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Research Article
2025
:37;
10552025
doi:
10.25259/JKSUS_1055_2025

Salicylic acid-mediated growth promotion, pigment enhancement, and secondary metabolite augmentation in Brassica juncea L. plants under thiamethoxam pesticide stress

, , , , , , ,
aDepartment of Botanical and Environmental Sciences, Guru Nanak Dev University, Amritsar, Punjab, India
bDepartment of Earth and Environmental Sciences, University of Ottawa, Ottawa, Canada
cDepartment of Botany and Microbiology, Faculty of Science, King Saud University, Riyadh 11451, Saudi Arabia
dDepartment of Botany, MGDC Charar-I-Sharief-191112, Budgam, Jammu and Kashmir, India
eResearch and Development Cell, Lovely Professional University, Phagwara, Punjab, 144411, India
fUniversity Centre for Research and Development, Chandigarh University, Mohali-140413, Punjab, India

* Corresponding author E-mail address: renubhardwaj82@gmail.com (R. Bhardwaj); parvaizbot@yahoo.com (P. Ahmad)

Received: , Accepted: ,
© 2025 Journal of King Saud University – Science - Published by Scientific Scholar
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This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-Share Alike 4.0 License, which allows others to remix, transform, and build upon the work non-commercially, as long as the author is credited and the new creations are licensed under the identical terms.

Abstract

Thiamethoxam (TMX) is a second-generation insecticide and belongs to the neonicotinoid class of pesticides. These synthetic compounds are applied to food crops to eliminate pests, particularly insects, and to maintain yields. Consequently, due to their higher solubilities in water, these systemic compounds get incorporated into the edible plant tissues and show impaired growth and developmental aspects. The objective of the present study was to evaluate the harmful effects of TMX pesticide on Brassica juncea L. and to uncover the defense responses exerted by the salicylic acid (SA) to curtail the losses and maintain the integrity of B. juncea field plants for 30, 45, and 60 days after growth. Experimentation with field plants was conducted, and some of the morphophysiological, biochemical, and secondary metabolites associated parameters were investigated in the B. juncea crop. The morphological metrics were found to be lowered in TMX stress conditions. Whereas the contents of photosynthetic pigments, including total chlorophyll content, were lowered, on the contrary, carotenoid and xanthophyll contents were enhanced under the TMX stressed conditions. The gaseous exchange parameters also showed a decline in the observed values. Subsequently, the enzymatic antioxidants and phenolic contents were marked by an increase under the TMX-stressed plants. Notably, the activities of antioxidative enzymes, such as superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), and ascorbate peroxidase (APOX), were significantly enhanced in plants supplemented with exogenous SA. The highest concentration of SA, such as SA3 (1mM), showed significant stress ameliorative potentials in all the studied parameters.

Keywords

Antioxidants
Gaseous exchange parameters
Neonicotinoids
Phytohormones
Photosynthetic pigments
Secondary metabolites

1. Introduction

Pesticides play a vital role in contemporary agriculture, being used to safeguard crops against weeds, diseases, and insect pests. This ultimately improves crop yield and guarantees food security. Nevertheless, the extensive and unselective application of these substances has generated substantial apprehensions regarding the protection of the environment and the quality of food, especially considering the growing worldwide population and the heightened need for agricultural production (Jiang et al., 2022; Tang et al., 2025). Neonicotinoids, including thiamethoxam (TMX), are highly efficient pesticides in controlling pests. But, they negatively impact the environment and human health, thus requiring meticulous regulation (Yi et al., 2023; Wang et al., 2025). Subsequently, neonicotinoids have been documented to disrupt various physiological processes in plants, leading to significant morphological and biochemical changes. For instance, Liu et al. (2021) and Sharma et al. (2016) demonstrated that imidacloprid, another neonicotinoid, adversely affects plant growth, pigment synthesis, secondary metabolites, and antioxidants activity in Cucumis sativus L. and Brassica juncea L. Similarly, Todorova et al. (2023) reported that pesticide stress influences key gas exchange parameters such as intercellular CO2 concentration, stomatal conductance, transpiration rate, and net photosynthesis.

TMX has proven to be highly effective in managing sucking and biting insect pests. This is mostly owing to its exceptional ability to get absorbed and transported within the plant system (Wang et al., 2020). Research has demonstrated that TMX can concentrate in the soluble parts of plant cells, leading to growth retardation and reduced photosynthetic activity (Cavusoglu et al., 2012; Wang et al., 2020; Singh et al., 2025). Research conducted on Zea mays and Brassica rapa var. chinensis has provided more evidence that TMX adversely affects the efficiency of photosynthesis, levels of pigments, and overall health of the plants (Todorenko et al., 2021).

Brassica juncea L., also referred to as Indian mustard, is a financially important oilseed crop that is nonetheless susceptible to the negative impacts of abiotic stressors as pesticides (Kour et al., 2024). Plants frequently utilize enzymatic antioxidants, secondary metabolites, and phytohormones to alleviate damage and restore physiological equilibrium in stressful settings (Khan et al., 2023; Wang et al., 2025). Salicylic acid (SA), a phenolic molecule, is crucial in improving plant resilience against many stresses. It enhances growth and development by facilitating seed germination, promoting chlorophyll biosynthesis, enhancing enzymatic potentials, and improving overall plant vitality. Significantly, scientific evidence has demonstrated that SA enhances the plant’s defense mechanisms against the harmful effects of pesticides (Khatami et al., 2022; Li et al., 2025). For instance, the external administration of SA has been discovered to enhance plant height, biomass accumulation, and photosynthetic parameters when plants are exposed to the stress of fomesafen pesticide (Li et al., 2022).

The objective of this study is to investigate the impact of SA on growth, photosynthetic characteristics, antioxidant potentials, and accumulation of phenolic compounds in Brassica juncea L. when subjected to TMX-induced stress. This research aims to enhance our understanding of potential methods for regulating and improving the response of agricultural crops to pesticide stress.

2. Materials and Methods

2.1 Plant material and design of experiment

The procurement of authenticated and disease-free seeds of Brassica juncea L. (var. RLC3) was conducted at the Seed Technology Unit of Punjab Agriculture University, Ludhiana, Punjab. Initially, the seeds were sterilized using Sodium hypochlorite solution (5% v/v) for 10 min, followed by rinsing with DDW. The seeds were subjected to priming using three distinct dosages of SA (SA) (SA1 0.01mM, SA2 0.1mM, and SA3 1mM) over a period of 8 h. A stock solution of TMX pesticide was prepared, and the experimental concentrations were selected based on the IC50 values (50% growth inhibition). Finally, the treated and untreated seeds of B. juncea with selected SA concentrations were sown in pots containing soil with varied concentrations of clay: sand: manure (3:1:1) amended with pesticide doses of (0 and 750 mg/kg) in soil. Plants were picked for harvest on the 30, 45, and 60 days after seed sowing for subsequent analysis.

2.2 Growth parameters

The growth attributes of plants were assessed for 30, 45, and 60 days after growth. Shoot length and root length were checked using the “cm” scale.

2.3 Photosynthetic pigments

Chlorophyll and carotenoid amounts were examined by adopting the protocols of Arnon (1949) and Maclachlan and Zalik (1963). Then, 1 g of plant sample was pulverized in 4 mL of acetone (80%) and was allowed to be centrifuged at 13000 rpm (4°C, 20 min). The isolate was taken for the quantification of chlorophyll and carotenoid, and the readings were recorded at 645 and 663 nm for the total chlorophyll content, whereas the carotenoid contents were observed at 480 and 510 nm, respectively.

Xanthophyll levels were achieved by implementing the AOAC protocol given by Lawrence (1990). Dried and crushed leaf samples up to 50 mg were taken in a flask, followed by the addition of a specific extractant mixture (30 mL), and kept for shaking for 10-15 min. Subsequently, 40% methanolic KOH (2 mL) was mixed into the flask and reintroduced into a water bath (20 min, 56°C). After cooling, the flask was subjected to incubation (60 min), administered with hexane (30 mL), intensive shaking (1 min), and followed by the addition of sodium sulfate (10%) solution to maintain a 100 mL volume. Following this, it was vigorously shaken (1 min), incubated in the dark (1 h), and finally, the 50 mL volumetric flask was adopted to collect the upper phase. Consistent addition of hexane was followed to attain a 50 mL volume, further mixing, and optical density was recorded at 474 nm.

2.4 Gaseous exchange parameters

The gaseous exchange indices, such as Net photosynthetic rate (Pn), Stomatal conductance (Gs), Inter-cellular CO2 concentration (Ci), and Transpiration rate (E), were assessed by adopting an open photosynthesis system IRGA (LI-COR LI-6400XT, instrument, USA). The air was entitled to pass through the analysis and reference lines simultaneously, originating from a consistent source and maintaining a constant CO2 level. These parameters, Pn, Gs, Ci, and E, were evaluated by analyzing the H2O and CO2 concentration differences detected in the air passing into the reference chamber and the air exiting the sample chamber. The measurements were conducted during the morning hours (10:00 to 12:00), following the sunny days.

2.5 Antioxidative enzyme activity

Superoxide dismutase (SOD) activity was performed using the method developed by Kono (1978). The plant sample was thoroughly crushed in sodium carbonate buffer (volume 3 mL with 50 mM conc and pH 7.8) and subjected to centrifugation at 12000 rpm (20 min and at 4°C). The ultimate reaction necessitates the inclusion of hydroxylamine hydrochloride (1mM), enzyme sample, 0.03% Triton X-100, 24 µM nitro blue tetrazolium, Na2CO3 buffer (50 mM, pH 7.8), and 0.1 mM EDTA. The readings were obtained at a wavelength of 560 nm.

Activity of peroxidase (POD) was performed according to the procedure provided by Pütter (1974). The sample was crushed in PPB (100 mM, pH 7) and then subjected to centrifugation at 12000 rpm (4°C, 20 min). The final resulting mixture consists of an enzyme sample, H2O2, guaiacol, phosphate buffer, and H2O2 solution. The intensity was measured at a wavelength of 436 nm.

Catalase (CAT) activity was estimated using the stringent procedure of Aebi (1984). Plant sample was homogenized in phosphate buffer (50 mM, pH 7) and spun at 12000 rpm (4°C, 20 min). The final reaction mixture consisted of 50 mM PPB (50 mM), H2O2 (15 mM), and enzyme extract. The spectroscopic readings were collected at a wavelength of 240 nm.

Ascorbate peroxidase (APOX) activity was determined using the method established by Nakano and Asada (1981). The fresh sample was ground up in PPB (50 mM, pH 7) and subjected to spinning at 12000 rpm (20 min, 4°C). Ultimately, the enzyme extract was added to the resulting solution consisting of H2O2 (1mM) and 0.5 mM ascorbate (PPB, 50 mM, pH 7.0). The spectroscopy was performed at a wavelength of 290 nm.

2.6 Phenolic compounds

Anthocyanin amounts were calculated by utilizing the methodology suggested by Mancinelli (1984). Then, 1 g of the vegetative sample was subjected to crushing in an acidified extractant (3 mL) having solvents in a ratio of 79:20:1 for methanol, double-distilled water, and hydrochloric acid. The mixture was administered for centrifugation at 1500 g (20 min), and the optical density was measured at 530 and 657 nm, respectively.

Analysis of total flavonoids was conducted by implementing the approach of Kim (2003). A vegetative sample (100 mg) was implemented for pulverization in absolute methanol (4 mL), and the homogenate underwent centrifugation at 13000 rpm (20 min, 4°C). Followed by the mixing of supernatant (1mL) into DDN (4 mL), and sodium nitrite (0.3 mL). Subsequent addition of aluminum chloride (0.3 mL) and kept for incubation for 5 min. Finally, a volume of 2 mL of Sodium hydroxide (NaOH) was mixed, and pink coloration took place. Subsequent addition of DW (2.4 mL) and absorbance was noted at 510 nm.

Total phenols were assessed by exploiting the approach of Singleton and Rossi (1965). For this, 400 mg of oven-dried tissues were chopped and immersed in 60 % ethanol (40 mL). After vigorous shaking, the test tubes were introduced to a water bath for 10 min at 60°C. Subsequently, the filtration and another round of extraction. Dilution of the extractant was conducted by the addition of 60% ethanol (100 mL). Furthermore, successive dilution of 2.5 mL of the isolate was done by adding 2.5 mL of distilled water. Finally, the upper mixture was taken (2 mL), and FC reagent (10 mL) and 8 mL Na2CO3 were added. The reaction concoction was kept for incubation for 2 h, and the OD was taken at 765nm.

2.7 Statistical analysis

The findings were presented as means ± standard error (S.E) based on three independent replicates. The data were evaluated using one-way analysis of variance (ANOVA) with SPSS software version 23. A Tukey test was performed at a significance threshold of p ≤ 0.05. Also, the tabulated values were expressed as the mean ± standard deviation (SD) of the mean at a significance value of p ≤ 0.05.

3. Results

3.1 Growth parameters

The findings showed a significant reduction in the root and shoot length when plants were exposed to the TMX stressed conditions by 35.066% and 28.793% in 30 days, 33.307% and 23.238% in 45 days, and 35.968% and 27.535% in 60-day-old plants in comparison to the control groups. However, SA administered plants with SA3 (1mM) concentrations and subjected to TMX environment elicited noticeable improvement of 53.621%, 61.413%, and 54.835% in root length as well as a significant increment of 43.288%, 40.062%, and 39.593% in shoot length of 30, 45, and 60 days old plants, respectively, in contrast with the TMX only treated plants (Fig. 1).

The impact of varying doses of SA (SA1 0.01 mM, SA2 0.1 mM, and SA3 1 mM) on the growth metrics, specifically root and shoot length, in 30-, 45-, and 60-day-old B. juncea plants in the presence of TMX pesticide stress. The data presented here comprises the means of three separate replicates, with the standard error (SE) indicated. The bar graphs display mean values of several treatments, with distinct superscripts indicating significant differences at a significance level of p ≤ 0.05 (according to Tukey’s test).
Fig. 1.
The impact of varying doses of SA (SA1 0.01 mM, SA2 0.1 mM, and SA3 1 mM) on the growth metrics, specifically root and shoot length, in 30-, 45-, and 60-day-old B. juncea plants in the presence of TMX pesticide stress. The data presented here comprises the means of three separate replicates, with the standard error (SE) indicated. The bar graphs display mean values of several treatments, with distinct superscripts indicating significant differences at a significance level of p ≤ 0.05 (according to Tukey’s test).

3.2 Photosynthetic pigments

Plants that were exclusively exposed to soils treated with TMX experienced a significant decrease in total chlorophyll content by 25.223%, 16.688%, and 11.634% in 30, 45, and 60 days, respectively, compared to plants in the control group. However, seeds that were treated with a concentration of 1mM of SA3 prior to planting and exposure to TMX, showed a significant increase in the levels of total chlorophyll content by 23.084%, 10.99%, and 13.830% compared to those treated exclusively with TMX for 30, 45, and 60 days of the growth period (Fig. 2).

The impact of varying doses of SA (SA1 0.01mM, SA2 0.1 mM, and SA3 1 mM) on the photosynthetic pigments, specifically total chlorophyll content, carotenoid content, and xanthophyll content, in 30-, 45-, and 60-day-old B. juncea plants under the presence of TMX pesticide stress. The statistical information provided here consists of the averages of three distinct replicates, with the standard error (SE) given. The bar graphs depict the average values of several treatments, with different superscripts showing significant differences at a significance level of p ≤ 0.05 (as determined by Tukey’s test).
Fig. 2.
The impact of varying doses of SA (SA1 0.01mM, SA2 0.1 mM, and SA3 1 mM) on the photosynthetic pigments, specifically total chlorophyll content, carotenoid content, and xanthophyll content, in 30-, 45-, and 60-day-old B. juncea plants under the presence of TMX pesticide stress. The statistical information provided here consists of the averages of three distinct replicates, with the standard error (SE) given. The bar graphs depict the average values of several treatments, with different superscripts showing significant differences at a significance level of p ≤ 0.05 (as determined by Tukey’s test).

Plants documented a noticeable improvement in carotenoid content by 22.564%, 13.227%, and 19.469% when subjected to TMX-stressed conditions and checked against the control plants. Applying a SA3 (1mM) concentration of SA to seeds, before they get exposed to TMX-treated soils, showed a significant increment in the carotenoid levels by 33.847%, 29.685%, and 24.988% in 30, 45, and 60 days of plants, respectively, in contrast to those just exposed to TMX-treated soils (Fig. 2).

The investigation revealed higher xanthophyll content of 41.078%, 31.672%, and 34.146% in 30, 45, and 60-day-old plants, respectively, when subjected to TMX as compared to the control plants. Remarkably, exogenous applications of SA to seeds supplemented with 1mM dosage and grown in TMX-treated soils showed considerably larger amounts of xanthophyll contents by 39.117%, 35.945%, and 23.409% in 30, 45, and 60 days of plants, exclusively with the TMX-exposed plants (Fig. 2).

3.3 Gaseous exchange parameters

Net photosynthesis rate gets substantially lowered under the TMX stressed condition by 18.988%, 18.518%, and 36.170% in 30, 45, and 60 days of plants, respectively, when analyzed against the control plants. However, an abrupt rise in net photosynthesis rate was assessed when the plants were pre-soaked in SA3 (1mM) dosage and further introduced to the pesticide-exposed soils by 20.445%, 27.534%, and 51.890% over three different growth periods of 30, 45, and 60 days, and checked against the only TMX-treated plants (Table 1).

Table 1. The impact of varying doses of salicylic acid (SA1 0.01 mM, SA2 0.1 mM, and SA3 1 mM) on the net photosynthetic rate, and stomatal conductance of 30-, 45-, and 60-day-old B. juncea plants, under the TMX stress conditions. Significance level checked at P ≤ 0.05, designated with*.
Treatments
 Net photosynthetic rate (µmole CO2 m -2 s -1) Mean ± SD
 Stomatal Conductance (mmol H2O m -2 s -1) Mean ± SD
TMX (mg/Kg) SA (mM/L) 30 Days 45 Days 60 Days 30 Days 45 Days 60 Days
0 0 38.76 ± 0.572 56.16 ± 0.907 62.98 ± 1.602 0.806 ± 0.068 1.072 ± 0.073 2.026 ± 0.080
0 0.01 38.56 ± 1.023 57.90 ± 1.498 65.92 ± 1.298 0.878 ± 0.061 1.145 ± 0.314 2.388 ± 0.392
0 0.1 39.90 ± 1.349 58.46 ± 1.173 65.10 ± 2.319 0.853 ± 0.045 1.149 ± 0.438 2.600 ± 0.402
0 1 43.18 ± 1.052 65.58 ± 1.329 70.12 ± 1.406 0.972 ± 0.087 1.736 ± 0.365 3.292 ± 0.256
750 0 31.40 ± 1.387 45.76 ± 1.250 40.20 ± 1.431 0.627 ± 0.081 0.782 ± 0.036 0.985 ± 0.101
750 0.01 32.32 ± 1.599 48.28 ± 1.175 45.68 ± 1.553 0.666 ± 0.064 0.839 ± 0.098 1.502 ± 0.218
750 0.1 36.48 ± 1.368 49.94 ± 1.089 51.42 ± 1.540 0.687 ± 0.127 0.905 ± 0.063 2.062 ± 0.136
750 1 37.82 ± 0.683 58.36 ± 1.176 61.06 ± 1.023 0.818 ± 0.016 1.129 ± 0.131 2.574 ± 0.320
F-ratio 54.249* 146.678* 236.224* 12.380* 7.615* 35.644*

The analysis revealed that plants subjected to TMX treatment for 30, 45, and 60 days showed a decrease in stomatal conductance by 22.285%, 27.032%, and 51.362%, respectively, compared to control plants. Seeds specifically exposed to a higher concentration of SA (SA), specifically 1 mM, and subsequently grown in soils with TMX pesticides, showed a significant improvement in stomatal conductance of 30.462%, 44.276%, and 161.213% in 30-, 45-, and 60-day-old plants, respectively, when compared to the untreated ones (Table 1).

The findings evaluated the impacts of TMX treatment on 30-, 45-, and 60-day-old plants, which exhibited a reduction in cellular CO2 concentration by 7.262%, 3.759%, and 9.580% respectively, compared to the untreated plants. Surprisingly, when SA was applied externally to seeds that were given an additional 1 mM treatment and cultivated in soils containing TMX, the plants exhibited significantly higher levels of 14.888%, 6.461%, and 10.890% for intercellular CO2 concentrations, when examined against the solely TMX-exposed ones in 30, 45, and 60 days of plants, respectively (Table 2).

Table 2. The impact of varying doses of SA (SA1 0.01mM, SA2 0.1 mM, and SA3 1 mM) on the cellular CO2 concentration, and transpiration rate of 30-, 45-, and 60-day-old B. juncea plants, under the TMX stress conditions. Significance level checked at P ≤ 0.05, designated with *.
Treatments
 Cellular CO2 Concentration (µmol CO2 mol-1) Mean ± SD
 Transpiration Rate (mmol H2O m-2 s -1) Mean ± SD
TMX (mg/Kg) SA (mM/L) 30 Days 45 Days 60 Days 30 Days 45 Days 60 Days
0 0 250.6 ± 4.277 276.6 ± 4.393 300.6 ± 6.066 9.080 ± 0.420 10.15 ± 0.641 11.04 ± 0.230
0 0.01 251.4 ± 4.159 279.4 ± 7.733 335.2 ± 51.67 9.678 ± 0.386 10.12 ± 0.570 11.30 ± 0.418
0 0.1 269.0 ± 16.73 287.0 ± 4.690 341.8 ± 14.51 9.704 ± 0.501 10.88 ± 0.258 11.56 ± 0.288
0 1 273.4 ± 4.159 293.8 ± 3.114 372.2 ± 55.09 10.82 ± 0.178 11.74 ± 0.230 12.64 ± 0.151
750 0 232.4 ± 9.889 266.2 ± 3.701 271.8 ± 1.483 7.306 ± 0.226 7.924 ± 0.375 7.792 ± 0.481
750 0.01 240.2 ± 5.974 271.8 ± 13.55 279.4 ± 5.899 7.850 ± 0.249 7.882 ± 0.101 8.874 ± 0.564
750 0.1 243.4 ± 6.348 274.6 ± 7.602 286.2 ± 4.324 8.260 ± 0.170 9.712 ± 0.486 9.590 ± 0.456
750 1 267.0 ± 13.09 283.4 ± 5.983 301.4 ± 2.966 9.440 ± 0.348 10.86 ± 0.056 11.26 ± 0.167
F-ratio 13.105* 7.726* 8.195* 60.212* 61.284* 91.814*

The investigation revealed that plants that were subjected to TMX treatment for 30, 45, and 60 days exhibited a decrease in transpiration rate of 19.537%, 21.946%, and 29.420%, respectively, compared to the unaffected plants, which displayed varying values. Interestingly, when seeds were treated with a higher concentration of SA, such as 1mM, and grown in pesticide-exposed soils showed a significantly higher transpiration rate by 29.208%, 37.079%, and 44.507% in 30-, 45-, and 60-day-old plants, when compared to the control plants (Table 2).

3.4 Antioxidative enzymes activity

Enhanced activities of SOD were detected in 30, 45, and 60 days of plant samples by 32.182%, 33.597%, and 33.261% when exposed to the TMX stress, compared to the untreated ones. A significant increase in SOD activity was observed when SA3 (1mM) was applied in seeds cultivated under TMX exposure by 52.822%, 56.063%, and 45.453% in contrast to the effects of TMX intervention alone (Fig. 3).

The impact of varying doses of SA (SA1 0.01 mM, SA2 0.1 mM, and SA3 1 mM) on the enzymatic antioxidants, specifically SOD, POD, CAT, and APOX, in 30, 45, and 60 days of B. juncea plants in the presence of TMX pesticide stress. The statistical data shown here contain the average values of three distinct replicates, together with their related standard error (SE). The bar graphs depict the average values of different treatments, with unique superscripts denoting statistically significant differences at a significance level of p ≤ 0.05, computed using Tukey’s test.
Fig. 3.
The impact of varying doses of SA (SA1 0.01 mM, SA2 0.1 mM, and SA3 1 mM) on the enzymatic antioxidants, specifically SOD, POD, CAT, and APOX, in 30, 45, and 60 days of B. juncea plants in the presence of TMX pesticide stress. The statistical data shown here contain the average values of three distinct replicates, together with their related standard error (SE). The bar graphs depict the average values of different treatments, with unique superscripts denoting statistically significant differences at a significance level of p ≤ 0.05, computed using Tukey’s test.

Under TMX stress, the activity of POD increased by 59.961%, 85.579%, and 80.221% in 30, 45, and 60 days of plants, compared to the control group. Notably, the enzyme activities of POD contents were found to be significantly enhanced by 57.870%, 28.373%, and 23.058% when seeds were exposed to a SA3 (1mM) concentration of SA and grew under TMX conditions (Fig. 3).

The CAT activities observed in the TMX-treated group exhibited a 34.409%, 42.169% and 27.193% increase compared to the untreated plants, which were harvested after 30, 45, and 60 days of growth period. The most significant rise of 89.265%, 75.876%, and 80.029% in the CAT activity was specifically detected when seeds were pre-soaked in the concentration of 1 mM of SA3, and introduced for growth in pesticide stress conditions in 30, 45, and 60 days of plants, in contrast with the only TMX-exposed plants (Fig. 3).

Furthermore, plants exposed to TMX showed a rise of 52.355%, 53.130%, and 48.483% in the enzymatic activity of APOX in 30-, 45-, and 60-day-old plants, compared to control plants. The APOX activities were significantly enhanced by 70.318%, 47.999%, and 49.536% by the addition of specified SA3 (1 mM) concentrations to plants subjected to TMX pesticide, and when compared to plants treated with TMX alone (Fig. 3).

3.5 Phenolic compounds

The contents of anthocyanin in plants infused with TMX had a substantial rise of 97.225%, 58.688% and 45.059% in 30-, 45-, and 60-day-old plants, respectively, compared to the untreated plants. Additionally, the application of SA3 (1mM) to TMX challenged plants resulted in an additional surge by 70.245%, 41.407% and 57.591% in 30-, 45-, and 60-day-old plants for anthocyanin contents and checked against the TMX-stressed plants only (Table 3).

Table 3. The impact of varying doses of SA (SA1 0.01 mM, SA2 0.1 mM, and SA3 1 mM) on the anthocyanin content of 30-, 45-, and 60-day-old B. juncea plants, under the TMX stress conditions. Significance level checked at P ≤ 0.05, designated with *.
Treatments
 Anthocyanin content (mg/gFW) Mean ± SD
TMX (mg/Kg) SA (mM/L) 30 Days 45 Days 60 Days
0 0 0.0254 ± 0.0003 0.0468 ± 0.0006 0.0558 ± 0.0014
0 0.01 0.0249 ± 0.0005 0.0486 ± 0.0011 0.0660 ± 0.0003
0 0.1 0.0378 ± 0.0016 0.0607 ± 0.0013 0.0729 ± 0.0007
0 1 0.0501 ± 0.0014 0.0744 ± 0.0012 0.0818 ± 0.0014
750 0 0.0471 ± 0.0020 0.0743 ± 0.0009 0.0810 ± 0.0001
750 0.01 0.0597 ± 0.0032 0.0818 ± 0.0023 0.0989 ± 0.0026
750 0.1 0.0602 ± 0.0001 0.0937 ± 0.0002 0.1116 ± 0.0010
750 1 0.0802 ± 0.0021 0.1051 ± 0.0026 0.1276 ± 0.0006
F-ratio 342.461* 545.358* 1008.017*

A significant augmentation in flavonoids of 139.343%, 46.107% and 34.011% was observed in 30, 45, and 60 days of plants subjected only to TMX, in contrast to the control set of plants. Furthermore, SA3 pre-treated seeds with a 1 mM dosage, and when exposed to the TMX-treated soils, the plants were found to have enhanced levels of 88.014%, 28.688%, and 62.800% for total flavonoid contents in 30-, 45-, and 60-day-old plants individually, when checked against the only TMX-treated ones (Fig. 4).

The impact of varying doses of salicylic acid (SA) (SA1 0.01mM, SA2 0.1mM and SA3 1mM) on the phenolic compounds, specifically flavonoid content and total phenols content, in 30, 45, and 60 days of B. juncea plants in the presence of TMX pesticide stress. The statistical information shown here includes the mean values of three separate replicates, in tandem with the corresponding standard error (SE). The bar graphs display the mean values of various treatments, with distinct superscripts indicating significant differences at a significance level of p ≤ 0.05, as determined by Tukey’s test
Fig. 4.
The impact of varying doses of salicylic acid (SA) (SA1 0.01mM, SA2 0.1mM and SA3 1mM) on the phenolic compounds, specifically flavonoid content and total phenols content, in 30, 45, and 60 days of B. juncea plants in the presence of TMX pesticide stress. The statistical information shown here includes the mean values of three separate replicates, in tandem with the corresponding standard error (SE). The bar graphs display the mean values of various treatments, with distinct superscripts indicating significant differences at a significance level of p ≤ 0.05, as determined by Tukey’s test

Total phenols get a noticeable enhancement with values of 23.346%, 42.311%, and 42.582% in TMX-stressed plants of 30, 45, and 60 days after growth, when compared to the untreated ones (CN). Furthermore, the seeds that received a treatment of 1mM of SA3 before being subjected to the TMX exposure exhibited a substantial increase of 86.480%, 48.997%, and 46.193% in the total phenol contents of 30-, 45-, and 60-day-old plants, respectively, when checked against the plants that only received the TMX treatment (Fig. 4).

4. Discussion

In the present study, owing to the stress caused by TMX in Brassica juncea L. plants, a decrease in the root and shoot length was assessed under the TMX stress conditions. However, an increment in root and shoot length was achieved in salicylic acid (SA) presoaked seeds when the plants were grown in TMX-treated soils. SA triggers the root length by upregulation of cell division and controls growth through cell proliferation and expansion activities (Li et al., 2022). These outcomes are controlled by SA by regulating the activity of the root apical meristem (RAM). Furthermore, the activities of cell division markers like CYCLIN B1;1 or CYCLIN genes are regulated by the SA concentrations (Bagautdinova et al., 2022). Subsequently, SA inhibits gibberellic acid (GA) signaling by facilitating the NPR1-mediated degradation of GA INSENSITIVE DWARF 1 (GID1), consequently affecting plant development (Yu et al., 2022; Salinas et al., 2025). Recent outcomes correlate with the findings of Bano et al. (2022) in Brassica napus under abiotic stress and Li et al. (2022) under the fomesafen toxicity in sugar beet.

However, studies also found that the total chlorophyll contents showed a reduction in TMX-stressed conditions. In studies conducted by Hatamleh et al. (2022), a consistent pattern of decline in the contents of total chlorophyll was observed in Solanum lycopersicum plants grown under the toxic environment of imidacloprid and mancozeb, respectively. The possible mechanism underlying the reduced total chlorophyll contents might be the damage in chloroplast structure, oxidation of chlorophyll via excessive ROS, upregulated chlorophyllase activity, and disruption of pigment biosynthetic enzymes under pesticide stress (Radwan et al., 2019; Hatamleh et al., 2022; Harpaz-Saad et al., 2007). Salicylic acid (SA) pretreatments help plants to upregulate the pigments biosynthetic processes under stress conditions (Radwan et al., 2019).

Carotenoid contents were found to be enhanced under the TMX stressed conditions, which, however, implies their potential to protect the photosynthetic processes. Carotenoids act like antioxidants in order to scavenge the singlet oxygen, and protect membranes from lipid peroxidation (Cupellini et al., 2020). Also, SA regulates the amounts of chlorophyll and carotenoid contents by employing RuBisCo (Ribulose-1,5-bisphosphate carboxylase/oxygenase) mediated carboxylase activity to modulate the photosynthesis rate (Hayat and Ahmad, 2007). These similar results were drawn from studies conducted by Khodary (2004) in Zea mays.

Xanthophyll content also showed a substantial increase in plants subjected to TMX stress, as well as when the SA pre-primed seeds were subjected to growth in TMX-stressed soils. These findings are in accordance with the reports of Sharma et al. (2016), which showed an enhanced amount of xanthophyll in B. juncea that were subjected to imidacloprid stress. The xanthophyll cycle participates in regulatory responses to protect the chloroplasts from photooxidative damage (Smirnoff and Wheeler, 2000). Also, changes in the expression of phytoene synthase (PSY) could be a possible reason for the increased levels of carotenoids and xanthophyll in plants grown under stress (Bakshi et al., 2023). Moreover, SA also has a strong effect on the structure of chloroplasts, which could be attributed to increased photosynthetic efficiency (Uzunova and Popova, 2000).

Various gaseous exchange parameters, including the net photosynthetic rate, stomatal conductance, transpiration rate, and concentration of intercellular CO2, were observed to be lowered in B. juncea plants that were grown under TMX stress. However, SA-supplemented plants grown under TMX-inoculated soils were found to have enhanced activities of all the gaseous exchange parameters. Similar observations were presented by Bakshi et al. (2023), where the gaseous exchange parameters decreased due to the application of chlorpyrifos and damage to the stomatal apparatus. On the other hand, abiotic stressors put pressure and interfere with the PSI and PSII photosystems and thus lower the mechanisms of gaseous exchange parameters (Garcia et al., 2019). Furthermore, the activities could be hampered by alterations in the Rubisco activity and in Calvin cycle enzymes (Pan et al., 2020). Current findings are consistent with Li et al. (2022), which showed a SA-mediated enhancement in the gaseous exchange parameters under the fomesafen stress by the upregulation of pigment synthesis, enhanced electron transfer rate, and protection of PSII from photodamage (Li et al., 2022). Also, the implementation of SA results in an augmentation in epidermal cell size, stomatal frequency, and stomatal pore size to maximize the photosynthetic efficiency of stressed plants (Orcen, 2017; Shekari et al., 2025).

Our investigations into TMX-stressed plants revealed an increase in reactive oxygen species (ROS) levels, which in turn resulted in the overexpression of antioxidative enzymes such as SOD, POD, CAT, and APOX. Notably, the addition of SA to TMX-treated B.juncea plants led to a significant increase in the expression of the enzymes mentioned earlier in turn reduces the oxidative damage. Among these enzymes, SOD is effectively able to convert the superoxide anions (O2-) into hydrogen peroxide (H₂O₂) and reactive molecular oxygen, while maintaining the membrane integrity (Wang et al., 2016). Hydrogen peroxide levels can be ascribed to the concerted activity of supplementary enzymes, such as CAT, POD, and APOX, which furthermore leads to the catalysis of H₂O₂ into water (H₂O) and some other non-toxic byproducts (Khatami et al., 2022; Kour et al., 2024). The increased CAT activity observed with SA supplementation indicates the important function of these antioxidants in converting H₂O₂ into oxygen (O₂) and water (H₂O) (Zhang et al., 2009). APOX, the initial enzyme of the ascorbate-glutathione (Halliwell-Asada) cycle, facilitates the reduction of H₂O₂ by utilizing ascorbate as an electron donor across many organelles (Sofo et al., 2015). The current study further corroborates the findings of Boulahia et al. (2023) in Phaseolus vulgaris L.

Subsequently, under the SA application, frequent upregulation in the principal enzymes of the shikimic acid pathway, phenylalanine ammonia lyase pathways was observed, which mediates the synthesis of secondary protective chemicals. Anthocyanins and flavonoids are widely recognized for their beneficial effects in mitigating abiotic stress situations and their antioxidant properties (Winkel-Shirley, 2001). Under the influence of TMX stress, B. juncea plants displayed a rise in anthocyanin and flavonoid contents. Under conditions of TMX stress, it is possible that the expression of chalcone synthase (CHS), a gene involved in anthocyanin production, may be elevated at higher levels. Furthermore, the use of SA may be a potential explanation for the increased levels of CHS expression in response to TMX-induced stress. Additionally, flavonoids are essential secondary metabolites that regulate enzymes associated with the production of ROS and protect cellular membranes against oxidative stress (Ahmad and Prasad, 2012; Keya et al., 2023). Our study showed a steady rise in the levels of total phenols in plants that were subjected to TMX stress. Additionally, plants that were soaked in SA before being exposed to TMX also exhibited an increase in total phenols. The potential reasons for the upregulated amounts of these phenols were due to the activation of the phenyl-propanoid pathway (Ahammed et al., 2013). These phenolic metabolites exhibit functions like defense, antioxidative potentials, and anti-inflammatory activities. Whereas they contribute to the structural stability and integrity by developing ester linkages with polysaccharides, leading to oxidative stress amelioration (Kumar et al., 2024). The studies corroborate the findings of Bakshi et al. (2023) in Brassica juncea crops.

5. Conclusions

The current findings summarize the ameliorative effects of Salicylic acid (SA) in Brassica juncea L. under the TMX stressed conditions. The data indicate the toxicity effects of TMX pesticide and disturbances on the growth parameters, photosynthetic pigments, gaseous exchange parameters, enzymatic potentials, and secondary metabolite contents. Consequently, the TMX leads to deteriorating impacts on the overall morpho-physiological and biochemical aspects of plants and subsequent losses in yield. On the contrary, SA interactions within plants have successfully alleviated the hazardous impacts of these pesticides by upregulating the activities of enzymatic antioxidants and other defense-related compounds. These findings are of advantage to tackle pesticide-mediated toxicity in crop plants and to minimize the losses in yield. Consequently, the use of salicylic acid, especially seed priming with SA, is proposed as a viable strategy to safeguard plants from cellular damage induced by TMX-related oxidative stress by enhancing antioxidant capacity and physiological performance.

Acknowledgement

The authors would like to extend their sincere appreciation to the Ongoing Research Funding Program (ORF-2025-236), King Saud University, Riyadh, Saudi Arabia

CRediT authorship contribution statement

Arun Dev Singh: Conceived, designed, and supervised the study, and defined the intellectual content. Jaspreet Kour, Shalini Dhiman, and Nitika Kapoor: Performed data analysis, statistical analysis, and prepared the manuscript draft. Akram Mohammad and Abdulaziz Abdullah Alsahli: Contributed to data acquisition, statistical analysis, and manuscript preparation. Parvaiz Ahmad and Renu Bhardwaj: Edited and reviewed the manuscript. All authors read and approved the final manuscript.

Declaration of competing interest

The authors declare that they have no competing financial interests or personal relationships that could have influenced the work presented in this paper.

Declaration of Generative AI and AI-assisted technologies in the writing process

The authors confirm that there was no use of Artificial Intelligence (AI)-Assisted Technology for assisting in the writing or editing of the manuscript and no images were manipulated using AI.

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