WITHDRAWN: Green Synthesis of Silver Nanoparticles and Effects on Winter Wheat and Barley Varieties

doi:10.21203/rs.3.rs-4269824/v2

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WITHDRAWN: Green Synthesis of Silver Nanoparticles and Effects on Winter Wheat and Barley Varieties

https://doi.org/10.21203/rs.3.rs-4269824/v2

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Cereals are exposed to various external conditions during the growing period, which affects their growth, development, and yield. Silver nanoparticles represent a potential solution for alleviating the negative effects of temperature stress. This study examines the impact of silver nanoparticles on extract yield, proline concentration, and antioxidant activity of winter wheat and barley during the tillering phase under winter field conditions. Silver nanoparticles (AgNPs) were synthesized using a green method with an aqueous extract of Agrimonia eupatoria L. Two varieties of winter cereals, Simonida (Triticum aestivum L.) and Nonius (Hordeum vulgare L.), were foliarly treated with concentrations of 5 mg/ml and 10 mg/ml AgNPs-H₂O. The experiment lasted for 10 days, during which the minimum temperature recorded was -7°C in field conditions. Proline concentration was higher in both varieties treated with nanoparticles compared to the controls. Antioxidant activity was assessed using the DPPH method on untreated and treated AgNPs-H₂O samples, with evaluation of the antioxidant activity of the nanoparticles themselves and ascorbic acid as a positive control. Results showed that AgNPs-H₂O increased proline concentration and antioxidant activity in both tested winter cereal varieties compared to the controls, while extract yield was higher with the application of certain concentrations. This highlights the potential of AgNPs-H₂O to improve the tolerance of winter cereals to cold and low temperatures through increased antioxidant activity.

Silver nanoparticles

green synthesis

cereals

proline

antioxidant activity

cold and low temperatures

Plants are exposed to various stresses during their growth and development, both in natural and agricultural conditions [1]. Fluctuations in temperature, whether rising or falling, influence the pace of plant development, with temperature stress disrupting cellular metabolism and functionality [2]. This stress induces alterations across multiple levels: morphological, physiological, and biochemical, depending on the species and duration of exposure [3]. Cold temperatures (<20°C) and freezing conditions (<0°C) represent one of the major abiotic stresses for plants in agriculture. The acclimatization of winter varieties begins after the temperature drops below 10°C. Yield losses induced by cold stress are characterized by a reduction in the number of productive tillers, spikes, and grains per spike, shorter stems, smaller leaf surface area, and decreased photosynthetic capacity. Winter cereals varieties, during the tillering stage, are sensitive to low temperatures, which cause a range of damages to plants such as membrane rigidification, changes in protein conformation, damage to the photosynthetic system, and excessive accumulation of various reactive oxygen molecules [4, 5, 6, 7, 8, 9]. During stressful conditions, one of the most damaging effects is oxidative stress, due to the generation of large amounts of reactive oxygen molecules, leading to damage to proteins, nucleic acids, lipid oxidation, cell membrane damage, and ultimately resulting in the inhibition of plant growth and development, and sometimes even plant death [10].

Silver nanoparticles (AgNPs) are a type of metallic nanoparticles with unique biological, chemical, and physical characteristics. Due to their exceptional catalytic activity, chemical stability, high electrical conductivity, optical and thermal properties [11], silver nanoparticles have become nanomaterials of great interest to science and have found wide-ranging applications. They are used in various fields: medicine [12, 13, 14, 15], dentistry [16], theranostics [17], air and water purification [18, 19], microbiology [20, 21], electronics industry [22], cosmetics [23], color degradation and environmental pollution prevention [24], food industry [25], and agriculture [26].

The utilization of silver nanoparticles in agriculture holds multifaceted significance, including their application as nanofertilizers [27], nano-pesticides [28, 29] nanobiosensors, nanometeorological instruments [30], improvement of soil properties [31], as well as growth stimulators and fruit ripening agents [32]. Silver nanoparticles at a specific concentration can lead to desired effects in plants [33]. Bhati-Kushwaha [34] reported that silver nanoparticles mitigate the harmful effects of cold stress in wheat. Silver nanoparticles have increased yield, antioxidant activity, and proline content in cereals under cold stress conditions [35, 36, 37]. Markarian [38] utilized ZnO nanoparticles and demonstrated their enhancement of wheat's resistance to cold stress. The same effect was achieved with gold nanoparticles in wheat seedlings under cold and low-temperature conditions [39, 40]

The synthesis of AgNPs, as well as other nanomaterials, can be physical, chemical, or biological. Biological synthesis is also referred to as green synthesis [41, 42]. Green synthesis of silver nanoparticles has advantages over chemical and physical methods. The methods used in green synthesis are environmentally and commercially acceptable, as well as simple. They do not require high energy inputs, such as high temperatures, pressures, forces, or the use of toxic chemicals [43]. Green synthesis methods are reliable, fast, and minimize adverse environmental effects [44]. Biological synthesis essentially consists of three steps: extraction, reducing agent, and the use of non-toxic materials. With the biological method, nanoparticles of specific size and shape can be obtained, which is one of the most important requirements in synthesis. Green synthesis of silver nanoparticles utilizes molecules obtained from biological systems such as plants, microorganisms, fungi, and algae [45]. Molecules obtained through extraction from biological systems such as phenols, terpenoids, amino acids, vitamins, polysaccharides, proteins, enzymes, tannins, alkaloids, and alcohol compounds are important as reducing and stabilizing agents [46]. The synthesis of silver nanoparticles using plant extracts occurs more rapidly compared to the use of microorganisms [47]. Plant-based synthesis of AgNPs is widely utilized compared to microorganism-based techniques because it is more efficient, less biocompromising, and does not require active cell cultures and their maintenance [48]. Physical methods follow a top-down synthetic approach, while chemical and biological methods, in contrast, follow a bottom-up approach [49]. Physical methods are suitable because they typically yield a large quantity of nanoparticles. However, physical methods require large amounts of energy and expensive equipment. Chemical methods carry the risk of toxic effects and environmental pollution, making them unsuitable and avoided for these reasons [50, 51, 52]. Silver nanoparticles obtained through green synthesis, unlike chemical synthesis, exhibit long-term antibacterial effects and lower phytotoxicity, thus reducing their negative impact on the environment. Molecules obtained from biological systems represent a renewable resource in the process of green synthesis. This differs from chemical synthesis, which requires the production of chemicals, often at high costs [53]. Various strategies have been used to overcome the negative effects of stress: selecting tolerant genotypes, applying different plant growth regulators, and using organic fertilizers. Species and varieties that can tolerate stress, combined with nanotechnology in agriculture, could be an effective strategy for achieving sustainable production and increasing yields during stressful conditions [54, 55]. Additionally, nanotechnology is environmentally friendly because its use reduces the effects of harmful chemicals on crops and the environment in general [56].

The aim of the research is to analyze the impact of silver nanoparticles on the antioxidant activity of winter wheat and barley varieties during winter conditions in a ten-day experiment conducted in the tillering stage at a field trial.

Chemicals

Silver nitrate (AgNO₃) was obtained from Sigma Aldrich, USA. 1,1-diphenyl-2-picrylhydrazyl (DPPH) free radicals were purchased from Tokyo Chemical Industry, Tokyo. L-ascorbic acid (C₆H₇O₆Na) was sourced from Carl Roth GmbH, Germany. Methanol was obtained from Zorka, Serbia. Ninhydrin and orthophosphoric acid were obtained from Centrohem, Serbia. Glacial acetic acid, toluene and sulfosalicylic acid were obtained from Hemos, Serbia. The prepared solutions and chemicals are of analytical grade. Solutions were prepared in methanol and distilled water.

Preparation of Plant Extract for Synthesis of Silver Nanoparticles

The preparation of a water extract of the plant A. eupatoria L. (Rosaceae family) was conducted according to the method described by Muzurovic [57]. In brief, maceration of finely chopped and dried plant material was performed using distilled water. 800 ml of distilled water was measured, and 60 g of plant material was soaked in it, then left at room temperature for 24 hours. The plant material was soaked with distilled water and filtered every 24 hours, a total of three times. The obtained filtrate was collected and then dried using a rotary evaporator (DLAB, RE 100 S) at 40°C. The dried extracts were subsequently stored at 4°C in a refrigerator.

Green Synthesis of Silver Nanoparticles

Green synthesis was performed according to the method described by Markovic [15]. AgNO₃ was used as the silver source for obtaining AgNPs. An aqueous A. eupatoria extract carried out the reduction and stabilization of silver ions, with a change in the color of the solution as confirmation of the synthesis (from light yellow to dark brown). Silver nitrate was dissolved in a concentration of 5 mM, the reaction temperature was 25°C, pH = 4, and 1% plant extract was used. The reaction was carried out on a magnetic stirrer (Magnetic stirrer MSH 300) for three hours. After the synthesis of Ag nanoparticles, the suspension was subjected to centrifugation using a centrifuge model CENTRIC 150 from the manufacturer Tehtnica, for 20 minutes at 4500 rpm. After centrifugation, the remaining material was re-suspended in distilled water. The precipitated nanoparticles were then dried in an air oven at 40°C and stored at a temperature of 4°C in a refrigerator. Data analysis was performed using OriginPro 2019b - 64-bit software. Monitoring the synthesis of Ag nanoparticles in the wavelength range of 200 to 800 nm was carried out using a PerkinElmer Lambda 365 spectrophotometer.

Characterization of the Silver Nanoparticles

The characterization of AgNPs-H₂O, including transmission electron microscopy (TEM), UV-visible spectrophotometry, and FTIR spectroscopy, was described in the scientific paper by Markovic [15].

Cereals growth conditions, treatment and sampling

Two winter cereal varieties were analyzed: wheat (T. aestivum L.), Simonida variety, and barley (H. vulgare L.), Nonius variety. The cereals were cultivated in a field trial at the Center for Small Grains, village of Sipic in Kragujevac, Serbia. The experiment was conducted during the 2023/2024 growing season for a duration of 10 days in January. Sowing was done at the end of the third decade of October. Previously, a corn crop was grown. Meteorological parameters regarding minimum and maximum temperatures and daily precipitation were obtained through daily measurements. Samples of aboveground parts of cereals in the tillering stage were collected for analysis of extract yield, proline concentration, and antioxidant activity after prior treatment with AgNPs-H₂O. The treatment was performed foliarly with concentrations of 5 mg/ml and 10 mg/ml of AgNPs-H₂O. Each variety was sown on an area of three m². Each square meter represented one concentration and one control. On the tenth day, the aboveground parts of the cereals were collected. Upon arrival at the laboratory, the plant material was left to dry at room temperature. After drying, the plant material was macerated using the method described by Muruzovic [57]. The obtained filtrate was collected and dried using a rotary evaporator (DLAB, RE 100 S) at 40°C. The dried extracts were stored at 4°C in a refrigerator.

Preparation of Extracts for Determining the Yield of Extracts from Wheat and Barley Samples

The yield of extracts was determined for 3 wheat samples and 3 barley samples. Methanol was used in the maceration process to determine the extract yield. For each sample, 5 g of dried and ground aerial parts of the plant (LSA) were used. Maceration was carried out according to the method described by Muruzovic [57].

Determination of Proline

The proline content was determined spectrophotometrically using the method of Bates [58]. The plant extract was homogenized in a porcelain mortar with a 3% solution of sulfosalicylic acid, after which the homogenate was filtered. Ninhydrin reagent and glacial acetic acid were added to the filtrate. The mixture was then incubated at 100°C for 1 hour. The reaction was stopped by transferring the tubes to ice, followed by the addition of toluene with mixing. After separating the toluene layer from the aqueous phase, the toluene layer containing proline was taken for absorbance measurement spectrophotometrically at a wavelength of 520 nm. The absorbance was measured using a UV-5100B spectrophotometer. Pure toluene was used as a blank. The proline concentration was determined from a standard curve prepared with known concentrations of proline, in the same manner as the sample. The proline concentration is expressed in µmol/g of extract. Each sample was measured in three replicates.

Determination of antioxidant activity

The determination of antioxidant activity was conducted using the DPPH method as described by Kumarasamy [59] The dry extract was dissolved in methanol (1000 μg/ml), and then a series of double dilutions was prepared. DPPH was dissolved to obtain a 40 mM solution. To each 2 ml diluted sample, 2 ml of 40 mM DPPH solution was added and left to stand in a dark place for 30 minutes at room temperature. Afterward, the absorbance was read at 517 nm using a UV-5100B spectrophotometer. A control with methanol instead of the sample was prepared in parallel. Ascorbic acid was used as the standard. All working samples and controls were tested in triplicate.

Based on the obtained results, the percentage inhibition of DPPH radicals and the IC₅₀ value were determined. The percentage of inhibition was calculated using the following equation:

% inhibition = ((A_control – A_sample) / A_control) × 100

where A_control was the absorbance of the control sample and A_sample the absorbance of the extract. The IC₅₀ value is the effective concentration at which 50% of DPPH radicals were scavenged. It was obtained from the graph of scavenging activity (%) versus concentration of samples, described in detail in Vasić [60]. The analysis of the data performed using Excel software, Version 2402 (Build 16.0.17328.20124)

The methodology for green synthesis and characterization of silver nanoparticles derived from aqueous (AgNPs-H₂O) extracts of A. eupatoria, as outlined in Marković [15], involved a comprehensive process. Briefly, the nanoparticles display an isometric morphology and a uniform size distribution (average diameter 35 ± 1 nm), as demonstrated by Transmission Electron Microscopy (TEM) and high-resolution TEM (HRTEM) analyses. The use of Scanning Transmission Microscopy (STEM) with High-Angle Annular Dark-Field (HAADF) imaging and energy dispersive spectrometry (EDS) confirms the crystalline nature of AgNPs. Fourier Transform Infrared (FTIR) analysis identifies identical functional groups in the plant extracts and their corresponding AgNPs, indicating the role of phytochemicals in the reduction of silver ions. Spectrophotometric monitoring of the synthesis process, influenced by various parameters, provides insights into the kinetics and optimal conditions for AgNP-H₂O formation.

Ten days after treating wheat and barley with AgNPs-H₂O, samples were collected, and extracts were prepared for further analysis. During the 10-day period, temperatures ranged from -7°C to +14°C (Figure 1).

Wheat samples were labeled as follows: control - WC, treatment with 5 mg/ml - W5, and treatment with 10 mg/ml - W10. Barley samples were labeled as follows: control - JC, treatment with 5 mg/ml - J5, and treatment with 10 mg/ml - J10.

Extraction of the aerial parts of plants (LSA) was performed for 3 wheat samples and 3 barley samples to determine the extract yield for each sample. After complete removal of the solvent, the extract yield was obtained in grams and percentages, as shown in Table 1.

Table 1: Extract yield in grams and percentages for wheat and barley samples

Samples	g	% w/w
WC	1.42	28.4
W5	1.39	27.8
W10	1.62	32.4
BC	1.67	33.4
B5	1.65	33
B10	1.59	31.8

The highest concentration of proline was detected in the barley extract treated with a concentration of 5 mg/ml AgNPs-H₂O (1.213 µmol/g), followed by the wheat extract treated with a concentration of 5 mg/ml AgNPs-H₂O (1.17 µmol/g). The lowest concentration was recorded in the control samples of wheat (1.074 µmol/g) and barley (1.031 µmol/g), as shown in Figure 2. Wheat and barley extracts treated with a concentration of 5 mg/ml AgNPs-H₂O had higher proline concentrations than the extracts treated with a concentration of 10 mg/ml AgNPs-H₂O. The control samples of wheat and barley had the lowest proline concentrations compared to both treatments with 5 mg/ml and 10 mg/ml AgNPs-H₂O. Overall, the concentration of proline was higher in the treated samples compared to the control samples, indicating that treatment with AgNPs-H₂O positively affects proline accumulation in wheat and barley during exposure to cold and low temperatures. The concentrations with standard deviations are presented in Table 2.

Table 2. Proline of wheat and barley samples.

values (µmol/g)
Investigated samples	Concentration of proline
WC	1.07 ± 0.007
W5	1.17 ± 0.008
W10	1.10 ± 0.007
BC	1.03 ± 0.007
B5	1.21 ± 0.004
B10	1.14 ± 0.007

The highest antioxidant activity was detected in the wheat extract treated with a concentration of 10 mg/ml AgNPs-H₂O (IC50 = 80.73 μg/ml) and the wheat extract treated with a concentration of 5 mg/ml AgNPs-H₂O (IC50 = 118.51 μg/ml). The lowest activity was detected in the barley treated with a concentration of 10 mg/ml AgNPs-H₂O (IC50 = 283.72 μg/ml). As shown in Figure 3, the extract made of wheat treated with a concentration of 10 mg/ml AgNPs-H2O improved the antioxidant activity of wheat, while the extract made of barley treated with a concentration of 5 mg/ml AgNPs-H₂O improved the antioxidant activity of barley, compared to the control samples. However, compared to the positive control (ascorbic acid IC50 = 23.91 μg/ml), the tested extracts both treated and untreated, showed limited antioxidant activity. The antioxidant activity of AgNPs-H₂O was low (Figure 3). The concentrations with standard deviations are presented in Table 3.

Table 3. Antioxidant activity of wheat and barley samples, AgNPs-H₂O and ascorbic acid.

IC50 values (µg/mL)
Investigated samples and standard	DPPH scavenging activity
WC	204.89 ± 0.14
W5	118.51 ± 0.18
W10	80.73 ± 0.68
BC	320.84 ± 0.6
B5	218.11 ± 0.09
B10	283.72 ± 0.27
AgNPs-H₂O	261.28 ± 1.30
AA	23.91 ± 0.09

The temperature, as a negative abiotic factor affecting cereals, has primarily been studied in terms of its impact on high temperatures and heat stress. However, cold and low temperatures can also adversely affect winter cereals during the tillering stage, reducing yield and growth [61]. According to Li [7], aside from low temperatures, repeated exposure to low temperatures over a specific period can also affect cereal yields. While lower concentrations of nanoparticles may stimulate antioxidant mechanisms in plants, higher concentrations can lead to oxidative stress that plants cannot overcome [62, 63]. Islam [63] evaluated the antioxidant activity in wheat and barley grass exposed to temperatures of 5-10°C and found that wheat grass had higher antioxidant activity than barley grass. Gorczyca [64] measured the antioxidant activity in the roots and leaves of wheat with and without nanoparticles, finding no significant differences from the control. During cold stress, AgNPs stimulated the germination, growth, and development of green bean seeds, with lower concentrations showing more favorable effects [65], while higher concentrations exhibited antimicrobial effects. Venzhik [39] demonstrated that gold nanoparticles at a concentration of 20 μg/ml had the most favorable effect on the survival of wheat seedlings at -3°C, increasing leaf length, chlorophyll a, and carotenoid content without accumulating MDA. Their subsequent study [40] confirmed that gold nanoparticles can increase the tolerance of wheat seedlings to low temperatures, with higher survival rates at -3°C compared to the control, though damage increased at -5°C and -7°C. Song [66] found that zinc oxide nanoparticles increased the cold resistance of rice by enhancing chlorophyll content, dry biomass, stem and root length, and antioxidant enzyme levels while reducing hydrogen peroxide, MDA, and proline levels. Similarly, TiO₂ nanoparticles at 5 mg/L reduced hydrogen peroxide content and increased photosynthetic activity in cold-tolerant chickpea [67] and increased cold stress resistance and antioxidant activity in licorice [68]. Feichtmeier [69] showed that various concentrations of gold nanoparticles did not affect barley seed germination, but higher concentrations led to phytotoxicity. Razzaq [70] reported that silver nanoparticles increased the number of roots in wheat without negatively affecting germination, with the best yield and growth at 25 ppm AgNPs, though higher concentrations had negative impacts. El-Temsah [71] found that 10 mg/L of silver nanoparticles inhibited seed germination and reduced barley shoot length. Numerous studies indicate the significance of silver nanoparticles [72, 73, 74, 75, 76, 77], with effects depending on the genotype, nanoparticle size, concentration, coating agents, application method, degree of dispersion, and phytochemical properties [78, 64]. Budhani [79] found that five different commercial silver nanoparticles negatively impacted germination, root growth, and shoot length in wheat. Our research used silver nanoparticles with an average diameter of 35 ± 1 nm Markovic [15], and different concentrations showed varying effects on germination and root elongation in corn, zucchini, and watermelon Almutairi [35]. Fayez [80] found that biologically synthesized silver nanoparticles and AgNO₃ had phytotoxic effects on barley, with the mildest effect at 0.1 mM, while higher concentrations were phytotoxic, similar to Dimkpa [81], where chemically synthesized AgNPs exhibited greater inhibitory effects on root length and fresh weight in Arabidopsis thaliana compared to Ag⁺.

Foliar treatment with silver nanoparticles at concentrations of 5 mg/ml and 10 mg/ml influenced the antioxidative activity and concentration of proline in two winter cereal varieties: Simonida (T. aestivum L.) and Nonius (H. vulgare L.) during the tillering stage under cold and low temperatures. The treated plants exhibited better antioxidative activity compared to the untreated ones. The best antioxidative activity was observed in wheat samples treated with 10 mg/ml AgNPs-H₂O, and in barley samples treated with 5 mg/ml AgNPs-H₂O, suggesting that lower concentrations of nanoparticles more effectively stimulate antioxidative mechanisms in barley. Overall, wheat samples demonstrated superior antioxidative activity compared to barley samples. The highest proline concentrations were recorded in plants treated with 5 mg/ml, both in wheat and barley, while plants treated with 10 mg/ml had lower proline concentrations. These results confirm that a lower concentration of silver nanoparticles more effectively increases proline concentration. The extract yield was highest in wheat treated with 10 mg/ml and in the control sample of barley. These results suggest that silver nanoparticles could potentially mitigate the negative impact of cold and low temperatures on cereals. Further studies need to evaluate the overall impact of AgNPs on antioxidant activity, considering factors such as nanoparticle concentration, exposure duration, and the physiological and developmental stages of the plants.

Author’s contribution: Nevena Djukic and Katarina Mladenovic conceptualized and designed the research; Djordje Minic, Nevena Djukic and Ana Kesic conducted the research experiment. Djordje Minic gathered literature, wrote the paper, and analyzed the results. Stefan Markovic, Mirjana Grujovic and Aleksandra Torbica read the paper. All authors participated in preparing the manuscript.

Conflict of interest: The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Funding declaration: This work was supported by the Ministry of Education, Science, Technological Development and Innovation of the Republic of Serbia (Agreement No. 451-03-66/2024-03/200122 and Agreement No. 451-03-65/2024-03/200122).

Disclosure of potential conflicts of interest: The authors declare that they have no known competing fnancial interests or personal relationships that could have appeared to infuence the work reported in this paper.

Research involving Human Participants and/or Animals: This research did not involve human participants or animals.

Informed Consent: This research did not involve human participants, so informed consent was not required.

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The authors declare no competing interests.

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WITHDRAWN: Green Synthesis of Silver Nanoparticles and Effects on Winter Wheat and Barley Varieties

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