaling molecule, and the level of ABA was strikingly higher under Cd stress in comparison to other treatment groups. ABA is a primary stress-related hormone that regulates various biological processes and facilitates plants in managing HM stress management [47]. It regulates the translocation of toxic metals from the roots to the shoots, induces stomatal closure, and reduces transpiration, thereby limiting HM transfer [48,49,50]. When the IL was applied, it reduced the level of ABA. Our results agree that IL has the potential to modulate the level of endogenous phytohormones that regulate plant stress tolerance [5,51]. Similarly, when the SA level was checked, in comparison with the negative control group, it was revealed that IL lowered the level of Cd stress by improving the level of SA. It acts as a defensive hormone in plants; if there is stress, the SA level becomes higher to cope with the stress [52,53]. Under HM stress, SA interacts with other phytohormones (e.g., IAA, ABA, and GA) to stimulate antioxidant defense system, thereby altering HM-treated plants and facilitating the counteractions of HM stress [54].
Extending the plant experiment, the six antioxidant parameters were also monitored to see the effectiveness of the treatment. The results revealed that under Cd stress, the level of SOD was pointedly higher than in other groups, due to SOD acting as a signaling molecule and activating the membrane-bound receptors. Moreover, it also promotes the apoptosis of cells [55,56,57]. However, when IL was applied to soybean plants, it reduced the SOD level, which showed the significance of the treatment. However, when catalase levels were compared, no significant difference was seen in all treatment groups. H2O2 is an important product of the redox that is attained under plant stress. The level of H2O2 was notably higher in the negative control group, but the IL treatment lowered the level of hydrogen peroxide and minimized the level of stress. Interestingly, it was seen that IL treatment enhanced the level of POD, polyphenol, and flavonoid in all treatment groups. The antioxidant parameters are part of the defense system, and all the results show that IL treatment enhanced the antioxidant defense biomarkers. Our results agree that IL has the potential to reduce stress by modulating the antioxidant defense system [23,58,59,60]. Moreover, the technical fluorescence parameters were monitored, with the results showing that IL has the potential to lower its stress by modulating the technical fluorescence, specific energy flux, quantum yield efficiencies, and phenological energy efflux. The level of amino acids results show that Cd reduced the essential amino acid; however, the IL treatment enhanced the level of amino acids in all treatment groups. Amino acids are essential metabolites that play crucial roles in cellular osmosis, mineral nutrient absorption, heavy metal detoxification, and signaling. Moreover, amino acids are the precursor of some essential phytohormones [61]. Our study concluded that IL is the alternative approach to cope with Cd stress and it is the best gateway towards sustainable agriculture production. IL, a clay mineral, can undergo dissolution, releasing anions that subsequently bind to HM cations present in the soil, thereby facilitating surface adsorption and ion coordination [62,63]. This process significantly reduces HM efficacy, bioavailability, and mobility, and mitigates HM stress in plants [64]. Our results align with those of earlier research [60], which established that the application of IL significantly mitigated the Cd stress in plants. Lately, to confirm the effectiveness of the treatment, the ICP analysis was computed to confirm the significance of the treatment. The results reveal that the level of the Cd was quietly lowered in the treatment group when it was compared with the negative control. All results are in favor of IL treatment enhancing the efficiency of the Cd stress tolerance. However, studies on a larger scale at the molecular level are required to exhibit the exact mechanism of action.

5. Conclusion and Prospective Future Research

In conclusion, these findings collectively substantiate that the IL application effectively mitigates Cd stress in soybean plants through the modulation of phytohormones, antioxidants, nutrient uptake efficiency, and production of various amino acids. This study underscores the potential of IL as a sustainable and cost-effective biofertilizer to enhance crop productivity under HM stress conditions. Further advanced research is required to expose the long-term effects and broader application of IL in agriculture.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/su162210039/s1, Table S1: GC/MS-SIM conditions used for analysis and quantification of the ABA; Table S2: HPLC conditions used for SA analysis.

Author Contributions

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

Funding

This research was supported by the “Regional Innovation Strategy (RIS)” through the National Research Foundation of Korea (NRF), funded by the Ministry of Education (MOE) (2021RIS-001).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are contained within the article and Supplementary Materials.

Conflicts of Interest

The authors declare no conflict of interest.

Abbreviations

Reactive oxygen species: ROS; abscisic acid: ABA; salicylic acid: SA; Illite: IL; cadmium: Cd; superoxide dismutase: SOD; chlorophyll contents: C.C; peroxidase: POD; inductively coupled plasma mass spectrometry: ICP-MS; root fresh biomass: RFB; shoot fresh biomass: SFW; root length: RL; shoot length: SL; relative water contents: RWC; plant-growth-promoting: PGP.

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Figure 1. Impact of IL on the soybean plant growth under Cd-induced stress.
Figure 1. Impact of IL on the soybean plant growth under Cd-induced stress.
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Figure 2. (A) Measurement of chlorophyll content (SPAD) and (B) leaf relative water contents (RWC) in different treatment groups. Different lowercase letters on top of the bars show significant differences between the treatments at p  ≤  0.05. The error bar represents the mean  ±  standard error of the mean (SEM) among the replicates.
Figure 2. (A) Measurement of chlorophyll content (SPAD) and (B) leaf relative water contents (RWC) in different treatment groups. Different lowercase letters on top of the bars show significant differences between the treatments at p  ≤  0.05. The error bar represents the mean  ±  standard error of the mean (SEM) among the replicates.
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Figure 3. (A) Quantification of the abscisic acid (ABA) and (B) salicylic acid (SA) in all treatment groups. Different lowercase letters on top of the bars indicate significant differences between the treatments at p  ≤  0.05. The error bar represents the mean  ±  standard error of the mean (SEM) among the replicates.
Figure 3. (A) Quantification of the abscisic acid (ABA) and (B) salicylic acid (SA) in all treatment groups. Different lowercase letters on top of the bars indicate significant differences between the treatments at p  ≤  0.05. The error bar represents the mean  ±  standard error of the mean (SEM) among the replicates.
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Figure 4. Application of Illite under cadmium-induced stress modulated the antioxidant defense system, such as (A) superoxide dismutase (SOD), (B) catalase (CAT), (C) peroxidase, (D) hydrogen peroxide (H2O2), (E) polyphenolic activity and (F) flavonoids content. Different lowercase letters on top of the bars indicate significant differences between the treatments at p  ≤  0.05. The error bar represents the mean  ±  standard error of the mean (SEM) among the replicates.
Figure 4. Application of Illite under cadmium-induced stress modulated the antioxidant defense system, such as (A) superoxide dismutase (SOD), (B) catalase (CAT), (C) peroxidase, (D) hydrogen peroxide (H2O2), (E) polyphenolic activity and (F) flavonoids content. Different lowercase letters on top of the bars indicate significant differences between the treatments at p  ≤  0.05. The error bar represents the mean  ±  standard error of the mean (SEM) among the replicates.
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Figure 5. Modulation in technical fluorescence and specific energy flux parameters.
Figure 5. Modulation in technical fluorescence and specific energy flux parameters.
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Figure 6. Analysis of all the essential amino acids of all the treatment groups under Cd-induced stress.
Figure 6. Analysis of all the essential amino acids of all the treatment groups under Cd-induced stress.
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Figure 7. ICP analysis of the ions, such as, (A) silicon (Si), (B) cadmium (Cd), and (C) aluminium (Al) content in all Cd-induced stress treatment groups. Different lowercase letters on top of the bars indicate significant differences between the treatments at p  ≤  0.05. The error bar represents the mean  ±  standard error of the mean (SEM) among the replicates.
Figure 7. ICP analysis of the ions, such as, (A) silicon (Si), (B) cadmium (Cd), and (C) aluminium (Al) content in all Cd-induced stress treatment groups. Different lowercase letters on top of the bars indicate significant differences between the treatments at p  ≤  0.05. The error bar represents the mean  ±  standard error of the mean (SEM) among the replicates.
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Table 1. Morphological characteristics of soybean plants treated with IL under Cd stress conditions. Different letters denote the significant differences among the treatments at p  ≤  0.05.
Table 1. Morphological characteristics of soybean plants treated with IL under Cd stress conditions. Different letters denote the significant differences among the treatments at p  ≤  0.05.
TreatmentSL (cm)RL (cm)SFW (g)RFW (g)
NT (Non-treated)13.25 ± 0.57 a17.90 ± 0.86 ab2.68 ± 0.07 a1.94 ± 0.06 abc
   IL1 (Illite 1%)12.58 ± 0.58 a18.53 ± 0.64 a2.84 ± 0.07 a2.01 ± 0.11 ab
   IL2 (Illite 2%)13.67 ± 0.56 a17.18 ± 0.76 ab2.88 ± 0.09 a2.14 ± 0.05 a
   Cd10.32 ± 0.76 b12.77 ± 0.82 c1.57 ± 0.17 c1.57 ± 0.22 c
   IL1 + Cd11.82 ± 0.28 ab16.55 ± 0.66 ab1.74 ± 0.14 bc1.67 ± 0.16 bc
   IL2 + Cd13.42 ± 0.74 a15.93 ± 1.05 b1.93 ± 0.11 b1.67 ± 0.05 bc
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Kang, S.-M.; Shaffique, S.; Injamum-Ul-Hoque, M.; Gam, H.-J.; Woo, J.-I.; Jeon, J.R.; Lee, D.-S.; Lee, I.-J.; Mun, B.-G. Deciphering Whether Illite, a Natural Clay Mineral, Alleviates Cadmium Stress in Glycine max Plants via Modulation of Phytohormones and Endogenous Antioxidant Defense System. Sustainability 2024, 16, 10039. https://doi.org/10.3390/su162210039

AMA Style

Kang S-M, Shaffique S, Injamum-Ul-Hoque M, Gam H-J, Woo J-I, Jeon JR, Lee D-S, Lee I-J, Mun B-G. Deciphering Whether Illite, a Natural Clay Mineral, Alleviates Cadmium Stress in Glycine max Plants via Modulation of Phytohormones and Endogenous Antioxidant Defense System. Sustainability. 2024; 16(22):10039. https://doi.org/10.3390/su162210039

Chicago/Turabian Style

Kang, Sang-Mo, Shifa Shaffique, Md. Injamum-Ul-Hoque, Ho-Jun Gam, Ji-In Woo, Jin Ryeol Jeon, Da-Sol Lee, In-Jung Lee, and Bong-Gyu Mun. 2024. "Deciphering Whether Illite, a Natural Clay Mineral, Alleviates Cadmium Stress in Glycine max Plants via Modulation of Phytohormones and Endogenous Antioxidant Defense System" Sustainability 16, no. 22: 10039. https://doi.org/10.3390/su162210039

APA Style

Kang, S.-M., Shaffique, S., Injamum-Ul-Hoque, M., Gam, H.-J., Woo, J.-I., Jeon, J. R., Lee, D.-S., Lee, I.-J., & Mun, B.-G. (2024). Deciphering Whether Illite, a Natural Clay Mineral, Alleviates Cadmium Stress in Glycine max Plants via Modulation of Phytohormones and Endogenous Antioxidant Defense System. Sustainability, 16(22), 10039. https://doi.org/10.3390/su162210039

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