INTRODUCTION

During the life cycle, plants encounter various abiotic stress factors (drought, salinity, low and high temperatures, heavy metals, etc.) that constrain the geographical distribution of species and reduce plant productivity. Under conditions of global climate changes and increasing anthropogenic pressure, the additional load is exerted on biocenoses. Plants represent the most vulnerable components of biocenoses due to their sessile lifestyle. In the course of evolution, plants have evolved several defense systems that ensure their resistance to stresses. A multicomponent antioxidant system (AOS) is one of the protective mechanisms. It acts as a universal shield against oxidative stress that is a constituent part of any abiotic treatment [1, 2]. The effective operation of AOS is especially important for photosynthetic organisms since chloroplasts are the major source of reactive oxygen species (ROS), such as superoxide anion radical (\({\text{O}}_{2}^{{\bullet - }}\)), hydroxyl radical (•OH), hydrogen peroxide (H2O2), and other interconvertible oxygen species [3–5]. Under optimal growth conditions, ROS generation is an indispensable part of plant metabolism. However, under the action of abiotic stress factors, the intracellular ROS level can increase dramatically and lead to oxidative stress development, which intensifies lipid peroxidation (LPO); injures the organelles, membranes, and nucleic acids; results in protein denaturation, etc. [5, 6]. Therefore, investigating the regulatory mechanisms of AOS operation, possibilities of AOS additional stimulation, and the maintenance of plant stress resistance in constantly changing environments is an urgent biological issue.

The powerful development of nanotechnology has led to the emergence of a wide diversity of nanomaterials in people’s lives. On the one hand, small sizes (up to 100 nm), high reactivity, and unique physicochemical, optical, and electrical properties [7, 8] imply certain risks from the interaction of nanoparticles (NPs) with living organisms. On the other hand, the materials based on NPs are already widely used in agriculture as nanofertilizers, regulators of plant growth and development, and substances with pesticidal and herbicidal activity [7, 9]. In this connection, the prospects for further introduction of nanomaterials in biological sciences and agriculture are of particular interest.

The NPs of metals and their oxides can affect various aspects of plant metabolism at all levels of system organization. By penetrating into plants, the NPs modulate plant metabolism, enhance or inhibit growth processes and photosynthesis, and affect water relations, the antioxidant system, the cell ultrastructure, and gene expression [7, 8, 10–12]. It seems warranted to conduct comprehensive studies that will not only uncover basic effects of NPs on plant organisms but will also reveal NP’s role in stress responses of plants to the action of various abiotic factors. The contribution of NPs to oxidative stress development and the effects of NPs on AOS as the main nonspecific plant-defense system are not yet entirely clear because numerous experimental data available in the literature are often contradictory. The aim of this analytical review is to systematize recent data on the participation of the widely applied metal NPs and their oxides in the regulation of pro-/antioxidant balance in higher plants.

INFLUENCE OF METAL AND METAL OXIDE NANOPARTICLES ON PRO-/ANTIOXIDANT BALANCE IN PLANTS

The ingress and distribution of NPs in plant cells and tissues, as well as the effects of NPs on plant organisms, are known to depend on a number of factors, such as the type, size, and zeta potential of NPs; the NP dose (concentration of colloidal solutions); plant species; the treatment procedure [13, 14]. We have analyzed data on the influence of NPs on the pro-/antioxidant balance of higher plants by taking into account the type of NPs, the concentration of applied agents, and the specifics of plant materials (Table 1). The analysis revealed that nanoparticles made of silver (Ag NPs), gold (Au NPs), and from oxides of cerium (CeO2 NPs), copper (CuO NPs), iron (Fe2O3 and Fe3O4 NPs), titanium (TiO2 NPs), and zinc (ZnO NPs) are the most widely used NPs in experiments with plants. The majority of researchers noted that almost all of these NPs caused oxidative stress, thus enhancing the generation and accumulation of ROS and LPO products in plant tissues [15–43]. This type of effects occurred irrespective of NP concentrations in solutions and were observed in a wide range of plant materials (Table 1). For example, the treatment of Vicia narbonensis seeds with TiO2 NPs elevated the H2O2 content in leaves [38], while the addition of ZnO NPs to nutrient solutions stimulated the accumulation of malondialdehyde (MDA), the end product of LPO in wheat leaves [43]. It should be noted that Au NPs applied at low concentrations (≤25 mg/L) caused the opposite effect, i.e., they reduced the content of ROS and LPO products [22, 44, 45].

Table 1. Participation of metal and metal oxide nanoparticles in regulation of pro-/antioxidant balance in plants
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However, NPs of metals and their oxides not only induce the development of oxidative stress but can also affect the plant AOS [17, 19, 21, 23, 24, 27, 31, 33, 36–38, 42–55] (Table 1). Under the influence of Ag NPs on Spirodela polyrhiza and potato plants [17, 19], the activity of antioxidant enzymes was found to increase in parallel with an advancement of oxidative stress. Similar results were observed with Au NPs in mustard and watermelon plants [23, 24], with CeO2 NPs in maize [27], and in other studies (Table 2). The decrease in activity of AOS enzymes was observed under the influence of Ag NPs, ZnO NPs, and Fe3O4 NPs [42, 56, 57]. It can be stated that, in the absence of additional stress factors, all examined NPs of metals and their oxides mediate both processes: on the one hand, they cause oxidative stress and, on the other hand, they elevate the activity of AOS enzymes (Table 1). In some cases, the action of NPs on these processes was clearly concentration dependent. For example, low concentrations of CuO NPs (10–50 mg/L) stimulated the activity of AOS enzymes, while high concentrations (100–1000 mg/L) led to the development of oxidative stress in rice [36]. Similar effects were found in Oenothera biennis under the influence of Fe2O3 NPs [37].

Table 2. Effects of metal and metal oxide nanoparticles on the pro-/antioxidant balance of plants under the action of abiotic factors
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It should be noted that some NPs of metals and their oxides stimulated the accumulation of low-molecular-weight antioxidants in plant tissues (Table 1). For example, the treatment with Ag NPs led to a significant increase in the proline content in wheat [21] and glutathione content in Spirodela polyrhiza [17], while ROS accumulation in leaves was enhanced in both studies.

There is evidence in the literature that NPs of metals and their oxides affect the expression of genes encoding various AOS components (Table 1). For example, Ag NPs promoted the level of gene transcripts involved in synthesis of superoxide dismutase, catalase, and ascorbate peroxidase in Arabidopsis thaliana and rice [18, 58], while CeO2 NPs altered the expression of genes encoding glutathione synthetase [28]. Similar effects were found under the influence of Au NPs [45] and Ti NPs [59].

Our analysis convincingly demonstrates that, under optimal growth conditions, NPs of metals and their oxides promote the accumulation of ROS and LPO products due to enhanced oxidative processes in plant tissues, but they elevate the activity of AOS at the same time by affecting the AOS enzymatic component and the content of low-molecular-weight antioxidants. Such a dual effect of NPs on the pro-/antioxidant balance of plants makes it difficult to clarify possible mechanisms of their action and the forthcoming utility of nanomaterials in biology. Therefore, the effects of NPs of metals and their oxides on oxidative processes and the pro-/antioxidant balance of plants under the action of abiotic stress factors are of great interest.

We have analyzed data on the role of metal NPs and their oxides in the regulation of oxidative stress in plants caused by the action of abiotic stress factors, such as low temperatures [51, 60, 61], salinity [62–69], drought [55, 70–75], and heavy metals [41, 76–87]. Data in Table 2 show the effects of metal NPs and their oxides on plants exposed to abiotic stress factors, as compared to the action of the same stress factors without the NP treatment. As can be seen, the plants treated with NPs were characterized by a higher stress resistance to abiotic factors compared to that of the control plant group untreated with NPs. The observed increase in plant stress resistance was associated in most cases with the prevention of oxidative stress development and the increased antioxidant protection (Table 2). For example, in chickpea plants treated with TiO2 NPs and subjected to subsequent cooling, the activities of catalase, ascorbate peroxidase, and guaiacol peroxidase increased, while the leaf content of MDA and H2O2 decreased compared to untreated plants under the same conditions [51]. In rice seedlings treated with ZnO NPs and exposed to low temperatures, the content of MDA and H2O2 in tissues was found to decrease on the background of the increased activities of superoxide dismutase and catalase and the altered content of the transcripts of genes encoding these enzymes [61]. Under the influence of Au NPs at increased salinity, the rate of ROS generation in wheat leaves was diminished along with the increased activity of AOS enzymes and the accumulation of proline content [62]. The treatment of rice plant roots with nanocomposites containing Au NPs reduced the toxic effect of cadmium, preventing its absorption by root cells and reducing the risk of oxidative stress [76, 77]. The treatment of sunflower, soybean, rice, and wheat plants with Fe-, Ti-, and Zn NPs and their oxides alleviated the oxidative stress caused by the action of heavy metals [78–86].

The above data suggest the possibility of using various NPs of metals and their oxides as adaptogens that enhance plant resistance to abiotic stress factors, the action of which is usually accompanied by the increased generation of ROS and, consequently, by the development of oxidative stress. The mechanisms of NP action on plants are actively discussed, but they remain largely hypothetical.

MECHANISMS OF ACTION OF METAL AND METAL OXIDE NANOPARTICLES ON OXIDATIVE PROCESSES IN PLANTS

The possible ways by which NPs of metals and their oxides affect the development and regulation of oxidative stress in plants are summarized in Fig. 1. Under optimal conditions, NPs were found to be able, on the one hand, to promote oxidative stress and, on the other hand, to control it by influencing AOS components. Let us consider some aspects of these processes.

Fig. 1.
figure 1

Mechanisms of action of metal and metal oxide nanoparticles on the development and regulation of oxidative stress in plants.

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First of all, the enhancement of ROS generation and the subsequent development of oxidative stress under the influence of NPs of metals and their oxides is a typical response of a plant organism to the intrusion of an alien chemical [88, 89]. Metal ions can be released from NPs and directly damage cells and their structural components, thereby enhancing ROS formation. In addition, NPs can come into contact with biomolecules, such as proteins and lipids, thus forming new biochemical complexes with high chemical activity [88, 89]. Within these complexes, the relatively stable free radical intermediates involved in ROS initiation are possibly formed. It is the high chemical activity of NPs that causes the enhanced generation of ROS, including such highly reactive forms as \({\text{O}}_{2}^{{\bullet - }}\) and •OH, which promote the development of oxidative stress in plant cells either directly or via the activation of enzymatic processes [88, 90].

In addition, the ability of NPs of metals and their oxides to trigger classical stress-signaling responses, such as the Ca2+-associated signaling pathway is being actively discussed in the literature. For example, the Ag NPs elevated the cytosolic Ca2+ level [20] and interacted directly with Ca2+-binding proteins, thus enhancing ROS signaling [90]. At the same time, the Co- and Fe NPs affected the transcript levels of genes encoding the Ca2+-binding proteins [90]. There is evidence that some NPs induced the synthesis of stress-signaling NO molecule [91, 92] that triggers a cascade of defense reactions in the organism [93]. It is supposed that NPs can mimic signaling molecules by binding to proteins and triggering various processes in cells, including ROS generation [90].

It should be noted that signaling functions of ROS and LPO products are quite important and are implemented through regulation of calcium status, hormonal signaling, and the redox-signaling systems as well as through the transcription factors and expression regulators of some chloroplast and nuclear genes [4]. It is ROS that act as a kind of “gauge” of the stress load and switch on the operation of AOS at a certain moment [3, 4]. Therefore, the NPs of metals and their oxides act as the triggers of oxidative stress and, at the same time, enhance the antioxidant defense of plants (Fig. 1).

Table 3 lists the means by which the NPs of metals and their oxides affect the development and regulation of oxidative stress under optimal growth conditions and under the action of abiotic stress factors. Under optimal conditions, the NPs promoted oxidative stress in most cases with a few exceptions. However, under the action of abiotic stress factors, the presence of NPs diminished the risk of oxidative stress. At the same time, the NPs of metals and their oxides stimulated AOS activity under both optimal and unfavorable (stress) conditions (Table 3). It should be pointed out that Table 3 is schematic, and the effects marked by arrows were noted in many works though not always. Once again, we emphasize that the effects of NPs depend on a number of parameters, including the type, size, and concentration of NPs in the colloidal solution, as well as on the plant materials and experimental conditions.

Table 3. Effects of metal and metal oxide nanoparticles on regulation of pro-/antioxidant balance under optimal conditions and under abiotic stresses
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A reasonable question arises as to how the NPs reduce the risks of oxidative stress development and increase the plant’s stress resistance under the action of abiotic stress factors. Is it only through the signaling functions of ROS and LPO products that NPs regulate the plant AOS under the action of stressors?

Many NPs of metals and their oxides are characterized by the phenomenon of surface plasmon resonance [94]. The essence of the phenomenon is that, due to the high surface area to volume ratio of the particle, the activity of electrons in nanoparticles increases manifold under the influence of light of certain wavelengths [94]. It is this effect that underlies the ability of NPs to regulate the rate of photosynthesis as the main source of ROS. For example, it was hypothesized that the NPs are able to “trap” light quanta and facilitate energy transfer within the light-harvesting complex (LHC) [95]. At the same time, the presence of NPs was reported to increase the rate of electron transport, promote the Hill reaction, and modify the parameters of chlorophyll fluorescence [95].

The effect of surface plasmon resonance is apparently related to catalytic properties of NPs [14, 96]. This term was first used in 2004 for gold nanoclusters exhibiting the properties of ribonuclease [97]. The CeO2 NPs were ascribed as the first nanoenzyme having antioxidant activity because these NPs neutralized \({\text{O}}_{2}^{{\bullet - }}\) during rapid interconversions between Ce3+ and Ce4+ and were able to decompose H2O2 [98]. Similar antioxidant properties were noted for Au NPs [99, 100], Co oxide NPs [101], and Fe oxide NPs [102]. For example, Gao et al. [102] described the peroxidase-like activity of Fe3O4 nanoparticles that were capable of reacting with H2O2 and converting it into hydroxyl radicals (Fenton reaction). The catalytic activity of Fe3O4 NPs was shown to enhance with the decrease in particle size and was most pronounced in acidic media (at pH 4.8) [14, 98, 102]. Of particular importance was the ability of metal atoms in the composition of NPs to quickly change the degree of oxidation due to the high mobility of electrons [96]. The extent of the catalytic activity of NPs depended on the NP type, shape, size, concentration, and the exposure duration. Since the activity of NPs as “nanoenzymes” can increase under stress conditions, these NPs usually diminished the risk of oxidative damage in plants under the action of abiotic stresses.

Some authors adhere to the view that NPs act as inducers of nonspecific (universal) defense mechanisms by activating genes encoding protein kinases or enzymes producing antioxidants, osmolytes, and other molecules with protective properties [103]. For example, Ag NPs were found to control the expression of genes encoding anion carrier proteins and the enzymes involved in proteolytic processes [104]; they also modified the expression of genes encoding aquaporins [58]. Many NPs were shown to be involved in the induction of Ca2+-dependent signaling pathways [20, 90, 91]. By promoting the induction of stress-signaling pathways, NPs “turn on” the genes associated with these pathways, thus increasing the stress resistance of plants [91]. There is evidence in the literature that Ag NPs regulated the expression of genes involved in the stress response to salinity [104] and drought [105], whereas ZnO NPs changed the expression of cold response genes [61]. The influence of many NPs on the expression of genes encoding the synthesis of osmolytes and AOS enzymes was demonstrated [18, 28, 45, 58, 59]. It should be pointed out that many NPs, such as Cu, Fe, Ni, Mn, Si, Co, Se, and Zn, can activate the enzymes and proteins, while ions released from the NPs can replace metals in some enzymes [106]. For example, Mn2+ ions effectively activated chloroplast RNA polymerase, phosphoenolpyruvate (PEP) carboxykinase, and manganese superoxide dismutase [107], while Zn- and Se NPs stimulated the activity of Na+/K+-ATPase and Ca2+/Mg2+-ATPase in plants under abiotic stress conditions [87].

Moreover, it was found that NPs affected the expression level of a number of miRNAs. For example, Au NPs modified the expression of miR398, miR408, miR164, miR167, and miR169 in A. thaliana plants grown under optimal conditions. At the same time, the expression of miR398 was associated with the function of genes that regulated seed germination and plant growth by influencing the auxin-signaling pathways. Changes in the expression of miR169, miR368, and miR408 affected the size of seedlings and the development of their root system; these changes also accounted for early flowering of plants and accelerated seed maturation [48].

The influence of NPs on the expression of genes encoding proteins of the photosynthetic apparatus (PSA) was also reported. For example, TiO2 NPs changed the expression of genes involved in the synthesis of Rubisco [108] and encoding the proteins of the light-harvesting complex [94, 109], while ZnO NPs changed the expression of genes encoding proteins of chlorophyll synthesis [40]. Considering the above facts, it can be supposed that NPs are able to “reprogram” plant development by enhancing or inhibiting the expression of genes and miRNAs involved in the regulation of growth and development, photosynthesis, antioxidant status, and stress response.

Thus, NPs of metals and their oxides act as stress-signaling molecules by “switching on” the molecular mechanisms of adaptive processes that remain largely unretrieved under normal conditions [89, 110]. Under the influence of abiotic stress factors, the program launched by NPs can overlap with the program of plant adaptation to a particular stressor, and this superposition may cause additional adaptive effects. We examined the influence of Au NPs on winter wheat plants exposed to low temperatures and found that nanoparticles enhanced the program of cold adaptation by inhibiting growth processes as well as by maintaining photosynthetic activity and favoring the accumulation of soluble sugars that perform numerous protective functions [110]. Mohammadi et al. [51] studied the effect of TiO2 NPs on chickpea plants under cooling conditions and concluded that NPs turn on “the confrontation metabolism” that additionally promoted the stress response induction in plants. It should be noted that a number of review studies convincingly show the role of many NPs as adaptogens that enhance plant resistance to various abiotic factors [14, 90, 91, 94, 105]. The ability of NPs to act as detoxifiers of ROS, inducers of AOS, and regulators of photosynthetic apparatus activity plays a decisive role in this process [14, 91].

CONCLUSIONS

Analysis of the literature published in recent years implies a dual role of NPs of metals and their oxides in the control of pro-/antioxidant balance: on the one hand NPs increased the generation of ROS, thus intensifying oxidative processes in plant cells and tissues; on the other hand, they regulated the rate of oxidative reactions by activating AOS components. It is important that, under the influence of abiotic stress factors, NPs acted as adaptogens, thereby enhancing the antioxidant defense of plants. Although a number of studies have shown the positive effect of many NPs on agricultural objects, the wide use of nanoparticles in agrobiology is limited, because the effects of NPs may vary depending on a number of factors (type, size, charge, and dose of NPs; the method of plant treatment and duration of exposure; the properties of plant materials; and other relevant conditions). This variability elevates the environmental risks of NP application. Further studies of NPs are needed in order to develop clear recommendations for their use not only as inducers of plant growth and development but also as antistress adaptogens. For this purpose, it is important to pursue studying the action mechanisms of NPs and the factors that determine their effects on plants. It should be emphasized that the mechanisms of NP action on plants are being investigated, but they still remain hypothetical. The study on the prospects of genetic “reprogramming” of plants under the influence of NPs can become one of the promising areas in modern experimental biology. An important aspect should be research on the accumulation of different types of NPs in the plant organism and their possible translocation along food chains. Such investigations are necessary to assess the toxicological risks from the use of NPs as adaptogens in biology and agriculture.