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Responses to exogenous elicitor treatment in lead-stressed Oryza sativa L.

BMC Plant Biology volume 24, Article number: 897 (2024) Cite this article

Abstract

Heavy metal toxicity adversely affects plants by changing physiological, biochemical, and molecular mechanisms. Lead (Pb) is one of the most common heavy metal pollutants. Hence this study investigated changes caused by exogenous methyl jasmonate (MeJA; 20 and 100 µM) and salicylic acid (SA; 2 and 20 mM) elicitors in local Karacadağ rice exposed to Pb stress (0, 100, and 400 ppm). The effects of elicitors on photosynthetic pigment content (chlorophyll a, chlorophyll b, and total carotenoid), proline, malondialdehyde (MDA), total phenolic and flavonoid, Pb, and total protein contents in stressed plants were evaluated. All parameters studied increased and decreased at varying rates in the treatment groups compared to the Pb-free group (control), indicating that rice plants were affected by Pb stress. The elicitors (MeJA, SA, and MeJA + SA) were applied by foliar spraying. The elicitor treatments increased photosynthetic pigment content, total protein, proline, total flavonoid, and phenolic contents depending on the elicitor type and concentration. MDA and Pb contents, increasing with Pb toxicity, decreased with elicitor treatments, and the stress degree was reduced. When the elicitors were compared, SA was more effective than MeJA in total flavonoid content at 400 ppm Pb toxicity. However, MeJA was more effective in photosynthetic pigment contents, MDA, total protein, Pb, total phenolic, and proline contents. The best results for all parameters examined in rice plants exposed to Pb toxicity were obtained from the 400 ppm Pb + 2 mM SA + 20 µM MeJA treatment group. In conclusion, this study showed that the combined application of MeJA + SA alleviated the harmful effects of Pb by reducing MDA and increasing photosynthetic pigments, total protein, proline, and secondary metabolites, especially at high Pb concentrations. Consequently, this study demonstrated that the combined use of MeJA and SA in rice plants eliminated the negative effects of stress quite effectively, even at high Pb concentrations. Therefore, future studies should focus on the synergistic application of different elicitors to better understand the effects of heavy metal toxicity on plant growth and development.

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Introduction

Plants, which have developed a series of mechanisms to ensure their survival [1] and successful reproductive cycles, may not always be in the best environmental conditions, which can lead to “stress” in the plant [2]. Stress caused by abiotic factors (temperature, salt, heavy metals, etc.) is the main cause of crop failure globally. Toxicity caused by heavy metals is one of the most important abiotic stress factors [3].

Heavy metal contamination is caused by various processes in agriculture, including fertilization and spraying, vehicle exhaust fumes, mining operations, and volcanic and industrial activities [4, 5]. Studies have reported that heavy metals also threaten the long-term sustainability of the agricultural sector [6, 7]. Many naturally occurring processes, including mineral and nutrient uptake, enzyme activity, photosynthesis, and germination, are adversely affected by the accumulation of heavy metals in plant tissues and cells [8]. Although heavy metals are considered environmental pollutants due to their toxic effects on humans, animals, and plants, they are persistent in nature as they accumulate in plants and soil [9]. Since lead (Pb) is not biodegradable, it can be transferred to plants and humans through soil, air, and water, making it one of the most dangerous heavy metal pollutants [10]. Pb is a metal that can reduce plant growth, chlorophyll content, and, therefore, photosynthesis, i.e. it interferes with the rate of carbon dioxide assimilation and causes oxidative stress and DNA damage in plants [11].

The defense mechanism of plants increases the production of signaling molecules or elicitors (jasmonates, salicylic, ethylene, etc.) to counteract the negative effects of internal and external stress factors [12, 13]. This increase in elicitors affects the biosynthesis of secondary metabolites (phenolics, flavonoids, steroids, etc.) in plants, including phenolic acids, and the biosynthesis of these compounds often occurs at higher levels. Therefore, it can be concluded that elicitor treatments can affect the levels of plant metabolites and change physiological and biochemical capacity [14].

Salicylic acid (SA) has been identified as a signaling molecule that regulates various aspects of growth, such as plant development and aging, stomatal opening and closing, cell growth, respiration, seed germination, seedling development, and pathogen tolerance [15]. Methyl jasmonate (MeJA), a volatile methyl ester of jasmonic acid (JA), defined as "an important signaling molecule in abiotic and biotic stress," is involved in various processes in plants, from molecular to morphological functions [16, 17]. Some exogenous substances, such as salicylic acid, jasmonates, and selenium, have been reported to significantly alleviate Pb stress in plants [18]. In another study, salicylic acid pretreatment of bean seeds exposed to cadmium stress increased the chlorophyll and carotenoid contents while reducing the H2O2 and MDA contents and oxidative damage [19]. For all these reasons, research on lead-induced toxicity, causes of toxicity, physiological and molecular responses to toxicity, and the emergence of tolerance mechanisms still maintains its importance and continues widely.

Rice (Oryza sativa L.) is the main food source for approximately half of the world's population and plays an important role in the food security of many countries [20]. Since rice is a plant with a high water demand, it is particularly exposed to water-related metal stress. Therefore, heavy metal stresses, such as Pb and cadmium (Cd), considerably limit rice productivity. The literature review found no study on the effects of elicitor treatments on lead toxicity in rice plants.

The present study, which aims to fill this gap and contribute to the literature, investigated changes caused by Pb toxicity in the local Karacadağ rice plant and the effects of elicitor (SA and MeJA) treatments on this toxicity. To this end, two elicitors (SA and MeJA) were applied to Karacadağ rice at different concentrations separately and in combination following Pb toxicity. The data on the photosynthetic pigment, total protein, proline, Pb, MDA, total phenolic, and flavonoid contents of the plants treated with the elicitors to eliminate the damage caused by the Pb stress factor were comparatively evaluated.

Material and methods

Material

The seeds of local Karacadağ rice (Hazro population) used as a starting material in this study were obtained from local producers in Türkiye. After soaking in 5% sodium hypochlorite (NaOCl) for three minutes, seeds of local Karacadağ rice of similar plumpness and size were rinsed with sterile distilled water to remove NaOCl.

Surface-sterilized seeds were kept in distilled water for approximately 24 h for absorption.

After sterilization and imbibition, seeds were planted in pots containing peat, perlite, and soil (3:3:1) as 20 seeds per pot and allowed to grow in the growth chamber [mercury fluorescent lamps (400 w, MBFR/U, Thorn) with light intensity of 30–60 μm m-2 s-1 and temperature control system of 25 ± 2ºC and 16 h light and 8 h dark photoperiod of 3000–5000 lumens]. They were watered with ¼ Hoagland’s [21] nutrient solution twice a week during the 4-week growth period. After the 4-week growth period, seedlings were watered with lead nitrate [Pb (NO2) 3] at varying concentrations (0, 100, and 400 ppm) for 14 days according to the field water capacity (65%) to generate Pb stress. Plants irrigated simultaneously and at the same rate with ¼ Hoagland’s nutrient solution without Pb were determined as the "control" group.

Afterward, plants were divided into groups, as shown in Table 1. Elicitors were applied with ¼ Hoagland’s nutrient solution supplemented with SA (2 and 20 mM), MeJA (20 and 100 µM), and two stimulants together (20 µM MeJA + 2 mM SA) by foliar spraying (approximately 10 mL) twice a week for 14 days. All groups were continued to be irrigated with ¼ Hoagland’s nutrient solution simultaneously and at the same rate according to the field water capacity (65%) (Fig. 1 a and b). The plants harvested after 14 days were prepared for analysis. A portion of the plants harvested after 14 days were powdered in liquid nitrogen and stored at -80ºC. The remaining portion was left to dry in the shade at room temperature to be ready for analysis.

Table 1 Elicitor and lead stress applications
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Fig. 1
figure 1

a 14-day development of rice plants in 400 ppm Pb b 14-day development of rice plants in 400 ppm Pb + 2 mM SA + 20 µM MeJA

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Methods

In this study, separate and combined elicitor treatments (MeJA and SA) were applied to Karacadağ rice plants exposed to different concentrations (0, 100, and 400 ppm) of the Pb stress factor to determine whether the negative effects of stress were eliminated. The plants’ photosynthetic pigment contents, the degree of lipid peroxidation, proline, total protein, total phenolic and flavonoid, and Pb contents were evaluated comparatively after the treatments.

Chlorophyll a, chlorophyll b, and total carotenoid contents were measured following Arnon [22]. Fresh leaf samples of Karacadağ rice plants were homogenized in a mortar and pestle with 80% acetone; the homogenate was filtered through filter paper and then added 80% acetone to make up to 5 mL. The extracts were centrifuged at 5000 rpm, and the absorbance was measured spectrophotometrically at 663 nm for chlorophyll a, 645 nm for chlorophyll b, and 480 nm for total carotenoid.

MDA, the end product of lipid peroxidation, was measured using the thiobarbituric acid (TBA) assay to assess damage to cell membranes [23]. A 100 mg sample was homogenized with 5% trichloroacetic acid (TCA), and the mixture was centrifuged at 12,000 rpm and 25 °C. The supernatant and the reaction mixture containing 20% TCA solution with 0.5% thiobarbituric acid (TBA) were kept in a hot water bath at 95 °C for 1 h, then placed in an ice bath to stop the reaction and centrifuged. The absorbance values were read with a UV–VIS spectrophotometer (UV 1601 Shimadzu, Japan) at a wavelength of 532 nm against the blank.

Proline content was determined spectrophotometrically by the acid ninhydrin method [24]. Fresh leaf samples were homogenized in 40% methanol and centrifuged at 1000 rpm and 4 °C for 10 min. 1 mL of the obtained supernatant was taken, and 1 mL of glacial acetic acid and 6 M orthophosphoric acid mixture (3:2 v/v) was added. 25 mg of ninhydrin was added to the prepared reaction medium, and the mixture was heated for 1 h at 95 °C in a water bath and allowed to cool at room temperature. Then, 5 mL of toluene was added to the mixture, and it was left for 5 min to ensure separation of the organic and water phases. To determine the amount of proline, the absorbance of the upper phase was measured spectrophotometrically at a wavelength of 520 nm, and the amount of proline was calculated using a standard curve prepared with known concentrations of the amino acid.

Plant samples that were left to dry during harvest to be used in antioxidant activity assays were turned into powder and macerated with ethanol for 24 h. After maceration, the solvent part of the extracts filtered through Whatman No:1 filter papers was removed with the help of an evaporator, and the remaining extract was made ready to be used in activity determinations. Stock solutions were prepared at a concentration of 1000 μg/mL from the obtained solid extracts to determine total phenolic and flavonoid contents.

The total phenolic content was determined as equivalent to gallic acid using the Folin-Ciocalteu reagent [25]. The extracts were prepared at a concentration of 1000 ppm. Sample solutions containing 100 ppm extracts were made up to 4.6 mL with distilled water. Then, 2% Na2CO3 solution and the Folin-Ciocalteu reagent (FCR) were added to this mixture and allowed to incubate at room temperature. Spectrophotometric measurements were taken at a wavelength of 760 nm.

The total flavonoid content was determined by the aluminum nitrate method equivalent to quercetin [26]. A 1000 ppm quercetin solution was prepared, and 0, 25, 50, 75, 100, 125, 150, 175, 175, and 200 μL of this solution were taken and made up to 4.8 mL with 80% ethanol. Then, 1 M potassium acetate and 10% aluminum nitrate were added to the mixture. After the incubation period, the absorbance was read at 415 nm in a UV–VIS (UV 1601 Shimadzu, Japan) spectrophotometer against the control.

The total protein content of the green parts of rice was measured following the method described by Lowry et al. [27]. After homogenizing 0.5 g of fresh material in 0.1 M phosphorous buffer (pH 7), the mixture was centrifuged at 12,000 rpm and 4 °C. The alkaline solution was added to the supernatant and kept in the dark at room temperature. Then, the Folin-Ciocalteu reagent was added and kept at room temperature for 30 min, and absorbance was read at 750 nm.

To ascertain the lead (Pb) concentrations, the dried and crushed leaf samples were mixed with concentrated HNO3 and stored at room temperature. Afterward, they were gradually heated on the heating plate, which could be adjusted until the colored vapors vanished. An inductively coupled plasma optical emission spectrometer (ICP OES; PerkinElmer, Optima 7000 DV, USA) was used to measure the amounts of lead in the diluted samples with HCl after all samples evaporated and the bottom sediment dried [28].

Statistical analysis

Three random design replications of the analysis were carried out. One-way analysis of variance (ANOVA) and Duncan's multiple range test were used to analyze the data. Test findings were generated using SPSS 21.0, a statistical analysis program. A p-value of 0.05 was used for statistical significance.

Results

Evaluation of photosynthetic pigment content

To determine changes in photosynthetic pigment content caused by Pb stress, chlorophyll a, chlorophyll b, and total carotenoid contents were investigated in local Karacadağ rice (O. sativa L.). Chlorophyll a content increased statistically significantly with 100 and 400 ppm Pb treatments compared to the control group. This increase in response to Pb toxicity indicates that the plant was affected by stress in terms of chlorophyll a content. In plants exposed to 100 ppm Pb toxicity, adding 2 mM SA elicitor resulted in the highest increase in chlorophyll a content (H4; 1.45 mg/g FW). Increasing the amount of the SA elicitor (H5; 1.01 mg/g FW) reduced chlorophyll a content statistically significantly. The use of the MeJA elicitor resulted in reduced chlorophyll a content compared to 100 ppm Pb toxicity. At 400 ppm Pb toxicity, elicitor treatment resulted in a gradual increase in chlorophyll a content. The highest increase in chlorophyll a content (1.53 mg/g FW) was observed in the experimental group treated with 400 ppm Pb + 2 mM SA + 20 µM MeJA (H13) (Fig. 2).

Fig. 2
figure 2

Effect of Pb stress and elicitor applications on photosynthetic pigment contents (mg/g FW) (Results are expressed as means ± standard deviation (n = 3). Different letters indicate significance differences (p < 0.05) among rice samples according to Duncan’s multiple range test) [H1-Control; H2-100 ppm Pb (NO3)2; H3- 400 ppm Pb (NO3)2; H4-100 ppm Pb (NO3)2 + 2 mM SA; H5- 100 ppm Pb (NO3)2 + 20 mM SA; H6- 100 ppm Pb (NO3)2 + 20 µM MeJA; H7-100 ppm Pb (NO3)2 + 100 µM MeJA; H8- 400 ppm Pb (NO3)2 + 2 mM SA; H9-400 ppm Pb (NO3)2 + 20 mM SA; H10- 400 ppm Pb (NO3)2 + 20 µM MeJA; H11-400 ppm Pb (NO3)2 + 100 µM MeJA; H12-100 ppm Pb (NO3)2 + 2 mM SA + 20 µM MeJA; H13-400 ppm Pb (NO3)2 + 2 mM SA + 20 µM MeJA]

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Chlorophyll b content was lower at both 100 (0.49 mg/g FW) and 400 ppm (0.45 mg/g FW) Pb concentrations compared to the control group (0.51 mg/g FW) (Fig. 2). While chlorophyll b content decreased in all groups with elicitor addition at 100 ppm Pb toxicity, depending on the elicitor type and concentration, chlorophyll b content increased in the group treated with 2 mM SA (H4; 1.05 mg/g FW). These changes in chlorophyll b content were statistically significant. Chlorophyll b content differed at 400 ppm Pb toxicity depending on the type and concentration of the elicitor used. Chlorophyll b content, which was 0.36 mg/g FW (H8) at 2 mM SA concentration, was measured as 0.56 mg/g FW (H9) in the 20 mM SA application. Chlorophyll b content, which was 0.45 mg/g FW at 400 ppm Pb concentration, increased with MeJA elicitor treatment and reached 0.97 mg/g FW (H11). However, the highest increase in chlorophyll b content (2.73 mg/g FW) in response to Pb toxicity was in the 2 mM SA + 20 µM MeJA treatment group.

Concerning total carotenoid content, when Pb toxicity was compared with the control (H1; 3.76 mg/g FW), the content that was statistically insignificant at 100 ppm decreased significantly with a value of 3.06 mg/g FW at 400 ppm Pb concentration. At 100 ppm Pb toxicity, total carotenoid content decreased with the increased concentration of MeJA or SA elicitors. The highest carotenoid content (4.31 mg/g FW) was obtained from the group treated with 2 mM SA (H4). At 400 ppm Pb toxicity, the addition of the elicitor caused a regular increase in total carotenoid content, which was statistically significant (Fig. 2). In addition, when the applied elicitors were compared, MeJA treatments increased the carotenoid content more than SA. Among all groups, the highest increase in total carotenoid content (5.52 mg/g FW) was observed when two elicitors (H13; 2 mM SA + 20 µM MeJA) were used in combination, similar to chlorophyll a and chlorophyll b levels, and the best result was obtained.

Evaluation of malondialdehyde (MDA) amount

MDA, one of the main products of biotic and abiotic stresses in plants and one of the end products of lipid peroxidation, was analyzed to investigate the effects on membranes of local Karacadağ rice, which are the primary target of stress (Fig. 3). MDA level increased twofold to 2.07 µmol/g FW at 100 ppm Pb application compared to the control group (H1; 1.22 µmol/g FW) and increased threefold to 3.70 µmol/g FW at 400 ppm Pb concentration. This increase in MDA content, even at 100 ppm Pb concentration, indicates that rice plants are affected by Pb toxicity even at low concentrations. In plants exposed to 100 ppm Pb (2.07 µmol/g FW) toxicity, low SA (H3; 1.59 µmol/g FW) and MeJA (H5; 1.95 µmol/g FW) applications decreased MDA content, while the increased elicitor concentration increased MDA content. MDA content, which was 3.70 µmol/g FW at 400 ppm Pb toxicity, decreased with elicitor application. This decrease, which was statistically significant, decreased to 1.10 µmol/g FW with the addition of 100 μM MeJA (Fig. 3). The highest decrease in MDA content (0.53 µmol/g FW) was in the experimental group treated with 2 mM SA + 20 µM MeJA (H13). This may result from the interaction between SA and MeJA stimulators, which reduce the MDA content, an indicator of cell membrane damage, and consequently, elicit Pb stress resistance.

Fig. 3
figure 3

Effect of Pb stress and elicitor applications on MDA content (µmol/g FW) (Results are expressed as means ± standard deviation (n = 3). Different letters indicate significance differences (p < 0.05) among rice samples according to Duncan’s multiple range test) [H1-Control; H2-100 ppm Pb (NO3)2; H3- 400 ppm Pb (NO3)2; H4-100 ppm Pb (NO3)2 + 2 mM SA; H5- 100 ppm Pb (NO3)2 + 20 mM SA; H6- 100 ppm Pb (NO3)2 + 20 µM MeJA; H7-100 ppm Pb (NO3)2 + 100 µM MeJA; H8- 400 ppm Pb (NO3)2 + 2 mM SA; H9-400 ppm Pb (NO3)2 + 20 mM SA; H10- 400 ppm Pb (NO3)2 + 20 µM MeJA; H11-400 ppm Pb (NO3)2 + 100 µM MeJA; H12-100 ppm Pb (NO3)2 + 2 mM SA + 20 µM MeJA; H13-400 ppm Pb (NO3)2 + 2 mM SA + 20 µM MeJA]

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Evaluation of total phenolic and flavonoid substance content

Plants contain chemicals called phenols and flavonoids, which are among the secondary metabolites that occur, especially in stressful environments. In addition to serving as natural defense mechanisms against harmful organisms, these substances also occur under abiotic stress conditions. Figure 4 shows changes in total phenolic and flavonoid contents with the stimulants (SA and MeJA) used to counteract Pb heavy metal toxicity in Karacadağ rice.

Fig. 4
figure 4

Effect of Pb stress and elicitor applications on total flavonoid (μg QEs/mg ekstre) and phenolic (μg GAEs/mg ekstre) contents (µmol/g FW) (Results are expressed as means ± standard deviation (n = 3). Different letters indicate significance differences (p < 0.05) among rice samples according to Duncan’s multiple range test) [H1-Control; H2-100 ppm Pb (NO3)2; H3- 400 ppm Pb (NO3)2; H4-100 ppm Pb (NO3)2 + 2 mM SA; H5- 100 ppm Pb (NO3)2 + 20 mM SA; H6- 100 ppm Pb (NO3)2 + 20 µM MeJA; H7-100 ppm Pb (NO3)2 + 100 µM MeJA; H8- 400 ppm Pb (NO3)2 + 2 mM SA; H9-400 ppm Pb (NO3)2 + 20 mM SA; H10- 400 ppm Pb (NO3)2 + 20 µM MeJA; H11-400 ppm Pb (NO3)2 + 100 µM MeJA; H12-100 ppm Pb (NO3)2 + 2 mM SA + 20 µM MeJA; H13-400 ppm Pb (NO3)2 + 2 mM SA + 20 µM MeJA]

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Compared to the control (H1) group, total phenolic content in the leaves of rice plants exposed to lead stress decreased statistically significantly at both Pb concentrations (100 ppm and 400 ppm). Elicitor treatments at 100 ppm Pb toxicity caused an overall increase in the total phenolic content, except for 20 mM SA (H5). In this toxicity, the highest increase in total phenolic content (67.97 μg GAEs/mg) due to elicitor treatment was obtained in the group with 20 μM MeJA (H6) added. Total phenolic content decreased with the increased concentration for both SA and MeJA elicitors. At 400 ppm Pb toxicity, there was an overall increase in total phenolic content with the addition of the stimulants. With the increased concentration of the elicitors, a regular and significant increase in the phenolic content occurred. The highest increase (92.24 μg GAEs/mg) was determined in the experimental group treated with 2 mM SA + 20 μM MeJA (H13) (Fig. 4). As a result, it can be said that stimulants added to rice plants at 400 ppm heavy Pb toxicity have an ameliorative effect by increasing the total phenolic content.

Compared to the control group (H1; 226.56 μg QEs/mg extract), total flavonoid content increased at 100 and 400 ppm Pb concentrations, with a greater increase at a higher Pb concentration (H3; 391.36 μg QEs/mg extract) (Fig. 4). There were significant changes depending on the elicitor concentration at 100 ppm Pb concentration. For both SA and MeJA elicitors, total flavonoid content decreased significantly with the increased concentration. The highest decrease (299.14 μg QEs/mg extract) was obtained in the group (H7), to which 100 μM MeJA was added. Likewise, at 400 ppm Pb toxicity, total flavonoid content decreased significantly with the increased elicitor concentration. The highest decrease (229.34 μg QEs/mg extract) was obtained in the group (H9) with 20 mM SA added. While total flavonoid content decreased depending on the increase in concentration when the elicitors were applied separately, the highest increase was in the group (H13) treated with 400 ppm Pb + 2 mM SA + 20 mM MeJA, where the two elicitors were administered in combination, with 553.03 μg QEs/mg extract value (Fig. 4).

Evaluation of proline content

In plants, proline is an important osmoregulator contributing to the integrity of proteins and the activation of enzymes, especially in stressed plants. When the proline content in the leaves of rice plants exposed to lead stress was compared to the control group (H1), it was found to decrease at both Pb concentrations (100 ppm and 400 ppm). Thus, proline content was affected by Pb toxicity in this sense (Fig. 5).

Fig. 5
figure 5

Effect of Pb stress and elicitor applications on proline (mmol/g FW) contents (Results are expressed as means ± standard deviation (n = 3). Different letters indicate significance differences (p < 0.05) among rice samples according to Duncan’s multiple range test) [H1-Control; H2-100 ppm Pb (NO3)2; H3- 400 ppm Pb (NO3)2; H4-100 ppm Pb (NO3)2 + 2 mM SA; H5- 100 ppm Pb (NO3)2 + 20 mM SA; H6- 100 ppm Pb (NO3)2 + 20 µM MeJA; H7-100 ppm Pb (NO3)2 + 100 µM MeJA; H8- 400 ppm Pb (NO3)2 + 2 mM SA; H9-400 ppm Pb (NO3)2 + 20 mM SA; H10- 400 ppm Pb (NO3)2 + 20 µM MeJA; H11-400 ppm Pb (NO3)2 + 100 µM MeJA; H12-100 ppm Pb (NO3)2 + 2 mM SA + 20 µM MeJA; H13-400 ppm Pb (NO3)2 + 2 mM SA + 20 µM MeJA]

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Proline content decreased with the increased concentration for both SA and MeJA elicitors at 100 ppm Pb toxicity, and this decrease was statistically significant. The experimental group treated with 20 µM MeJA (H6; 3.57 mmol/g FW) showed the highest increase in proline content with the addition of the stimulant at 100 ppm Pb toxicity, while the group treated with 100 µM MeJA (H7; 1.61 mmol/g FW) showed the lowest content. However, the proline content in the 100 ppm Pb + 2 mM SA + 20 μM MeJA (H12) treatment group, where the two elicitors were applied in combination, was lower than the separate applications (1.00 mmol/g FW). At 400 ppm Pb toxicity, elicitor treatments increased proline content in response to Pb stress. SA treatments increased proline content with the increasing concentration, whereas MeJA treatments decreased proline content significantly with the increased concentration. The 2 mM SA + 20 mM MeJA (H13) treatment group, where the two elicitors were used in combination, had the highest proline content with 5.59 mmol/g FW (Fig. 5). The results showed that the 400 ppm Pb + 2 mM SA + 20 mM MeJA treatment had the greatest effect on proline content to alleviate Pb stress.

Changes in total protein amount

The total protein content in the leaves of rice plants exposed to lead stress was affected by stress by decreasing up to 81.22% (400 ppm Pb) compared to the control group (Fig. 6).

Fig. 6
figure 6

Effect of Pb stress and elicitor applications on total protein (mmol/g FW) contents (Results are expressed as means ± standard deviation (n = 3). Different letters indicate significance differences (p < 0.05) among rice samples according to Duncan’s multiple range test) [H1-Control; H2-100 ppm Pb (NO3)2; H3- 400 ppm Pb (NO3)2; H4-100 ppm Pb (NO3)2 + 2 mM SA; H5- 100 ppm Pb (NO3)2 + 20 mM SA; H6- 100 ppm Pb (NO3)2 + 20 µM MeJA; H7-100 ppm Pb (NO3)2 + 100 µM MeJA; H8- 400 ppm Pb (NO3)2 + 2 mM SA; H9-400 ppm Pb (NO3)2 + 20 mM SA; H10- 400 ppm Pb (NO3)2 + 20 µM MeJA; H11-400 ppm Pb (NO3)2 + 100 µM MeJA; H12-100 ppm Pb (NO3)2 + 2 mM SA + 20 µM MeJA; H13-400 ppm Pb (NO3)2 + 2 mM SA + 20 µM MeJA]

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At 100 ppm Pb (H2; 1.08 mmol/g FW) toxicity, the addition of the elicitors both separately and in combination increased the total protein content statistically significantly. The highest increase compared to 100 ppm Pb treatment occurred in the group treated with 20 µM MeJA (H6) with a protein value of 4.96 mmol/g FW. This value was higher in terms of total protein content than the treatment group, where both elicitors were used in combination (H13).

At 400 ppm Pb toxicity, the addition of the elicitors increased the total protein content statistically significantly. The total protein content increased with the increased concentration for both SA and MeJA elicitors. In this sense, MeJA was more effective than SA with its higher protein content. The 400 ppm Pb + 2 mM SA + 20 µM MeJA (H13) treatment group, where the two elicitors were applied in combination, had the highest total protein content with a protein value of 8.32 mmol/g FW (Fig. 6).

Evaluation of Pb content

With the increased Pb concentration in Karacadağ rice plants exposed to the Pb stress factor, Pb content, which was 0 in the control group, increased to 5.08 mg/kg (H3). Different rates of increase and decrease were observed in Pb content depending on the type and concentration of the stimulant applied at 100 ppm Pb toxicity. Pb content increased at high MeJA and SA concentrations while decreasing at low concentrations. Among all elicitors added at 100 ppm Pb toxicity, the 2 mM SA treatment group had the lowest Pb content with a value of 2.44 mg/kg.

The addition of the stimulants at 400 ppm Pb toxicity caused statistically significant decreases in lead content. When the stimulants were applied separately, Pb content decreased with the increased concentration, and MeJA (H10-2.89 mg/kg; H11-2.431 mg/kg) was more effective than SA (H8-4.11 mg/kg; H9-3.97 mg/kg) in terms of these decreases. Among all treatment groups, the group with a high Pb concentration and stimulants applied together (H13) had the lowest Pb content with 2.09 mg/kg (Fig. 7).

Fig. 7
figure 7

Effect of Pb stress and elicitor applications on Pb (mg/kg) contents (Results are expressed as means ± standard deviation (n = 3). Different letters indicate significance differences (p < 0.05) among rice samples according to Duncan’s multiple range test) [H1-Control; H2-100 ppm Pb (NO3)2; H3- 400 ppm Pb (NO3)2; H4-100 ppm Pb (NO3)2 + 2 mM SA; H5- 100 ppm Pb (NO3)2 + 20 mM SA; H6- 100 ppm Pb (NO3)2 + 20 µM MeJA; H7-100 ppm Pb (NO3)2 + 100 µM MeJA; H8- 400 ppm Pb (NO3)2 + 2 mM SA; H9-400 ppm Pb (NO3)2 + 20 mM SA; H10- 400 ppm Pb (NO3)2 + 20 µM MeJA; H11-400 ppm Pb (NO3)2 + 100 µM MeJA; H12-100 ppm Pb (NO3)2 + 2 mM SA + 20 µM MeJA; H13-400 ppm Pb (NO3)2 + 2 mM SA + 20 µM MeJA]

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Discussion

The overabundance of heavy metals in the soil seriously threatens all living things, including plants. Various metals and metalloids, including arsenic, lead, cadmium, and mercury, are extremely hazardous to plants [29]. After arsenic, lead is regarded as the second hazardous heavy metal. Lead toxicity affects plant growth by interfering with transpiration, cell division, root elongation, seedling development, and chlorophyll production. These effects vary depending on plant species, Pb concentration, exposure time, and plant developmental stage [10]. Studies have reported that plant hormones such as ABA, IAA, SA, and JA, which are used to overcome the negative effects of stress in plants exposed to heavy metal stress, play an essential role in ameliorating heavy metal toxicity [30].

It is considered that the threshold for lead toxicity is 150–300 mg/kg in agricultural soils and 2 mg/kg in plants. Exceeding these levels reduces seed germination, increases chlorophyll degradation, decreases photosynthetic rate, and damages membranes [31]. The heavy metal concentrations used in the present study were chosen considering the threshold value of Pb toxicity in plants in mind. The amount used is below the threshold value for 100 ppm Pb concentration and above the threshold value at 400 ppm. As for the concentrations chosen for the combined application of SA + MeJA, since no comparable study was found, a low concentration of each was selected to prevent toxic effects.

For all these reasons, the present study investigated the effects of elicitor (SA and MeJA) treatments on the photosynthetic pigment contents (chlorophyll a and b and total carotenoid), total phenolic and flavonoid contents, MDA, Pb, proline, and total protein contents of rice (Oryza sativa L.) seedlings exposed to different concentrations (0, 100, and 400 ppm) of Pb.

Plant growth and development are based on photosynthesis, and the amount of pigments used in photosynthesis directly influences the rate of photosynthesis [32]. Decreased photosynthetic pigment levels have a detrimental effect on photosynthesis, one of the physiological processes most vulnerable to Pb [33]. Shu et al. [34] reported that elevated lead concentrations decreased the amounts of carotenoid and chlorophyll in Jatropha curcas L. Another study on the effects of lead on sunflowers found that chlorophyll content decreased significantly [35]. A study on the chili pepper plant showed that carotenoid content gradually decreased with increasing Cd concentration, which was linked to Cd disrupting photosynthetic pigment synthesis and affecting the function of chloroplasts [36]. Similar to studies conducted with other plant species [37,38,39], in this study, chlorophyll b and total carotenoid contents decreased in response to Pb stress, which can be associated with the effect on the function of chloroplasts, as stated by the researchers. Studies on the effects of elicitor treatments in response to heavy metal stress reported that crop failure occurred under Pb metal stress in wheat [40] and rice [41]. MeJA and Se treatments were reported to increase carotenoid content. Furthermore, Se use in Oryza sativa [33, 42] and the synergistic use of silicon (Si) and MeJA in Solanum lycopersicum [43] were stated to reduce Cd heavy metal accumulation. MeJA was also shown to improve photosynthetic traits in response to heavy metals in Triticum aestivum [44], Mentha arvensis [45], and kenaf [46]. In our present study, similarly, the application of MeJA and SA to plants under Pb stress increased photosynthetic pigments, as stated by the researchers, leading to the conclusion that photosynthesis may have been improved. However, similar to the results of studies on wheat and rice where the combined elicitor application (MeJA + Se) [40, 41] was more effective than separate elicitor applications, in the present study, the reduced effect of the combined application (MeJA + SA) on Pb accumulation in Karacadağ rice plants was more effective than a separate application.

MDA level increases under stress conditions due to peroxidation of unsaturated fatty acids in phospholipids, and increased MDA level also increases the amount of reactive oxygen species (ROS). Therefore, studies have used MDA, which is used to assess plant stress levels, as a significant parameter [29, 32]. In two distinct cluster bean types subjected to varying Pb doses, MDA content increased in the study by Sharma et al. [47]. However, MeJA treatment decreased the harmful effects of Pb by lowering MDA content. The same study concluded that exogenously administered MeJA enhanced tolerance to Pb stress by shielding the biological membrane and reducing lipid peroxidation. In the present study, the MDA level in rice plants increased significantly in response to the Pb stress factor, indicating that the plant was significantly affected by Pb stress. The use of SA and MeJA significantly reduced MDA content, a measure of membrane damage, compared to Pb-treated groups, indicating that the elicitors used protect the cell membrane, as stated by the researchers. Likewise, studies on rice [48] and bean [49] plants under copper, cadmium, and arsenic stress found that exogenous MeJA administration reduced MDA content. The leaf tissues of lead-treated Trifolium pratense were found to produce high levels of MDA and ROS [50]. This situation was associated with membrane damage and lipid peroxidation due to oxidative damage caused by Pb stress. Exogenous MeJA administration reduced lipid peroxidation in Pb-stressed kenaf plants by increasing enzymatic and non-enzymatic antioxidant levels [46]. MeJA, especially its high concentration, has been shown to significantly inhibit oxidative stress indicators. As in many studies mentioned above, exogenous MeJA administration significantly reduced MDA content in response to Pb stress in the present study. Therefore, it can be concluded that oxidative damage was prevented in our study, especially at a high Pb (400 ppm) concentration, and high MeJA application significantly reduced MDA content.

To adapt to abiotic stress, plants produce various organic solutes, such as proline, protein, soluble carbohydrates, etc., which regulate different physiological functions. MDA and proline contents increase with increasing Pb concentration, according to the research on the effects of Pb toxicity on pepper (Capsicum annuum L.) plants [51]. According to reports, osmolytes, antioxidant enzymes, and carotenoids can accumulate when MeJA and SA are applied to plants exogenously, reducing the harmful effects of heavy metals [52, 53]. Our study determined that rice plants under Pb stress had lower proline and protein contents, which increased when plants were treated with exogenous MeJA and SA. Likewise, MeJA pretreatment under Pb stress restored cellular homeostasis, enhanced tolerance in kenaf plants, and increased osmolytes (proline, protein, and starch) [46]. In a study where Pb and MeJA were applied hydroponically to rice plants separately or in combination, the addition of MeJA improved the growth of rice under lead stress by adjusting proline metabolism [54]. According to Sofy et al. [55], exogenous treatments of JA, SA, and proline, as well as their combination, improved maize plants' capacity to withstand oxidative damage induced by Pb toxicity; especially the combination was the most effective treatment for growth and development. The combined application of MeJA + SA at a high Pb concentration increased the total protein and proline contents in the present study, which may be associated with the increased capacity of rice plants to withstand oxidative damage in response to stress. According to Sharma and Dubey [56], proline increases plant tolerance to heavy metal toxicity by acting as a metal chelator and protein stabilizer. Therefore, the increased proline and protein accumulation in elicitor-treated plants in this study may indicate that the plant defense mechanism is stimulated to adapt to stressful conditions.

Plants employ an antioxidant system to overcome the harmful effects of oxidative stress and accumulate secondary compounds to minimize the damage caused by free radicals, which results in lower lipid peroxidation and cell membrane damage. Numerous investigations have documented that phenolic and flavonoid compound levels increase when plants are subjected to environmental stressors [57]. Lajayer et al. [58] reported that phenolic chemicals play a significant role in the plant's non-enzymatic antioxidant system and help it withstand abiotic stress. Chen et al. [59] and Zoufan et al. [60] demonstrated a direct correlation between elevated secondary chemical synthesis and metallic stress resulting from lead and cadmium. A study on alfalfa (Medicago sativa L.) plants investigated varying doses of lead and determined that phenolic compounds increased in the leaves and roots of lead-treated plants [61]. It was reported that the total phenolic contents in the leaves of different barley (Hordeum vulgare L.) cultivars treated with lead increased with the increasing concentration of lead [62]. In our study, the flavonoid content increased while the total phenolic content decreased in rice plants exposed to Pb stress. Elicitors, particularly MeJA and SA, play a crucial role in plant defense responses by activating biosynthetic genes involved in secondary metabolites such as flavonoids, terpenoids, phenylpropanoids, and alkaloids in the signal transduction pathway [63, 64]. Bali et al. [65] reported that JA administered to tomato seedlings under Pb stress increased the expression of several genes associated with secondary metabolites (total phenols, polyphenols, flavonoids, and anthocyanins), which in turn decreased Pb toxicity. MeJA treatment was also shown to upregulate Brassica napus's expression of phenylalanine ammonia lyase in response to arsenic stress [66]. The present study showed that exogenous elicitor applications to rice (O. sativa L.) seedlings under lead stress caused an overall increase in total phenolic and flavonoid contents. This indicates that they play an important role in rice plants’ defense responses to Pb stress, as stated by the researchers.

The high concentration of Pb in plant cells causes partitioning, exclusion of Pb within cell vacuoles, and the formation of the insoluble Pb fraction in the cell wall and cell membrane [67, 68]. Recent research has demonstrated that jasmonates can control heavy metal transport systems, preventing buildup and boosting tolerance [48, 69]. According to Salavati et al. [54], MeJA applied to rice plants decreased Pb accumulation in shoots. The 400 ppm Pb (H3) application gave the highest value for Pb content in the present study, which decreased with MeJA and SA treatments in different ways depending on the elicitor type and concentration. Sharma et al. [47] reported that exogenous MeJA administration under Pb stress considerably reduced Pb uptake in two distinct bean cultivars' shoot and leaf tissues. It was concluded that MeJA reduces the negative effects of lead by promoting antioxidant enzyme activity and growth and reducing lead accumulation. Additionally, previous studies have obtained similar results regarding the reduction in Pb [65, 70], Cd [71], and As [48, 72] sorption with MeJA treatment. It has been emphasized that elicitors, particularly jasmonates, can function as signaling molecules that can decrease the expression of the heavy metal transporter protein and, in turn, reduce the uptake of metals. In the current study, MeJA treatments outperformed SA in lowering Pb absorption at a Pb concentration of 400 ppm. Consequently, as suggested by earlier research, MeJA treatment can be regarded as a useful technique for inhibiting heavy metal toxicity.

Conclusion

This study investigated changes caused by exogenous MeJA and SA elicitor treatments in local Karacadağ rice exposed to Pb heavy metal stress. The combined application of MeJA and SA gave the best results for all the parameters examined, especially at high Pb concentrations.

The research results revealed that the elicitors may improve photosynthetic pigment, total protein, proline, and secondary metabolite (total phenolic and flavonoid) contents and modulate the toxic effects of Pb by reducing MDA levels. These improvements may have been due to the synergistic effect of the stimulants, decreased Pb accumulation, and, thus, the minimization of the damage caused by ROS production. The combined use of the elicitors positively affected the stress tolerance levels even at high Pb concentrations, revealing the difference between the current study and previous research in the literature.

Furthermore, the present study’s findings provide new insights into the co-administration of MeJA and SA in plants exposed to Pb toxicity. However, further research is required to fully understand the biochemical process triggered by their synergistic effects and functions during Pb stress. To better grasp the effects of Pb exposure on plant growth and development, future research should understand the effects of MeJA + SA co-administration on the molecular processes of Pb uptake and accumulation.

Data availability

No datasets were generated or analysed during the current study.

Availability of data and materials

All data generated or analysed during this study are included in this published article.

Abbreviations

Pb:

Lead

SA:

Salicylic acid

MeJA:

Metil Jasmonat

FW:

Fresh Weight

QEs:

Quercetin Equivalents

GAEs:

Gallic Acid Equivalents

ROS:

Reactive oxygen species

MDA:

Malondialdehyde

min:

Minute

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Authors and Affiliations

  1. Department of Biology, Institute of Gradute Studies, Batman University, Batman, Türkiye

    Hıdır Altun

  2. Department of Food Process, Technical Science Vocational School, Batman University, Batman, Türkiye

    Pınar Orcan

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  1. Hıdır Altun
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P.O.,H.A. –Analysis, interpretation, literature review, writing. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Pınar Orcan.

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Altun, H., Orcan, P. Responses to exogenous elicitor treatment in lead-stressed Oryza sativa L.. BMC Plant Biol 24, 897 (2024). https://doi.org/10.1186/s12870-024-05600-9

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BMC Plant Biology

ISSN: 1471-2229

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