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Article

Sustainable Approaches to Alleviate Heavy Metal Stress in Tomatoes: Exploring the Role of Chitosan and Nanosilver

by
Marcelina Krupa-Małkiewicz
1 and
Ireneusz Ochmian
2,*
1
Department of Plant Genetics, Breeding and Biotechnology, West Pomeranian University of Technology Szczecin, Słowackiego 17 Street, 71-434 Szczecin, Poland
2
Department of Horticulture, West Pomeranian University of Technology Szczecin, Słowackiego 17 Street, 71-434 Szczecin, Poland
*
Author to whom correspondence should be addressed.
Agronomy 2024, 14(11), 2477; https://doi.org/10.3390/agronomy14112477
Submission received: 18 September 2024 / Revised: 15 October 2024 / Accepted: 21 October 2024 / Published: 24 October 2024
(This article belongs to the Section Plant-Crop Biology and Biochemistry)
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Abstract

:
This study investigates the impact of copper (Cu) stress on tomato plants (Solanum pimpinellifolium) and explores the potential of chitosan and nanosilver (nAg) in mitigating its effects. Copper, while essential for plant growth, can be toxic at elevated levels, leading to oxidative stress and reduced plant productivity. This research focuses on determining how chitosan and nAg treatments influence plant growth, fruit yield, and biochemical responses under Cu-induced stress. A greenhouse experiment was conducted, where tomato plants were treated with Cu, chitosan, nAg, and their combinations. The results revealed that chitosan improved root growth, and enhanced antioxidant properties, including increased ascorbic acid and lycopene content. Nanosilver treatments, while reducing shoot growth, significantly increased fruit yield and potassium uptake. The combination of Cu with chitosan or nAg provided synergistic benefits, improving plant resilience and fruit quality. Specifically, copper+chitosan (Cu+Ch) increased dry matter and delayed ripening, while Cu+nAg enhanced potassium uptake and overall fruit yield. Additionally, Cu accelerated the ripening of tomatoes. These findings suggest that chitosan and nanosilver are effective strategies to mitigate copper toxicity in tomato plants, offering a sustainable approach to improve crop productivity and quality under heavy metal stress conditions.

1. Introduction

Copper (Cu) is an essential micronutrient for plant growth, playing critical roles in various physiological processes, including photosynthesis, respiration, and enzyme activity. Some soils are naturally characterized by high Cu levels. However, in most soils, high Cu levels are due to the anthropogenic release of heavy metals into the environment from mining, smelting, agricultural production, and waste disposal technologies [1]. Excessive Cu concentrations can lead to toxicity, resulting in oxidative stress, impaired photosynthetic efficiency, and inhibited growth in plants [2]. Nevertheless, heavy metals as trace elements can play an important role in various redox reactions. For example, copper acts as a key cofactor for various enzymes involved in the oxidative stress response, such as catalase, superoxide dismutase, peroxidase, cytochrome c oxidase, ferroxidase, monoamine oxidase, and dopamine β-monooxygenase [3].
Tomato plants are globally significant both nutritionally and economically, being the second most consumed vegetable worldwide. They are rich in essential nutrients like lycopene, vitamin C, and flavonoids, contributing to their high dietary value [4,5]. Solanum pimpinellifolium, known as the currant tomato, is a wild tomato species native to Ecuador and northern Peru, characterized by its small, sweet, and cherry-like fruits [6]. It is a valuable genetic resource for breeding programs due to its high genetic diversity, disease resistance, and tolerance to abiotic stresses like drought and salinity [7]. Researchers utilize S. pimpinellifolium to introduce desirable traits such as improved flavor [8], enhanced disease resistance [9], and greater stress tolerance into cultivated tomato varieties [6]. However, tomatoes are particularly sensitive to heavy metal stresses, including copper (Cu) [10], Cd [11], and Zn [12]. In countries like Spain, Italy, and Greece, where tomatoes are widely grown, copper-based fungicides have been used extensively to control fungal diseases, particularly in vineyards, olive groves, and vegetable crops, including tomatoes. This is especially relevant when these fungicides are used in areas where mixed agricultural activities, such as vineyards and vegetable cultivation (e.g., tomatoes), coexist. Studies have indicated that copper fungicide residues can accumulate in soils and lead to the uptake of not just copper but also other heavy metals, thereby affecting crops like tomatoes, which are sensitive to heavy metal stress. This long-term use has led to soil copper accumulation, which can cause toxicity in sensitive crops like tomatoes [13,14]. Excessive Cu can disrupt plant physiological processes, leading to stunted growth and reduced productivity [15]. Given these challenges, exploring effective mitigation strategies to alleviate Cu stress in tomato plants is crucial for sustaining their cultivation and productivity.
The negative effects of environmental stresses on plants have contributed to the search for new solutions, such as the use of biologically active substances or nanotechnology. Nanotechnology, as a relatively new scientific field, has a very broad application in agriculture. Silver nanoparticles are one of the rapidly developing engineered nanomaterials, increasingly utilized across various consumer products. Recently, metal-based nanomaterials, such as silver nanoparticles, have gained significant attention due to their environmentally friendly applications, particularly in agriculture, where they help improve sustainability and stress management in crops [16]. The use of various nanoparticles makes it possible to reduce ion deficiency in plant tissues. This contributes to increasing the tolerance of plants to stress factors, thereby improving growth and increasing yields [17]. Nanosilver (nAg), with its unique physicochemical properties, has been investigated for its role in plant stress management. nAg exhibits potent antimicrobial properties and has been reported to enhance plant growth and stress tolerance by modulating physiological and biochemical pathways [18,19]. In the context of Cu stress, nanosilver can reduce the accumulation of reactive oxygen species (ROS) and enhance the activity of antioxidant systems, thereby protecting plants from oxidative damage. Additionally, nAg can influence gene expression related to stress responses, further contributing to plant resilience under Cu stress [20]. The use of chitosan may also be an alternative solution for mitigating the effects of environmental stress on plants. Chitosan (Ch), a natural polysaccharide derived from chitin, has garnered attention for its potential to enhance plant stress tolerance. Its biocompatibility, biodegradability, and ability to elicit plant defense responses make it an attractive candidate for alleviating heavy metal stress [21]. Chitosan application has been shown to improve plant growth [22], enhance antioxidant enzyme activities, and reduce oxidative damage under various abiotic stresses [23]. Specifically, chitosan can increase the activity of key antioxidant enzymes such as superoxide dismutase (SOD) and catalase (CAT), which mitigate oxidative damage caused by Cu stress [24]. Furthermore, chitosan can improve water retention and nutrient uptake, enhancing overall plant health and resilience [25].
The combination of chitosan and nanosilver may offer a synergistic approach, providing a dual mechanism to counteract the detrimental effects of Cu stress in tomato plants. Chitosan can improve physical and biochemical plant defenses, while nanosilver can enhance stress tolerance at the molecular level. This study aims to investigate the alleviating effects of chitosan and nanosilver on tomato plants under Cu stress. By evaluating growth parameters, photosynthetic performance, and biochemical responses, this research seeks to elucidate the potential of these compounds in enhancing tomato plant resilience to Cu-induced toxicity. The findings could contribute to developing sustainable and effective strategies for managing heavy metal stress in crop production.

2. Materials and Methods

2.1. Plant Materials

A greenhouse experiment was conducted at the Department of Plant Genetics, Breeding and Biotechnology and the Department of Horticulture at the West Pomeranian University of Technology Szczecin, Poland. Plants of Solanum pimpinellifolium were derived from an in vitro culture. Explants were initially selected under heavy metal (Cu) stress under in vitro conditions [5] and then made adaptive to in vivo conditions at the beginning of June 2023 (Figure 1). The plantlets with well-developed shoots and roots were transferred into round plastic pots with a volume of 400 mL, and filled with approximately 100 g of the commercial substrate, based on miller peat+chalk+NPK 14-16-18 for growing tomato, at pH 5.5–6.5. The pots were placed on 60 cm high tables in the greenhouse at 20 °C/15 °C day/night temperature cycles and a light intensity of 110 mol m−2 s−1 during the experimental period. The temperature inside the greenhouse was regulated by automatically opening vents, and automated shading screens were used to reduce heating during the day and limit heat loss at night. After three weeks of the transplantation, the plants were irrigated (100 mL solution per pot) with 18 mg L−1 CuSO4 (7.2 mg Cu L−1) (Chempur, Piekary Śląskie, Poland), 20 ppm chitosan (Ch) of molecular weight 3.33 kDa (Center of Bioimmobilisation and Innovative Packaging Materials at West Pomeranian University of Technology in Szczecin, Szczecin, Poland), a solution of 6 mg L−1 nAg (<100 nm Merck, Darmstadt, Germany, PCODE 1003419144 CAS No 7440-22-4 MKCQ4804), and combinations of Cu+20 ppm Ch and Cu+6 mg L−1 nAg. Control plants were irrigated with 100 mL of distilled water. Each treatment was repeated six times at weekly intervals. The tomato plants were grown for seven weeks. On the last day of the experiment, the plants were removed from the pots and rinsed in tap water, and the morphological characteristics (shoot and root length (cm), weight of 1 fruit, percent of ripe and unripe fruits) were recorded.

2.2. Measurements in Leaves and Fruits

Extraction of a compound mixture of tomato was performed using 70% ethanol, at 20 °C, for 60 min, with constant stirring. Following centrifugation at 4000 rpm for 10 min, the supernatant was filtered under reduced pressure through a cellulose membrane with a 1.2 μm pore diameter, and the supernatant was concentrated at 40 °C in a vacuum evaporator, to remove acetone. Subsequently, the aqueous phase was diluted with water. The plant extract was serially diluted using redistilled water to obtain a gradient of concentrations for use in analytical and biological activity assays [26]. Total polyphenol contents (TPCs) were determined spectrophotometrically employing the Folin–Ciocalteu reagent (Sigma-Aldrich, Steinheim, Germany). The standard curve, calculated using gallic acid as a standard, was measured spectrophotometrically at 700 nm and expressed as mg of gallic acid equivalents (GAEs) per mg g−1 of plant material [27].
To extract carotenoids from tomato samples, five grams of tomato fruit was first weighed and then thoroughly ground in a mortar, together with 1 g of quartz sand and 0.5 g of ascorbic acid. The extraction process started by binding water with methanol, following a previously described method. Carotenoids were extracted using 1,2-dichloroethane through a liquid–liquid partitioning technique. After adding 1 mL of doubly distilled water, the mixture was mechanically shaken for 15 min to separate the polar and non-polar phases. The lower, non-polar phase was then separated using a separating funnel. The non-polar phase was dried over anhydrous sodium sulfate (Na2SO4) and the solvent was evaporated under a vacuum at 30 °C. The remaining residue was dissolved in HPLC-grade acetone or in a 30% dichloromethane in methanol solution. Finally, the sample was filtered through a 0.45 µm PTFE syringe filter, making it ready for high-performance liquid chromatography (HPLC) analysis [28]. The content of β-carotene (provitamin A) in tomatoes was determined by high-performance liquid chromatography with UV and fluorescence detection [29]. Ten average-weight, red ripe fruits per replication were chosen for the measurements.
2,2′-azo-bis-3-ethylbenzothiazoline-6-sulfonic acid (ABTS•+) was used to observe the enzyme kinetics of assays [30]. Additionally, DPPH (1,1-diphenyl-2-picrylhydrazyl) and the ferric reducing antioxidant property (FRAP) were also determined [31,32]. The antioxidant capacity was expressed as millimoles of Trolox per 100 g of distilled water. ABTS•+ and FRAP assay measurements were carried out on a UV-2401 PC spectrophotometer. Sigma-Aldrich (Steinheim, Germany) reagents were used.
The sample was dried at 65 °C ± 2 °C until a constant weight was achieved. The dry matter content was then calculated based on the difference in the sample’s mass before and after drying. The dry matter was determined using three repetitions of 250 g from each combination.
Titratable acidity was determined using a potentiometric method and expressed as equivalents of citric acid. The soluble solid content was determined with a digital refractometer, PAL-1 (Atago, Tokyo, Japan). L-ascorbic acid and nitrate content was measured with an RQflex 10 requantometer (Merck, Darmstadt, Germany) [33]. All samples were assayed in triplicate.

2.3. Elemental Analysis

The estimation of the mineral content in dry-weight plants was carried out using certified reagents (Chempur, Piekary Śląskie, Poland; Merck, Darmstadt, Germany). All tests were performed in three replications. After harvesting the leaves and fruits (tomatoes), a harvest sample was prepared, which was dried and ground. The content of elements in leaves and fruits was determined after mineralization: N, P, K, Mg, and Ca were measured after wet mineralization in H2SO4 (96%) and HClO4 (70%). The content of Cu, Zn, Mn, and Fe was determined after mineralization in HNO3 (65%) and HClO4 (70%) in a ratio for leaves and fruits of 3:1.
The total nitrogen concentration in plants was determined by the Kjeldahl distillation method using a Vapodest 30 (Gerhardt GmbH, Königswinter, Germany). The content of K was measured with the atomic emission spectrometry; Mg Ca, Cu, Zn, Mn, and Fe content was measured with the flame atomic absorption spectroscopy using iCE 3000 Series (Thermo Fisher Scientific, Waltham, MA, USA). Phosphorus (P) was assessed by the colorimetric method on a Specol 221 apparatus (Carl Zeiss, Jena, Germany) [34].

2.4. Leaf Pigment Estimation

Leaf pigment estimation, with the pigment extracted from the middle part of the shoot, was conducted using a spectrophotometer CM-700d (Konica Minolta, Tokyo, Japan). Measurements were conducted in the CIE L*a*b* system [35], employing the 10° observer type and D65 illuminant. Color readings were taken in triplicate for each experimental combination.
The pigment contents were displayed on the screen as the Normalized Difference Vegetation Index (NDVI) and Normalized Anthocyanin Index (NAI) (type pigment analyzer 1101, Control in Applied Physiology, Berlin, Germany) [36].

2.5. Proline and MDA

The concentration of proline was determined according to the method of Bates et al. [37] using a spectrophotometer at 520 nm in leaves and calculated as µmol g−1 fw. The content of the malondialdehyde (MDA, a product of lipid peroxidation) in plant tissue was determined by the method described by Sudhakar et al. [38] using the MDA Assay Kit (Dojindo Laboratories Tabaru, Kumamoto, Japan). The concentration of MDA was calculated from the absorbance at 600, 532, and 450 nm, and MDA contents were estimated using the following equations:
MDA (nmol·g−1 fw) = [6.45 × (A532 − A600) − 0.56 A450] × V/fw.
where V is the volume of the sample, A is the absorbance, and fw is the fresh weight.

2.6. Statistical Analysis

All statistical analyses were performed using Statistica 12.5 (StatSoft Polska, Cracow, Poland). Statistical significance of the differences between means was determined by testing the homogeneity of variance and normality of distribution, followed by an ANOVA with Tukey’s post hoc test. The significance was set at p < 0.05.

3. Results and Discussion

3.1. Growth and Yield

Plants respond to various environmental stresses by modifying internal processes. Copper toxicity can lead to severe ultrastructural damage, thus affecting key biochemical transformation processes in plants. It has been observed that the application of several chemical compounds can perform anti-stress functions in the plant, alleviating the adverse effects of abiotic stresses on plants. The results of the application of chitosan and nAg on the shoot and root length of tomato plants under Cu stress conditions are given in Table 1. Our results showed that there were no statistical differences between explants grown on different mediums despite the fact that the tomato plants after application of nAg and nAg with Cu were 30% and 27%, respectively, smaller in comparison to the control. The control group shows a steady increase in shoot length over time, reaching an average shoot length of 42.6 cm by the end of the experiment. The application of Cu results in a slightly higher growth rate compared to the control, with a mean shoot length of 45.5 cm. The shoot length at each measurement point is consistently higher than the control. The application of chitosan to the tomato plants under stress conditions shows a reduced growth rate compared to Cu alone, with a mean shoot length of 40.9 cm, slightly below the control group. However, the application of chitosan alone results in a mean shoot length of 40.4 cm, similar to the combination with Cu, indicating chitosan may slightly inhibit shoot growth compared to the control. The most noticeable changes were after the application of the nanosilver solution. These plants grew much more slowly in in vitro culture and were therefore smaller than the other combinations of the experiment at the very beginning of the field experiment. The application of nanosilver significantly reduces the shoot length compared to the control and other treatments, with a mean shoot length of 32.3 cm. In addition, the combination of nAg and Cu shows a slight improvement over nanosilver alone but is still substantially lower than Cu alone (27%) or with chitosan (19%), with a mean shoot length of 33.0 cm. It was observed that the root lengths of tomato plants treated with Cu and Ch alone were on the same level and were higher than the control by 48% and 53%, respectively (Table 1). However, the longest roots were characterized by plants treated with Cu and Ch (174% of control) and treated with Cu and nAg (167% of control). The application of nAg alone did not influence the length of the root, which was similar to the control.
In the study provided, copper (Cu) at a 100 µM concentration was shown to enhance both shoot and root growth compared to the control group. According to Mediouni et al. [2] and Chen et al. [39], Cu is an essential micronutrient for plant growth and development. Copper acts as a cofactor for various enzymes involved in photosynthesis, respiration, and antioxidant defense systems. These functions are critical for normal plant growth and metabolism. The results of this study confirmed that moderate copper levels can enhance shoot and root length. In contrast, Mediouni et al. [2] observed that 7-day tomato seedlings after growing on nutrient solution supplemented with different concentrations of CdCl2 or CuSO4 resulted in the inhibition of shoot and root growth despite low metal concentrations being applied. Ernst et al. [40] observed that barriers may exist in the roots of higher plants to prevent the movement of heavy metals to the shoot tips. Hence, some tolerance mechanisms are likely to be present in root cells. The application of chitosan under stress conditions results in a positive impact on the root length of tomato plants. This is in line with the study of Pongprayonn et al. [41] in rice, Jabeen and Ahmad [42] in safflower and sunflower, Krupa-Małkiewicz and Smolik [21] in Petunia × atknsiana D. Don., and Ullah et al. [43] in tomato. The application of nAg alone did not significantly affect root length, which remained similar to the control. This suggests that while nAg can have a pronounced negative impact on shoot growth, its effect on root growth is less clear and may depend on other interacting factors such as nutrient availability and soil conditions [39]. Also, Rostami and Shahsavar [44] confirmed the negative impact of nAg on the morphological traits of Olea europea L. plants. Their findings revealed that increased nAg concentration led to a reduction in the growth of explants.
In regard to the reproductive stage, various treatments (Cu, Cu+Ch, Ch, Cu+nAg, nAg) result in different effects on fruit weight (Figure 2). The most significant increase in the weight of one fruit of tomato was observed after treatment of Cu+Ch (207% compared to the control) and nAg alone (151% compared to the control). Conversely, for red fruit, yield decreases or shows modest increases depending on the treatment. The application of copper (Cu) alone resulted in the complete ripening of all fruits, suggesting that copper may accelerate the ripening process (Figure 3). In contrast, the combination of copper with chitosan (Cu+Ch) and chitosan alone (Ch), and also Cu+nAg, clearly delayed ripening, as the majority of fruits remained unripe. For example, Cu+Ch reduces red fruit yield to 29.7% compared to the control, whereas plants treated with nAg increase it to 152% compared to the control. Moreover, the highest increase in the yield of green tomato fruits was recorded with the Cu+nAg, Ch, and nAg treatments (572%, 315%, and 247% compared to the control, respectively) (Figure 4). Notably, nAg treatments enhance both weight and yield across different fruit types compared to the control. A significant increase in total fruit yield (145% compared to the control) with the highest number of green fruit (572% compared to the control) was also observed after treatment with the Cu+nAg solution. These results suggest that copper accelerates ripening, while chitosan and nanosilver may have the opposite effect, delaying the process.
Similar observations were described by Hernández et al. [25] after the application of CuNPs. According to them, the increase in tomato fruit yield was due to the ability of CuNPs to cause a greater accumulation of photosynthates in organs requiring a supply of nutrients, or the activation of genes that determine plant growth and development. Similarly, Wang et al. [45] described a 10% increase in tomato yield after the application of CeO2 NPs at a concentration of 10 mg L−1. They suggested that this effect was probably due to the plants transferring more energy to fruit growth. In contrast, Sonmez et al. [46] observed that total yield, fruit number, root dry weight, and plant height decreased with increasing soil Cu content. Data shown by El Amerany et al. [47] indicated that a foliar spray of chitosan, especially at 0.75 mg L−1, can improve the growth of tomato plants. However, there was no significant effect on yield after the application of 1 mg L−1 of chitosan. They suggested that the reducing effect of 1 mg L−1 chitosan on plant and fruit growth might be related to the high production of ethylene.
It can therefore be assumed that the addition of nanosilver extended the ripening period of tomato fruit (Figure 3), while also increasing the yield (Figure 4). This effect was reflected in the color of the leaves and fruit (Figure 5), the content of macro- and microelements (Table 2 and Table 3), and the NDVI (Figure 6). It was observed that the leaves of plants treated with Cu+nAg and nAg solutions were characterized by a significant decrease in N content (48.3% and 52.5% compared to the control, respectively) while increasing the nitrogen content in fruits (127% and 107% compared to the control, respectively).
The study showed that different soil additives significantly affected the ripening of tomato fruits (Figure 3). In the control group, approximately 70% of the fruits ripened, serving as a baseline for comparison. The application of copper (Cu) alone resulted in full ripening of all fruits, suggesting that copper may accelerate the ripening process. In contrast, the combination of copper with chitosan (Cu+Ch) and chitosan alone (Ch) clearly delayed ripening, as most fruits remained unripe. Similarly, the combination of copper with nanosilver (Cu+nAg) resulted in most fruits ripening, although some remained green, indicating a moderate effect. Nanosilver alone also delayed ripening, with nearly equal numbers of ripe and unripe fruits. These results suggest that copper accelerates ripening, while chitosan and nanosilver have the opposite effect, delaying the process.
Soil-applied chitosan may have a significant impact on delaying fruit ripening, although its mechanism of action may differ from foliar applications. The primary effect of soil-applied chitosan is improving plant health by enhancing nutrient uptake, increasing resistance to environmental stress, and stimulating antioxidant enzyme activity. Chitosan activates enzymes like catalase and superoxide dismutase, which help reduce the accumulation of reactive oxygen species (ROS) in the plant. Reduced oxidative stress leads to slower cellular breakdown in fruits, thereby delaying ripening [48]. Our findings are similar to Hemeir et al. [49] who describe that no tomato plant could grow at concentrations of 1000 and 2000 mg kg−1 Cu. In contrast, Cu addition at 200 mg kg−1 increased the production of fresh biomass of the above-ground parts. At 500 mg kg−1, the effect of Cu application became negative.

3.2. Pigmentation and Stress Markers

The leaves in the control sample were darker and had an intense green hue. The application of CuSO4 and nanosilver lightened the leaves and reduced the intensity of the green color, shifting the shade toward a more yellowish hue. In other studies, Cu applied at a dose of 100 mg kg−1 of soil significantly decreased SPAD levels, which also indicates that the leaves became lighter [3]. The fruits in the control sample were relatively bright and had a moderate red and yellow hue. The application of Cu darkened the fruits but increased the intensity of the red hue, while nanosilver made them both more red and yellow.
The presence of Cu, whether in deficiency or excess, can significantly impact the pigment profile, especially anthocyanins and carotenoids. Excessive copper in the soil can reduce chlorophyll content, leading to more intense red and yellow hues in tomato leaves and fruits, which directly affects the commercial quality of tomatoes [50]. In appropriate amounts, copper can also increase the intensity of red in tomato fruits by stimulating the accumulation of carotenoids such as lycopene, a key pigment responsible for the red color of the fruit [51].
Silver nanoparticles (nAg) increase the activity of stress-resistant enzymes, which can help reduce oxidative damage and improve plant tolerance to stress [52]. The application of nAg enhances chlorophyll content in leaves, leading to improved photosynthesis efficiency and increased uptake of essential nutrients such as nitrogen, phosphorus, and potassium [53,54]. However, our research did not confirm such a relationship. The effectiveness of nAg might depend on the method of its application.
The results highlight the effects of different soil treatments on the NAI (Normalized Anthocyanin Index) and NDVI (Normalized Difference Vegetation Index), which are indicators of plant health and stress response (Figure 6), as well as the proline and malondialdehyde (MDA) content in tomato leaves (Figure 7).
The NAI, which measures anthocyanin content (a plant pigment associated with stress response), was highest in the control group (0.28), while copper and nanosilver treatments resulted in negative NAI values (−0.37 for Cu+nAg and −0.22 for nAg), indicating a significant reduction in anthocyanin content, likely due to stress.
The Normalized Difference Vegetation Index (NDVI), calculated as the normalized difference between red and near-infrared spectral bands, is widely recognized as a key structural vegetation index and serves as a numerical measure of vegetation greenness [55]. The NDVI, which frequently exhibits a nonlinear temporal trend in tomato plants [56], has been used to track changes in canopy structure. These changes are often the result of stress factors affecting the plants [57,58].
The NDVI, an indicator of photosynthetic activity, was highest in the control group (0.73), reflecting healthy plant growth. Copper alone significantly reduced the NDVI to 0.64, and the Cu+nAg and nAg treatments resulted in the lowest NDVI values (0.29 and 0.33, respectively), suggesting that these treatments severely impaired the plants’ photosynthetic efficiency. Copper induces the highest stress levels in tomato plants, as reflected by increased proline and MDA content and reduced NAI and NDVI values. Chitosan appears to mitigate some of the negative effects of copper, while nanosilver combined with copper (Cu+nAg) shows moderate stress indicators, although it still reduces overall plant health, as indicated by the negative NAI and low NDVI values.
Proline, an amino acid involved in stress tolerance, shows the highest concentration in leaves treated with copper (Cu), at 15.2 μmol g−1, indicating a significant stress response. The combination of copper and nanosilver (Cu+nAg) also resulted in elevated proline levels (12.6 μmol g−1), though not as high as Cu alone. Lower proline levels were observed in the control (8.4 μmol g−1) and chitosan-only (Ch) treatments (7.7 μmol g−1), suggesting minimal stress under these conditions. The application of copper increased the accumulation of proline and polyphenols. This accumulation significantly increased with higher doses of Cu [59]. In terms of MDA, a marker of oxidative stress and cell membrane damage, the highest levels were again seen in copper-treated plants (31.0 nmol g−1), indicating severe oxidative stress. The Cu+nAg treatment showed slightly lower MDA levels (27.3 nmol g−1), while the control group exhibited the lowest MDA content (18.9 nmol g−1), suggesting minimal oxidative damage in untreated plants.

3.3. Mineral Content of the Leaves and Fruit

The toxicity threshold for copper in soil is 100 mg kg−1 [60]. At a copper content level of 500 mg kg−1, negative effects on plants were observed [49]. Copper binds to clay minerals and humus, and its solubility depends on soil pH, element interactions, redox properties, and climate [61,62,63]. Soils may have elevated copper levels due to the intensive use of pesticides and fertilizers [64,65], particularly in organic farming [66]. Since Cu moves very minimally in most soils, the potential for Cu accumulation in tomato fields is significant during continuous tomato cultivation [67].
In the leaves, the highest nitrogen (N) content was found in the control group (4.93 g 100 g−1), with slightly lower values observed in the chitosan (Ch) treatment (4.82 g 100 g−1). The Cu+nAg treatment had the lowest nitrogen content (2.55 g 100 g−1). Soils used for tomato cultivation require large amounts of nitrogen fertilizers, which lead to greater bioavailability of this element in the fruits [68].
The content of potassium (K) was highest in the Cu+nAg treatment (4.11 g 100 g−1), indicating a positive effect of this combination on K uptake. In contrast, the control group exhibited a lower potassium level (3.37 g 100 g−1). Calcium (Ca) content was elevated in Cu+Ch (2.17 g 100 g−1) and Cu+nAg (1.85 g 100 g−1), while magnesium (Mg) and phosphorus (P) levels were generally lower across treatments, with the lowest levels found in Cu+nAg. The copper (Cu) concentration in leaves was highest in the Cu+nAg treatment (20.8 mg 1000 g−1), showing increased copper uptake, while the control group had the lowest copper concentration (16.5 mg 1000 g−1). Depending on the species, copper levels in leaves generally range up to 20 mg kg−1 [69,70]. However, concentrations as high as 1490 mg kg−1 have been reported, while the maximum allowable tolerance level is 200 mg kg−1 [71]. Elevated copper levels in the soil contribute to higher copper content in fruits [67].
In the fruits, nitrogen content was highest in the Cu+nAg and Ch treatments (246 and 239 mg 100 g−1, respectively), while the control group had a moderate nitrogen level (194 mg 100 g−1). Potassium content followed a similar trend, with the highest levels in Cu+nAg (293 mg 1000 g−1) and the lowest in the control group (211 mg 1000g−1). Copper content was again highest in the Cu+nAg treatment (118 mg 1000 g−1) and lowest in the control (105 mg 1000 g−1). Calcium and magnesium levels were generally lower across all treatments, with the lowest levels of calcium observed in Cu+nAg (30 mg 1000 g−1) and the lowest magnesium in Cu+Ch (15 mg 1000 g−1).
Overall, the Cu+nAg treatment increased the uptake of key elements like potassium and copper, both in leaves and fruits, but resulted in lower levels of nitrogen, magnesium, and calcium in certain cases. The chitosan treatment appeared to balance elemental content, with high nitrogen and potassium levels and moderate copper uptake. Chitosan is most commonly applied as a foliar spray and exhibits a copper-chelating effect [72]. When applied to the soil, it helped alleviate stress caused by excess boron in the soil [73]. The control group showed moderate elemental content across all parameters, serving as a baseline for comparison.
Based on the relationships depicted in the image and the elemental content data from the table, we can infer several interactions between elements in tomato leaves and fruits, taking into account the synergistic and antagonistic effects between elements.
Potassium (K) shows antagonism with calcium (Ca) and magnesium (Mg). This explains why in treatments with high potassium content (such as Cu+nAg), the calcium and magnesium levels are lower in both leaves and fruits. For example, the Cu+nAg treatment has high potassium content (411 mg 1000 g−1 in leaves and 293 mg 1000 g−1 in fruits) but lower calcium and magnesium levels, which is consistent with the antagonistic relationship between these elements.
Calcium (Ca) and magnesium (Mg) are synergistic, meaning they often increase together. In the control and chitosan treatments, where calcium content is higher, magnesium levels are also relatively higher in both leaves and fruits, suggesting a positive correlation. For instance, the control group has relatively high Ca (211 mg 1000 g−1 in leaves) and Mg (49 mg 1000 g−1 in leaves), demonstrating this synergy.
Copper (Cu) shows antagonism with iron (Fe) and zinc (Zn). In treatments where copper content is elevated, such as Cu+nAg, zinc and iron levels are affected. While copper content in Cu+nAg is high (208 mg 1000 g−1 in leaves), zinc and iron show relatively lower levels compared to other treatments, illustrating this antagonistic effect.
Phosphorus (P), which shows antagonistic interactions with several elements, such as calcium, magnesium, and zinc, is generally lower in the Cu+nAg and Cu+Ch treatments, whereas other elements (like copper) are higher. This suggests that the presence of high copper concentrations can inhibit phosphorus uptake, likely due to these antagonistic relationships.
Sodium (Na) does not show strong interactions in this dataset, but its levels in treatments like Cu+nAg are lower than in other treatments, which might suggest some indirect interactions, particularly with potassium.
Nitrogen (N) and potassium (K) have a synergistic relationship, as observed in the treatments where potassium content is higher (such as Cu+nAg and Cu+Ch), and where nitrogen levels are also elevated. This is particularly clear in fruits, where high potassium corresponds with high nitrogen content. Hemeir et al. [49] and Toselli et al. [74] showed that Cu applied to soil is antagonistic to K.

3.4. Fruit Quality and Health-Promoting Properties

The results show that different soil treatments significantly influence the chemical composition and quality of tomato fruits. The highest dry matter content was observed in tomatoes treated with a combination of copper and chitosan (Cu+Ch), indicating that this treatment enhances the accumulation of solid substances in the fruit. Soluble solids, which reflect sugar content, were highest in the control group and the chitosan-treated tomatoes, suggesting that these treatments lead to sweeter fruits. Interestingly, the Cu+nAg treatment resulted in the highest titratable acidity, which may contribute to a stronger, more intense flavor, while chitosan alone produced the least acidic fruits (Table 4).
In terms of ascorbic acid (vitamin C) content, tomatoes in the control group had moderate levels, while the application of copper alone significantly reduced this important antioxidant. However, both chitosan and its combination with copper (Cu+Ch) boosted the ascorbic acid levels, highlighting the potential of these treatments to improve the nutritional value of the fruit. The highest β-carotene content, responsible for the orange color and vitamin A activity, was found in tomatoes treated with copper, while chitosan resulted in lower levels of this compound.
According to Leonardi et al. [75], the proximate composition, as well as the physical and biochemical properties of tomatoes, are influenced more significantly by their maturity and ripening stages than by their genotype. Additionally, Soytong et al. [76] described that the correlation between results obtained with methods used for β-carotene determination was lower and depended on the color of the tomato fruits. Starch accumulates in green tomatoes, and its content begins to decrease with the onset of ripening, accompanied by an increase in soluble solid content [77]. The total content of soluble solids increases with color and ripeness [78]. Rodriguez et al. [79] observed soluble solid contents in tomatoes ranging from 4.08 °Brix to 8.68 °Brix, while acidity may range from 0.26 g 100 g−1 to 0.91 g 100 g−1. The values of the tomatoes from our study fall within this range, with the soluble solid content in the upper range and the acidity in the lower range, which may be due to the fact that the variety we studied belongs to the fresh consumption varieties, and such tomatoes need to be sweeter. As the soluble solids increase, titratable acidity decreases [80].
In plants, the metabolism of L-ascorbic acid is correlated with defense against oxidative stress [81]. The vitamin C content ranged from 22.61 mg 100 g−1 FW in ‘Argeș 11’ to 32.21 mg 100 g−1 FW. These values are higher than those observed in our study.
Lycopene, a powerful antioxidant known for its health benefits and contribution to the red color of tomatoes, was most abundant in the chitosan-treated group, indicating that this treatment enhances the health-promoting properties of the fruit. In contrast, copper alone resulted in the lowest lycopene levels, suggesting that while copper improves certain aspects of fruit quality, it may reduce others. Overall, these findings demonstrate that specific combinations of soil treatments, such as Cu+Ch and chitosan alone, can modulate different aspects of tomato fruit quality, depending on the desired characteristics such as sweetness, acidity, or antioxidant content. The lycopene content of fresh tomatoes ranges from 15 to 160 mg and depends on the agronomics, harvest date, and cultivar of the fruit [82]. Leaves taken from plants treated with Ch and control plants had the highest nitrogen content and the largest amount of lycopene in the fruits, although this amount was at the lower end of the ranges reported in the literature. When the availability of nitrogen (N) is limited, the C/N balance in plants can be disrupted, which restricts the production of metabolites [83].
The results from Table 5 indicate that different soil treatments, including copper (Cu), chitosan (Ch), and nanosilver (nAg), significantly influence the antioxidant capacity and phenolic content of tomato fruits. In the ABTS•+ assay, which measures antioxidant activity, the lowest value is observed in the chitosan-only (Ch) treatment (79 μmol T g−1), suggesting that chitosan enhances the antioxidant potential of the tomatoes by reducing their oxidative stress. Conversely, the Cu+Ch treatment has the highest ABTS•+ value (151 μmol T g−1), indicating a weaker antioxidant effect.
In the DPPH assay, lower values reflect stronger antioxidant activity. The lowest value is found in the Cu+nAg treatment (156 μmol T g−1), indicating that the combination of copper and nanosilver provides the best antioxidant protection in this test. On the other hand, the control group (211 μmol T g−1) and copper alone (204 μmol T g−1) show higher values, indicating weaker antioxidant activity.
Our results are in line with the findings of Sharma et al. [84] regarding the effects of Cu on S. lycopersicum. They reported an increase in ABTS•+ and DPPH values with moderate copper treatments, which was attributed to the enhanced synthesis of flavonoids and phenolic acids, leading to improved antioxidant capacity. Also, Zhou et al. [85] confirmed in their study on Cucumis sativus that copper nanoparticles (CuNPs) positively influenced antioxidant activities, including DPPH radical scavenging ability, suggesting that Cu may enhance the production of phenolic compounds. This results in higher antioxidant capacity. These studies suggest that Cu, particularly in nanoparticle or sulfate forms, can enhance the antioxidant activities (DPPH and ABTS•+ assays) in various plants by boosting phenolic compounds and antioxidant enzyme systems, though the effect is dose-dependent.
The FRAP assay also supports this trend, with the Cu+nAg treatment showing a low value (185 μmol T g−1), meaning stronger reducing power, while Cu alone (129 μmol T g−1) and Ch (143 μmol T g−1) exhibit higher values, indicating weaker antioxidant capacity.
Soil contamination with heavy metals can have varying effects on the free radical scavenging ability of extracts prepared from tomatoes. In most cases, a decrease in scavenging capacity was observed, although some heavy metals increased the activity of the tested tomatoes [86].
For total phenolic content, which is a key indicator of antioxidant compounds, the highest values are found in the nanosilver (55.8 mg GAE kg−1) and chitosan (52.4 mg GAE kg−1) treatments, suggesting that these treatments increase the concentration of phenolic compounds in the fruits, potentially contributing to their higher antioxidant capacity. Copper combined with chitosan (Cu+Ch) and copper alone show lower phenolic content, indicating that while Cu stress influences phenolic production, chitosan and nanosilver may mitigate some of its negative effects. Higher concentrations of nAg caused greater stress in plants compared to the control, resulting in increased production of proline and a decrease in polyphenol levels [87]. The content of phenolic compounds is highly dependent on cultivation conditions and the occurrence of stress factors in the fields. Kisa et al. [88] observed a decrease in polyphenol content in tomatoes, which became more pronounced with increasing copper levels in the soil.
The combination of copper with nanosilver (Cu+nAg) shows the best overall antioxidant capacity, as evidenced by lower values in the ABTS•+, DPPH, and FRAP assays, while chitosan and nanosilver treatments increase phenolic content and also contribute to enhancing antioxidant properties under copper-induced stress. Copper alone exhibits the weakest antioxidant activity, highlighting the importance of using mitigating agents like chitosan and nanosilver to alleviate stress effects.

4. Conclusions

  • The application of chitosan significantly improved root development in tomato plants under copper-induced stress. It also enhanced antioxidant properties by increasing ascorbic acid and lycopene content, contributing to better plant health and fruit quality.
  • Treatment with nanosilver resulted in a notable increase in fruit yield and potassium uptake, despite a reduction in shoot growth. This suggests that nanosilver can enhance certain growth parameters and nutrient assimilation under copper stress.
  • Combining copper with either chitosan or nanosilver provided synergistic benefits. The Cu+chitosan treatment notably increased dry matter content and delayed fruit ripening, while Cu+nanosilver improved potassium uptake and overall fruit yield, enhancing both plant resilience and fruit quality.
  • Both chitosan and nanosilver treatments influenced the levels of stress markers such as proline and malondialdehyde (MDA) in tomato plants. These treatments helped in mitigating oxidative stress caused by excessive copper, leading to improved plant vitality.
  • The treatments modulated the uptake and distribution of essential nutrients like nitrogen, potassium, calcium, and magnesium in both leaves and fruits. This adjustment in nutrient balance contributed to the plants’ ability to cope with copper toxicity.
  • The use of chitosan and nanosilver presents effective and sustainable strategies to alleviate heavy metal stress in tomato cultivation. Implementing these treatments can enhance crop productivity and fruit nutritional value under adverse environmental conditions caused by heavy metal contamination.

Author Contributions

Conceptualization, M.K.-M.; methodology, M.K.-M. and I.O.; software, M.K.-M. and I.O.; validation, M.K.-M. and I.O.; formal analysis, M.K.-M. and I.O.; investigation, M.K.-M. and I.O.; resources, M.K.-M. and I.O.; data curation, M.K.-M. and I.O.; writing—original draft preparation, M.K.-M. and I.O.; writing—review and editing, M.K.-M. and I.O.; visualization, M.K.-M. and I.O.; supervision, M.K.-M. and I.O. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

The samples and any additional research data are available from the authors upon request.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Plantlets of tomato: in vitro stage (a), adaptation stage (b), and acclimatized plants (c).
Figure 1. Plantlets of tomato: in vitro stage (a), adaptation stage (b), and acclimatized plants (c).
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Figure 2. The weight of 1 fruit of tomato (S. pimpinellifolium) in percent compared to the control (100%). Mean values denoted by the same letter do not differ statistically significantly at 0.05 according to Tukey’s test.
Figure 2. The weight of 1 fruit of tomato (S. pimpinellifolium) in percent compared to the control (100%). Mean values denoted by the same letter do not differ statistically significantly at 0.05 according to Tukey’s test.
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Figure 3. Percentage of ripe and unripe tomato fruit depending on application of copper, chitosan, nanosilver particles, and their combinations.
Figure 3. Percentage of ripe and unripe tomato fruit depending on application of copper, chitosan, nanosilver particles, and their combinations.
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Figure 4. The yield of the fruits of tomatoes (S. pimpinellifolium) in percent compared to the control (100%). In the figure, lowercase letters indicate statistical differences between green (unripe) tomatoes, uppercase letters represent statistical differences for red (ripe) tomatoes, and italic letters denote differences for the total yield. Mean values denoted by the same letter do not differ statistically significantly at 0.05 according to Tukey’s test.
Figure 4. The yield of the fruits of tomatoes (S. pimpinellifolium) in percent compared to the control (100%). In the figure, lowercase letters indicate statistical differences between green (unripe) tomatoes, uppercase letters represent statistical differences for red (ripe) tomatoes, and italic letters denote differences for the total yield. Mean values denoted by the same letter do not differ statistically significantly at 0.05 according to Tukey’s test.
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Figure 5. Effect of different applications of copper, chitosan, nanosilver particles, and their combinations on leaf (green) and fruit (red) color of S. pimpinellifolium, using CIE L*a*b* system: a* (green/red color) and b* (yellow/blue color) (a) and L* (the lightness coefficient) (b), at end of experiment. In the figure, lowercase letters indicate statistical differences between tomatoes (red color on the figure), while uppercase letters represent statistical differences for leaves (green color on the figure). Mean values denoted by the same letter do not differ statistically significantly at 0.05 according to Tukey’s test.
Figure 5. Effect of different applications of copper, chitosan, nanosilver particles, and their combinations on leaf (green) and fruit (red) color of S. pimpinellifolium, using CIE L*a*b* system: a* (green/red color) and b* (yellow/blue color) (a) and L* (the lightness coefficient) (b), at end of experiment. In the figure, lowercase letters indicate statistical differences between tomatoes (red color on the figure), while uppercase letters represent statistical differences for leaves (green color on the figure). Mean values denoted by the same letter do not differ statistically significantly at 0.05 according to Tukey’s test.
Agronomy 14 02477 g005aAgronomy 14 02477 g005b
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Figure 6. NAI (Normalized Anthocyanin Index) and NDVI (Normalized Difference Vegetation Index) value in leaves of tomato (S. pimpinellifolium). In the figure, lowercase letters indicate statistical differences for the NAI parameter, while uppercase letters represent statistical differences for the NDVI parameter. Mean values denoted by the same letter do not differ statistically significantly at 0.05 according to Tukey’s test.
Figure 6. NAI (Normalized Anthocyanin Index) and NDVI (Normalized Difference Vegetation Index) value in leaves of tomato (S. pimpinellifolium). In the figure, lowercase letters indicate statistical differences for the NAI parameter, while uppercase letters represent statistical differences for the NDVI parameter. Mean values denoted by the same letter do not differ statistically significantly at 0.05 according to Tukey’s test.
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Figure 7. Proline and MDA contents in tomato (S. pimpinellifolium) leaves depending on the application of copper, chitosan, nanosilver particles, and their combinations (n = 32). Capital letters are for MDA small letters are for proline. Mean values denoted by the same letter do not differ statistically significantly at 0.05 according to Tukey’s test.
Figure 7. Proline and MDA contents in tomato (S. pimpinellifolium) leaves depending on the application of copper, chitosan, nanosilver particles, and their combinations (n = 32). Capital letters are for MDA small letters are for proline. Mean values denoted by the same letter do not differ statistically significantly at 0.05 according to Tukey’s test.
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Table 1. Characteristics of the tomato (S. pimpinellifolium) depending on the application of Cu, chitosan, nanosilver particles, and their combinations (n = 32).
Table 1. Characteristics of the tomato (S. pimpinellifolium) depending on the application of Cu, chitosan, nanosilver particles, and their combinations (n = 32).
Shoot Length [cm]
WeekControlCuCu+Ch Ch nAg Cu+nAg
021.821.821.321.520.220.2
I29.331.327.026.521.221.0
II37.040.535.33621.622.0
III42.346.842.041.529.631.0
IV48.352.046.345.536.638.4
V55.059.353.052.544.645.4
VI64.566.861.859.552.253.4
Mean42.6 a45.5 a40.9 a40.4 a32.3 a33.0 a
Root Length [cm]
Mean21.8 a32.3 a37.8 a33.3 a23.3 a36.3 a
In the line, mean values denoted by the same letter do not differ statistically significantly at the 0.05 level according to Tukey’s test.
Table 2. The content of macroelements and microelements in leaves (d.w.) of the tomato (S. pimpinellifolium) depending on the application of copper, chitosan, nanosilver particles, and their combinations.
Table 2. The content of macroelements and microelements in leaves (d.w.) of the tomato (S. pimpinellifolium) depending on the application of copper, chitosan, nanosilver particles, and their combinations.
N Ca Mg P K Na Fe Mn Cu Zn
g 100−1 mg 1000−1
control 4.93 c 2.11 d 0.49 d 0.47 d 3.37 a 1.35 bc 88 a 33 a 16.5 a 62 a
Cu 4.11 b 1.73 a 0.39 c 0.38 c 3.06 a 1.42 c 112 b 41 b 18.4 b 84 c
Cu+Ch 3.87 b 2.17 d 0.32 b 0.31 b 3.89 bc 1.33 b 109 b 37 ab 19.0 b 78 b
Cu+nAg 2.55 a 1.85 b 0.33 b 0.22 a 4.11 d 1.20 a 127 c 49 c 20.8 c 94 d
Ch 4.82 c 1.73 a 0.53 d 0.46 d 3.30 a 1.38 bc 90 a 35 a 16.7 a 77 b
nAg 2.34 a 1.94 c 0.27 a 0.24 a 4.06 cd 1.11 a 125 c 56 d 21.3 c 90 d
In the column, mean values denoted by the same letter do not differ statistically significantly at the 0.05 level according to Tukey’s test.
Table 3. The content of macroelements and microelements in fruits (d.w.) of the tomato (S. pimpinellifolium) depending on the application of copper, chitosan, nanosilver particles, and their combinations.
Table 3. The content of macroelements and microelements in fruits (d.w.) of the tomato (S. pimpinellifolium) depending on the application of copper, chitosan, nanosilver particles, and their combinations.
N Ca Mg P K Na Fe Mn Cu Zn
g 100−1 mg 1000−1
control 1.94 ab 0.42 d 0.24 d 0.31 d 2.11 a 1.29 a 51 a 13 a 10.5 b 45 c
Cu 1.83 a 0.32 ab 0.17 b 0.27 c 2.35 b 1.55 b 59 a 18 bc 9.6 a 40 ab
Cu+Ch2.25 c 0.40 d 0.15 b 0.21 b 2.71 c 1.52 b 69 b 16 ab 10.2 b 39 a
Cu+nAg2.46 d 0.30 a 0.12 a 0.17 a 2.93 d 1.69 c 78 b 22 c 11.8 d 48 d
Ch2.39 d 0.34 b 0.21 c 0.33 d 2.75 c 1.74 c 57 a 15 ab 11.3 c 43 bc
nAg2.07 b 0.37 c 0.11 a 0.25 c 2.88 d 1.25 a 72 b 21 c 9.7 a 46 cd
In the column, mean values denoted by the same letter do not differ statistically significantly at the 0.05 level according to Tukey’s test.
Table 4. Nutrient content and chemical composition of tomato fruit (S. pimpinellifolium) depending on the application of copper, chitosan, nanosilver particles, and their combinations.
Table 4. Nutrient content and chemical composition of tomato fruit (S. pimpinellifolium) depending on the application of copper, chitosan, nanosilver particles, and their combinations.
Dry Matter
(%) 		Soluble Solids
(%) 		Titratable Acidity
(g 100 g−1) 		Ascorbic Acid
(mg kg−1) 		β-Carotene
(mg kg−1) 		Lycopene
(mg kg−1)
control 8.3 b 8.0 c 0.33 de 217 c 9.1 cd 27.3 d
Cu 7.9 b 6.7 a 0.27 ab 145 a 9.4 d 18.7 a
Cu+Ch 9.4 e 7.2 b 0.31 cd 178 b 8.6 b 22.8 c
Ch 8.5 b 8.3 c 0.25 a 205 c 7.7 a 31.4 e
Cu+nAg 9.0 d 7.1 b 0.35 e 132 a 8.8 bc 20.5 b
nAg 7.6 a 6.7 a 0.29 bc 166 b 9.2 d 24.1 c
In the column, mean values denoted by the same letter do not differ statistically significantly at the 0.05 level according to Tukey’s test.
Table 5. The antioxidant capacity and total phenolic of the tomato fruit (S. pimpinellifolium).
Table 5. The antioxidant capacity and total phenolic of the tomato fruit (S. pimpinellifolium).
ABTS•+
(μmol T g−1) 		DPPH
(μmol T g−1) 		FRAP
(μmol T g−1) 		Total Phenolics
(mg GAE kg−1)
control124 bc 211 c 167 bc 48.5 bc
Cu 140 cd 204 c 129 a 49.7 c
Cu+Ch 151 d 175 b 204 d 45.3 a
Ch 79 a 224 c 143 a 52.4 d
Cu+nAg 115 b 156 a 185 cd 47.2 ab
nAg 82 a 160 ab 162 b 55.8 e
In the column, mean values denoted by the same letter do not differ statistically significantly at the 0.05 level according to Tukey’s test.
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Krupa-Małkiewicz, M.; Ochmian, I. Sustainable Approaches to Alleviate Heavy Metal Stress in Tomatoes: Exploring the Role of Chitosan and Nanosilver. Agronomy 2024, 14, 2477. https://doi.org/10.3390/agronomy14112477

AMA Style

Krupa-Małkiewicz M, Ochmian I. Sustainable Approaches to Alleviate Heavy Metal Stress in Tomatoes: Exploring the Role of Chitosan and Nanosilver. Agronomy. 2024; 14(11):2477. https://doi.org/10.3390/agronomy14112477

Chicago/Turabian Style

Krupa-Małkiewicz, Marcelina, and Ireneusz Ochmian. 2024. "Sustainable Approaches to Alleviate Heavy Metal Stress in Tomatoes: Exploring the Role of Chitosan and Nanosilver" Agronomy 14, no. 11: 2477. https://doi.org/10.3390/agronomy14112477

APA Style

Krupa-Małkiewicz, M., & Ochmian, I. (2024). Sustainable Approaches to Alleviate Heavy Metal Stress in Tomatoes: Exploring the Role of Chitosan and Nanosilver. Agronomy, 14(11), 2477. https://doi.org/10.3390/agronomy14112477

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