WITHDRAWN: The impact of silver nanoparticles on the antioxidant activity of winter wheat and barley varieties

doi:10.21203/rs.3.rs-4269824/v1

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WITHDRAWN: The impact of silver nanoparticles on the antioxidant activity of winter wheat and barley varieties

https://doi.org/10.21203/rs.3.rs-4269824/v1

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Cereals are exposed to various environmental conditions during the vegetation period, which affects their growth, development, and yield. Silver nanoparticles present a potential solution to mitigate the adverse effects of temperature stress. This study examines the impact of silver nanoparticles on the antioxidant activity of winter wheat and barley varieties during the tillering stage under winter conditions in a field trial. Silver nanoparticles were obtained through green synthesis using a water extract of the plant Agrimonia eupatoria L. Two winter cereal varieties, Simonida (Triticum aestivum L.) and Nonius (Hordeum vulgare L.), were foliar treated with concentrations of 5 mg/ml and 10 mg/ml. The experiment lasted for 10 days, during which a minimum temperature of -7°C was recorded under agricultural conditions. Antioxidant activity was assessed using the DPPH method before and after silver nanoparticle treatment, alongside evaluating the antioxidant activity of the nanoparticles themselves and ascorbic acid as a positive control. According to the obtained results, silver nanoparticles increased the antioxidant activity in both tested winter cereal varieties compared to the controls, with higher values observed in wheat compared to barley. This underscores the potential of silver nanoparticles to enhance the tolerance of winter cereals to cold and low temperatures through increased antioxidant activity.

silver nanoparticles

green synthesis

wheat

barley

tillering

cold and low temperatures

antioxidant activity

Plants are exposed to various stresses during their growth and development, both in natural and agricultural conditions (Seleiman et al., 2020). Fluctuations in temperature, whether rising or falling, influence the pace of plant development, with temperature stress disrupting cellular metabolism and functionality. (Djukic et al., 2019). This stress induces alterations across multiple levels: morphological, physiological, and biochemical, depending on the species and duration of exposure. (Desoky et al., 2020). 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. (Fowler et al., 1999; Valluru et al., 2012; Crosatti et al., 2013; Li et al., 2014; Li et al., 2015; Hussain et al., 2018). 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 (Avasthi et al., 2015).

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 (Shaikh et al., 2018), silver nanoparticles have become nanomaterials of great interest to science and have found wide-ranging applications. They are used in various fields: medicine (Asgary et al., 2016; Hernández-Arteaga et al., 2017; Saratale et al., 2017; Markovic et al., 2024), dentistry (Fernandez et al., 2017), theranostics (Sakthi et al., 2022), air and water purification (Sharma et al., 2021; Zahoor et al., 2021), microbiology (Rajkumar et al., 2019; Rozhin et al., 2021), electronics industry (Bouafia et al., 2021), cosmetics (Foteva, 2024), color degradation and environmental pollution prevention (Mehta et al., 2021), food industry (Shaikh et al., 2020), and agriculture (Panda et al., 2024).

The utilization of silver nanoparticles in agriculture holds multifaceted significance, including their application as nanofertilizers (Fatima et al., 2021), nano-pesticides (Dangi et al., 2021; Mansoor et al., 2021), nanobiosensors, nanometeorological instruments (Manna et al., 2019), improvement of soil properties (Khan et al., 2023), as well as growth stimulators and fruit ripening agents (Alghuthaymi et al., 2015). Silver nanoparticles at a specific concentration can lead to desired effects in plants (Jasrotia et al., 2018). Bhati-Kushwaha et al. (2013) 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 (Almutairi & Alharbi, 2015; Mohamed et al., 2017; Karimi & Sasan, 2017). Markarian et al. (2023) 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 (Venzhik et al., 2022a; Venzhik et al., 2022b).

The synthesis of AgNPs, as well as other nanomaterials, can be physical, chemical, or biological. Biological synthesis is also referred to as green synthesis (Sesuvium et al., 2010; Lee & Jun, 2019). 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 (Banerjee et al., 2014). Green synthesis methods are reliable, fast, and minimize adverse environmental effects (Rauwel et. al., 2015). 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 (Mustapha et al., 2022). 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 (Ahmed et al., 2016; Sudheer et al., 2022). The synthesis of silver nanoparticles using plant extracts occurs more rapidly compared to the use of microorganisms (Sharma et al., 2019). 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 (Xu et al., 2020). Physical methods follow a top-down synthetic approach, while chemical and biological methods, in contrast, follow a bottom-up approach (Silva et al., 2017). 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 (Mallick et al., 2004; Tran et al., 2013; Yaqoob et al., 2020). 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 (Zhang et al., 2021). 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 (Arif, 2020; Kumari et al., 2022). Additionally, nanotechnology is environmentally friendly because its use reduces the effects of harmful chemicals on crops and the environment in general (Ahmad et al., 2022).

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. The prepared solutions and chemicals are of analytical grade. Solutions were prepared in methanol and distilled water.

Preparation of plant extract

The preparation of a water extract of the plant A. eupatoria L. (Rosaceae family) was conducted according to the method described by (Muruzovic et al., 2023). 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.

Experiment

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 from the Republic Hydrometeorological Service of Serbia for the Kragujevac area. Samples of aboveground parts of cereals in the tillering stage were collected for analysis of antioxidant activity after prior treatment with silver nanoparticles. The treatment was performed foliarly with concentrations of 5 mg/ml and 10 mg/ml. Each variety was sown on an area of three m². Each square meter represented one concentration and one control. During the 10-day period, temperatures ranged from − 7 to + 14°C. 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 et al. (2023). 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.

Green synthesis of silver nanoparticles

Green synthesis was performed according to the method described by Markovic et al., (2024). AgNO₃ was used as the silver source for obtaining silver nanoparticles. An aqueous plant 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.

Antioxidant activity

Determination of antioxidant activity was conducted using the DPPH method as described by Kumarasamy et al. (2007). 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.

Characterization of the silver nanoparticles

Characterization of silver nanoparticles, transmission electron microscopy (TEM), UV-visible spectrophotometry, and FTIR spectroscopy were described in the scientific paper by Markovic et al. (2024).

Statistical analysis

Statistical analysis of the data was performed using Excel software, Version 2402 (Build 16.0.17328.20124).

The antioxidant activity of the samples, nanoparticles, and ascorbic acid was determined using the DPPH method, and the results are presented in Fig. 1, as the average IC50 values. The results obtained in this study indicate that both treatments with concentrations of 5 and 10 mg/ml showed higher values of antioxidant activity compared to the controls. The highest antioxidant activity was observed in the wheat sample treated with a concentration of 10 mg/ml, while in the barley samples, it was highest at a concentration of 5 mg/ml. The wheat samples generally exhibited higher antioxidant activity compared to the barley samples. Ascorbic acid showed the highest antioxidant activity compared to all tested samples.

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 have adverse effects on winter cereals during the tillering stage, reducing yield and growth (Ji et al., 2017; Choi et al., 2020). According to the study by Li et al. (2014), 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 (Pittol et al., 2017; Islam et al., 2021). A study by Islam et al. (2021), similar to ours but without silver nanoparticles, evaluated the antioxidant activity in wheat and barley grass exposed to temperatures of 5–10°C. The obtained values showed that wheat grass has higher antioxidant activity than barley grass. In the study by Gorczyca et al. (2015), cold stress was not applied, and the antioxidant activity in the roots and leaves of wheat with and without nanoparticles was measured. Antioxidant activity was assessed using the enzymes catalase and superoxide dismutase, and it was found that the values of treated plants did not differ from the control. During cold stress, silver nanoparticles stimulated the germination, growth, and development of green bean seeds, with lower concentrations showing more favorable effects (Prażak et al., 2020). In contrast, higher concentrations that exhibited antimicrobial effects were observed. The study by Venzhik et al. (2022a) demonstrated that gold nanoparticles at a concentration of 20 µg/ml^− 1 had the most favorable effect on the survival of wheat seedlings at a temperature of -3°C. Additionally, an increase in the average length of leaves, chlorophyll a and carotenoid content was recorded, but there was no accumulation of MDA. Although the antioxidant activity increased, it did not differ significantly compared to the control and treated plants. Their subsequent study, Venzhik et al. (2022b), confirmed that gold nanoparticles can increase the tolerance of wheat seedlings to low temperatures. The seedlings were exposed to temperatures of -3°C and showed the highest survival rate compared to the control. As the temperature increased to -5°C and − 7°C, damage increased while the survival rate decreased. Zinc oxide nanoparticles, according to Song et al. (2021), increased the cold resistance of rice. Treatment with zinc oxide nanoparticles increased chlorophyll content, dry biomass, stem and root length. Additionally, lower levels of hydrogen peroxide, malondialdehyde (MDA), and proline were recorded, while the levels of antioxidant enzymes, including superoxide dismutase, catalase, and peroxidase, were increased compared to the control. TiO₂ nanoparticles, under cold stress (4°C) at a concentration of 5 mg/L, reduced the hydrogen peroxide content and increased the photosynthetic activity in cold-tolerant chickpea compared to the cold-sensitive variety (Hasanpour et al. 2015). Similar results were presented by Ghabel et al. (2020) under cold stress (4°C) using TiO₂ nanoparticles with licorice (Glycyrrhiza glabra L.) as the studied plant. Treatments with concentrations of 2 and 5 ppm TiO₂ nanoparticles increased cold stress resistance along with increased antioxidant activity, fresh and dry weight, and water content. The increase in these parameters was accompanied by an increase in nanoparticle concentration. The study by Feichtmeier et al. (2015) showed that exposing barley seeds to various concentrations of gold nanoparticles did not affect germination. However, increasing the concentration led to phytotoxicity, characterized by yellow and necrotic leaves, and the roots became brownish in color. According to the study by Razzaq et al. (2016), silver nanoparticles did not have a negative effect on germination but influenced an increase in the number of roots in wheat. They emphasized that higher concentrations and prolonged exposure had a negative impact. The best effect on yield and growth was achieved with a concentration of 25 ppm AgNPs. A concentration of 10 mg/L of silver nanoparticles inhibited seed germination and reduced barley shoot length (El-Temsah et al., 2012). Numerous literature data on silver nanoparticles indicate their significance (Ijaz et al., 2020; Bhatt et al., 2021; Mughal et al., 2021; Shaikh et al., 2021; Khalid et al., 2022; El-Saadony et al., 2022). The effect exerted by nanoparticles depends on the genotype of the organism under investigation, nanoparticle size, concentration, coating agents, application method, degree of dispersion, and phytochemical properties of the nanoparticles (Yan et al., 2019; Prażak et al., 2020). The study by Budhani et al. (2019) on silver nanoparticles revealed that five different commercial silver nanoparticles had a negative impact on germination, root growth, and shoot length in wheat, regardless of their size and type of coating. In our research, silver nanoparticles with an average diameter of 35 ± 1 nm, as reported in the study by Markovic et al., (2024), were used. Different concentrations of silver nanoparticles showed varying effects on germination and root elongation in corn, zucchini, and watermelon (Almutairi et al., 2015). Fayez et al. (2017) investigated the phytotoxicity of silver nanoparticles obtained through biological synthesis and silver in the form of AgNO₃ on the germination, root growth, and shoot length of barley. All concentrations of AgNO₃ exhibited phytotoxic effects, especially on the roots, with the mildest effect observed at a concentration of 0.1 mM. The application of silver nanoparticles at only 0.1 mM concentration was better than the control, while higher concentrations acted phytotoxically. Similar results were reported by Dimkpa et al. (2013). However, chemically synthesized AgNPs exhibited a greater inhibitory effect on root length and fresh weight in Arabidopsis thaliana compared to Ag⁺.

The foliar treatment with silver nanoparticles at concentrations of 5 mg/ml and 10 mg/ml demonstrated an influence on the antioxidative activity in two winter cereal varieties: Simonida (T. aestivum L.) and Nonius (H. vulgare L.) during the tillering stage under cold and low temperatures. It was determined that the antioxidative activity exhibited higher values in the plants treated with silver nanoparticles compared to the untreated ones. The antioxidative activity was highest in the wheat sample treated with a concentration of 10 mg/ml, while in the barley samples, it was highest at a concentration of 5 mg/ml, indicating that lower concentrations of nanoparticles more effectively stimulate antioxidative mechanisms in barley. Overall, wheat samples demonstrated superior antioxidative activity compared to barley samples. Based on the obtained results, silver nanoparticles could have potential applications in alleviating the negative impact of cold and low temperatures on cereals.

Acknowledgment This work was supported by the Ministry of 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).

Author’s contribution N.Dj. and K.M. conceptualized and designed the research; Dj.M., N.Dj. and A.K. conducted the research experiment. DjM. Dj.M. gathered literature, wrote the paper, and analyzed the results. S.M., M.G. and A.T. read the paper. All authors participated in preparing the manuscript.

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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.

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WITHDRAWN: The impact of silver nanoparticles on the antioxidant activity of winter wheat and barley varieties

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