Metal Nanoparticles and Abiotic Stress Tolerance

Abstract

Nanotechnology opens a large scope of novel applications in the fields of biotechnology and agricultural industries. Nanoparticles (NPs) are described as particles with at least one dimension in the 1–100 nm size range. They have unique physicochemical properties, i.e., high surface area, high reactivity, tunable pore size, and particle morphology. Abiotic stresses like drought, salinity, flooding, heat, heavy metals, etc. are major constraints that affect the growth and productivity of plants. To overcome the impact of these abiotic stresses, many strategies could be considered to support plant growth including the use of metal nanoparticles. Several metal nanoparticles (such as Zn, Fe, Ti, Ag, Mn, Cu, and Mo NPs) are being studied to assess their potential in protecting plants from abiotic stresses, improving plants, and modulating various plant processes. The present review has investigated the beneficial role of metal nanoparticles in alleviation of various abiotic stresses in some plants.

1. Introduction

Nanotechnology, the fourth wave of the industrial revolution, is one of the new technologies that is developing rapidly [1]. In the last decade, nanotechnology has been considered as an important tool to increase agricultural production. Nanotechnology has the potential to transform the agricultural industry through the development of new formulations for pesticides and fertilizers, the identification and diagnosis of plant diseases, water supply for agriculture, and soil management [2]. The agricultural industry is considered as one of the important economic pillars of developed countries. As the world’s population grows, the need for food and agricultural products is increasing. Factors such as climate change, limited soil and water resources, increased environmental pollution, and plant diseases create problems in agriculture and the production of sufficient and healthy food [3]. In general, nanotechnology can make a significant contribution to the growing prosperity of the industry by optimizing the consumption of agricultural inputs such as water, fertilizers, and pesticides and reducing effluents and pollution [4]. Nanotechnology can improve the overall use efficiency of agricultural inputs such as water, light, and chemicals. Health and functions of both soil and plant improve through microbiome enhancement and decreasing losses by managing crop disease better, which leads to less collateral damage to the environment. Therefore, nanotechnology has a promising potential to develop sustainable agriculture [5].

The environmental factors that restrict plant growth, vitality, and fertility are known as abiotic stresses. Plants are naturally exposed to a variety of abiotic stresses such as drought, salinity, heavy metals, chilling, and heat [6]. Plants as sessile organisms have numerous mechanisms to cope with changes in their growth conditions to show the necessary flexibility in responding to environmental stresses, without affecting cellular, physiological and developmental processes [7]. One of the main concerns in sustainable agriculture is increasing tolerance to abiotic stresses. Based on this, researchers have been able to take a big step in global sustainable agriculture by reducing the harmful effects of abiotic stresses [8]. When plants are exposed to abiotic stresses, reactive oxygen species (ROS) accumulate at the toxicity level in the cell. Overproduction of ROS causes the degradation of membrane lipids and proteins, cell toxicity, and reduction of plant growth. The antioxidant defense system scavenges ROS to alleviate oxidative stress [9]. In the last years, the use of nanoparticles in technology has been considered due to their properties such as small size, high surface area, higher solubility, and reactivity compared to bulk materials [10]. Metallic nanoparticles (MNPs) including Zn, Fe, Ti, Ag, Mn, Cu, and Mo NPs have earned significant attention due to their environmentally friendly implementations in the agricultural sector [11]. They have recently been used for seed germination, plant growth, and stress tolerance of a number of plants [12, 13]. The goal of this review was to better understand the stress resistance mechanisms and MNP-mediated plant tolerance increase via antioxidant activity regulation.

2. Types of nanoparticles

Nanoparticles (NPs) have dimensions between 1 and 100 nm. They have unique physical and chemical properties such as high surface vitality, large surface-to-volume ratio, and high reactivity [14]. NPs are generally classified into different groups: metal-based NPs, metalloid NPs, metal magnetic NPs, metal oxide NPs, dendrimers, and carbon-based NPs (Table 1). In the last decade, metal and metal oxide-based NPs are comprehensively studied in agriculture fields for the improvement of crop productivity and increasing the plant flexibility and tolerance under abiotic stress conditions [16]. Metal-based NPs and their oxides including nanomaterials of gold, silver, copper, aluminum, iron, titanium dioxide (TiO₂), cerium oxide (CeO₂), iron oxide (FeO), aluminum oxide (Al₂O₃), and zinc oxide (ZnO) are gaining so much attention of scientists to modulate abiotic stress [12, 13, 17].

Types of Nanoparticles	Example
Metal-based NPs	Gold, copper, aluminum, iron, silver, platinum, palladium
Metalloid NPs	Selenium, silicon, boron, arsenic, tellurium
Metal magnetic NPs	Cobalt, manganese, nickel, iron
Metal oxide NPs	Titanium dioxide, cerium oxide, iron oxide, aluminum oxide, zinc oxide, copper oxide
Dendrimers	Hybrid, tecto, micellar, chiral, liquid crystalline, triazine
Carbon-based NPs	Carbon nanotubes, carbon nanohorn, nanodiamond, fullerene, graphite, graphene, graphene oxide, carbon dot

Table 1.

Types of nanoparticles [15].

3. Effect of metal nanoparticles on antioxidant defense system improving of plants during abiotic stress exposure

Reactive oxygen species (ROS) are generated in various plant cell compartments such as plasma membranes, endoplasmic reticulum, peroxisomes, chloroplasts, mitochondria, and cell wall in natural and stress conditions [18]. ROS such as singlet oxygen (¹O₂), superoxide (O²⁻), hydrogen peroxide (H₂O₂), and hydroxyl radicals (OH^.) are accumulated in all the abiotic stresses that result in oxidative stress. Increased ROS act as a signal, and ROS scavengers are one of the defense mechanisms in plants [8]. As the level of ROS is elevated in plants in response to abiotic stress exposure, an antioxidant defense system that is capable of scavenging ROS is activated [19]. Antioxidant defense system of plants includes a number of antioxidant enzymes such as catalase (CAT), ascorbate peroxidase (APX), dehydroascorbate reductase (DHAR), guaiacol peroxidase (GPX), glutathione reductase (GR), monodehydroascorbate reductase (MDHAR), and superoxide dismutase (SOD) and non-enzyme antioxidant compounds such as proline, glycine betaein, anthocyanins, flavonoids, carotenoids, glutathione, and ascorbate [20, 21, 22]. As shown in Figure 1, MNPs enter the plant cell through penetration or transportation via specific channels in the plasma membrane. Then, as stress signaling molecules, by inducing the expression of regulatory factors in the activation of the defense system, they result in stress tolerance.

Figure 1.

Antioxidative mechanism of action of MNPs in plants under abiotic stress (NPs: Nanoparticles; MDHAR: Monodehydroascorbate reductase; SOD: Superoxide dismutase; APOX: Ascorbate peroxidase; DHAR: Dehydroascorbate reductase; GR: Glutathione reductase; ROS: Reactive oxygen species) [17].

In addition, MNPs can activate the plant defense system under stress by maintaining ROS levels to induce the ROS signaling network. MNPs treatment alters biological pathways involved in defense mechanisms by upregulation of genes that encode proteins that play a key role in ROS balance such as peroxidases (POX), NADPH oxidase, glutathione S-transferase (GST), and superoxide dismutase (SOD) [23]. MNPs upregulate the genes responsible for the activation of antioxidant enzymes. For instance, Laware and Raskar experiments on onion seedlings showed that TiO2 NPs enhanced SOD enzyme’s activity in NP-supplemented plants [24]. Also, results from transcriptomic studies showed that the expression of Cu/Zn SOD, Fe/Mn SOD, catalase, and ascorbate peroxidase in plants that were treated with ZnO NPs under drought was notably enhanced [25]. Concrete evidence provided by Thakur et al. showed that an increase in GPX and SOD activities in wheat plants treated with ZnO NPs under heat stress improved heat tolerance by further reducing H₂O₂ levels and establishing membrane stability [26]. Studies have also reported that MNPs participate in the induction of Ca²⁺-binding protein expression, resulted in stress tolerance by launching a cascade of intracellular signaling and upregulation of associated genes [27].

4. Secondary metabolites role induced by MNPs in abiotic stress tolerance

Metabolites are essential molecules for growth, adaptation to stress, and defense of a living organism. Metabolic pathways leading to the synthesis of molecules including carbohydrates, proteins, amino acids, fatty acids, and nucleotides are considered as the primary metabolism, and the compounds produced in these pathways, which are necessary for plant survival, are called primary metabolites [28]. Primary metabolites are involved in various life functions in plants, such as cell division, growth and development, photosynthesis, respiration, and reproduction [29]. Plants produce a diverse group of organic compounds called secondary metabolites that do not have a role in processes such as photosynthesis, respiration, metabolism, protein synthesis, and nutrient accumulation directly [30]. A significant number of secondary metabolites, such as terpenoids, steroids, phenolics, flavonoids, and alkaloids, by the removal of ROS in cellular stress and defense response, function as an adaptation mechanism to stress conditions [31]. Evidence has shown that secondary metabolites are involved in the non-enzymatic defense of plants against stress [32]. The MNPs are commonly found in agrochemicals such as pesticides, fungicides, herbicides, and fertilizers [33]. A few studies have demonstrated that treatment of plants with MNPs resulted in increased production of secondary metabolites, which might act as antioxidants to scavenge the ROS [34, 35]. Several studies have shown that MNPs have the potential to induce plant secondary metabolites’ production (Table 2).

MNPs	Species	Concentration	Secondary metabolite	Refs
CuNPs	Cucumis sativus	10 and 20 mg L^−1	Acetyl glucosamine, Phenyl lactate, 4-aminobutyrate	[36]
AgNPs	Artemisia annua	900 mg L^−1	Artemisinin	[37]
	Arabidopsis thaliana	0.2–25 μg mL^−1	Anthocyanin and Flavonoid	[38]
	Corylus avellana	0–10 mg L^−1	Taxol and Baccatin II	[39]
CeNPs	Solanum lycopersicum	0–500 mg kg^−1	lycopene	[40]
ZnNPs	Thymus vulgaris	100 and 150 mg L^−1	Thymol and Carvacrol	[41]
TiNPs	Salvia officinalis	0–1000 mg L^−1	Monoterpenes and Camphene	[42]
FeNPs	Hypericum perforatum	0–150 mg L^−1	Hypericin and Hyperforin	[43]

Table 2.

MNPs as an elicitor for secondary metabolites.

5. Alleviation of abiotic stress by metal-based and metal-oxide NPs application

Abiotic stresses including drought, salinity, heat, chilling, heavy metal toxicities, etc. are major obstacles to plant growth and productivity [7]. Plants adapt to and alleviate abiotic stresses by alterations in morphological, physiological, biochemical, and molecular levels. Researchers have shown that MNPs help plants to overcome abiotic stresses by their concentration-dependent impact on plant growth and development [15]. MNPs can be supplied to plants in form of seed coating, soil, or foliar application according to their mode of action. Extensive researches have elucidated the positive effects of some MNPs on some plant species under different abiotic stress conditions (Table 3). For instance, MNPs were effective in ameliorating the detrimental effects of abiotic stresses by increasing flavonoid, anthocyanin, phenolic, and photosynthetic pigment contents, upregulating the antioxidant enzymes, reducing the stress markers (MDA and H₂O₂), water balance, ion accumulation, improvement of the nutrient absorption, and the Na⁺/K⁺ ratio [17, 44, 45, 46, 47, 48, 49, 50, 51, 52, 53, 54, 55, 56, 57, 58, 59, 60].

MNPs	Characters and Size (nm)	Species	Abiotic stress	Mode of application	Morphophysiological responses	Refs
Silver NPs	Hexagonal and spherical (17–34)	Solanum melongena	Drought	Foliar spray	Upregulating the antioxidant enzymes	[17]
	Spherical (27–33)	Triticum aestivum	Salinity	Foliar spray	Upregulating the antioxidant enzymes, proline metabolism, and ion accumulation	[44]
	Cubic to rectangular (8–28)	T. aestivum	Heat	Soil application	Balanced relative water content, and improved chlorophyll content	[45]
	Spherical (~10 nm)	Phaseolus vulgaris	Chilling	Seed treatment	Increased seedling height, fresh and dry weight, and net photosynthesis	[46]
	Mono nanopowder (15)	Glycine max	Flooding	Silica sand	Improve the growth by accumulation of calnexin/calreticulin and glycoproteins	[47]
Zinc NPs	NR	Cucumis sativus	Drought	Foliar application	Reduction in ROS accumulation and lipid peroxidation, improve antioxidant defense system, nutrient absorption, and osmolytes accumulation	[48]
	Spherical and hexagonal (~20 nm)	Brassica napus	Salinity	Seed treatment	Seedling development through the biosynthesis of pigments, osmotic protection, reduction of ROS accumulation, adjustment of antioxidant enzymes, and improvement of the nutrient absorption	[49]
	Spherical (80)	wheat cultivars	Heat	Foliar spray	Increasing antioxidant enzymes activities	[50]
	Spherical (30)	Oryza Sativa	Chilling	Foliar application	Upregulation of the chilling-induced gene expression of the antioxidant system and chilling response transcription factors	[51]
	Hexagonal, square and spherical (2–64)	Leucaena leucocephala	Heavy metals	Hydroponic application	Reduced MDA content and the elevated level of antioxidant enzyme activities	[52]
Copper NPs	Crystalline powder (30–40)	Zea mays	Drought	Seed treatment	Water balance, photosynthesis pigment, ROS-scavenging enzyme activities and anthocyanin biosynthesis	[53]
	Spherical (20–50)	Lycopersicon esculentum	Salinity	Foliar application	Improving the Na^+/K^+ ratio and stimulates the plant’s antioxidant mechanism	[54]
Iron NPs	Spherical (20–40)	Dracocephalum moldavica	Salinity	Foliar application	Increasing non-enzymatic system as phenolic compounds and flavonoid content	[55]
	NR	T. aestivum	Drought	Seed treatment	increases photosynthetic pigments, proline, reduced lipid peroxidation, electrolyte leakage, and improved antioxidative defense system	[56]
	Spherical (50)	wheat cultivars	Heat	Foliar spray	Increasing antioxiodant enzymes activities, appearance of new bands in some isozymes and decreasing of lipid peroxidation product malondialdehyde	[50]
	Spherical (16)	L. esculentum	Heat	Foliar spray	enhanced photosynthesis by regulating energy dissipation, caused cooling of leaves through inducing stomatal opening	[57]
Titanium NPs	Crystalline and nearly spherical (15–25)	T. aestivum	Drought	Foliar application	Increased growth, yield, gluten, and starch content	[58]
	Spherical (16)	L. esculentum	Heat	Foliar spray	Enhanced photosynthesis by regulating energy dissipation, caused cooling of leaves through inducing stomatal opening	[57]
	Spherical-like shapes (70–90)	D. moldavica	Salinity	Hydroponic application	Positive impact on agronomically important attributes by increased antioxidant enzyme activity	[59]
Aluminum NPs	Crystalline powder (30–60)	G. max	Flooding		Upregulated the AsA/GSH pathway (ROS scavenger) and increased ribosomal proteins	[60]

Table 3.

Application of some metal NPs induce abiotic stress tolerance in different plant species.

NR: not reported.

6. Conclusion

Plant production globally is subjected to various environmental stress challenges. Today, the application of nanotechnology in various scientific fields is expanding. Recent studies have highlighted the potential applications of nanotechnology in improving plant growth and performance. MNPs due to their small size and having large surface area, as compared to their bulk chemical forms penetrate and absorb in relatively shorter period of time into plant cells. It has been found that MNPs have a multitude of beneficial effects on morphological, physiological, and biochemical characteristics of plants and enhance their tolerance under a variety of abiotic stresses. Accordingly, the application of MNPs in abiotic stress improvement has been noticed by agricultural researchers. MNPs enhance ROS level in plants that is associated with the amplification of a stress signal that can efficiently activate defense systems of them. It may be concluded that MNPs alleviate the abiotic stress-caused damage by activating the defense system in plants. In addition to, MNPs can regulate photosynthetic efficiency, water balance, nutrient absorption, and osmolytes accumulation, thereby enhancing growth and productivity of plants. However, to investigate the exact action of MNPs in improve plant stress, further research is needed at molecular and subcellular levels. Although MNPs have many advantages that deserve to be explored for alleviation of abiotic stress in plants; it must be noticed that its application without care can lead to a series of issues to the plants, animals, and finally to humankind. The toxicity level of MNPs is related to their concentration, size, number, surface activity, modification, and aggregation. Thus, ambiguities about the risk of use and fate of MNPs in plants and soil, as well as their interaction with the environment, should not be overlooked. In addition, green synthesized MNPs in comparison with chemically synthesized MNPs can be efficiently used due to the lack of limitation of use and toxicity in modulating various abiotic stresses in plants. Finally, developing a comprehensive database, an alert system, as well as international cooperation in regulation and legislation is essential for the use of this technology.