Seed Nanopriming to Mitigate Abiotic Stresses in Plants

Abstract

Abiotic stresses affect crop plants extensively during their life span, reducing productivity and threatening global food security. Stress conditions can result in failures of seed germination, uniformity, crop yield, cellular redox homeostasis, and the over-accumulation of reactive oxygen species. Seed nanopriming, pre-treating seeds with nanoparticles, is one way to overcome these limitations and successfully increase the tolerance of plants to future biotic and abiotic stress conditions. Nanopriming can play a significant role through the induction of several metabolic and physiological methods to better tolerate abiotic stresses. However, further research is needed to determine whether nanoparticles are stress promoters or stress inhibitors in plant systems. Here, we review how nanoparticle agents-based seed priming has the capacity to mitigate abiotic stresses.

1. Introduction

The stressor factors negatively affect plant growth, development, and seed yield, which are commonly connected to biochemical, physiological, and molecular variations [1]. Priming is a technique to mitigate these stresses that allows plants to deploy a stronger and speedier defense response against of them [2]. Priming induces a collection of metabolic activities in seeds and seedlings which help them to tolerate various abiotic stresses. Therefore, under subsequent stimuli, plants can show better growth biomarkers and stress tolerance when repeatedly exposed to stress [3]. Pathogens, pests, useful microorganisms, natural and synthetic compounds, nanomaterials, and the existence of abiotic stresses at mild levels can trigger a priming event [4, 5].

There have been several advancements in use of nanoparticles (NPs) for improving sustainability in agriculture, such as nanopesticides, nanofertilizers, and nanosensors [6]. NPs can optimize depending on their unique physicochemical characteristics in order to increase the growth and development of plants, and resilience to stressful conditions [7, 8]. The utilization of NPs is also being investigated as a priming agent to ensure better germination and growth of the seedling, thereby increasing plant yields and nutritional value [9, 10]. The extremely small size of NPs, their surface area, and their slow release rate aid plants in increasing nutrient uptake [11]. There are many benefits associated with nanoparticle-based priming, including change in metabolism, physiology, enzyme activity, and their interplay with phytohormones, etc. [12, 13]. Here, we summarize the potential use of seed nanopriming to mitigate abiotic stresses.

2. Nanoparticles in agriculture

Nanoparticles on the nanoscale (less than 100 nm) have the capacity to contribute to a new technology-based agricultural revolution [14]. NPs exhibit unique physicochemical properties such as high surface area-to-volume ratios and high reactivity that make them suitable for several of agriculture applications. NPs can load and deliver agrochemicals (e.g., fertilizers and pesticides) with controlled releases, biomolecules (e.g., nucleotides, proteins, activators), and monitoring plant health (e.g., sensors) [5]. Agri-nanosustainability can use NPs to stimulate plant growth, increase crop productivity, protect plants, improve soil quality, and detect pathogens and pesticide residues [15]. During the last decade, NPs have been widely used as fertilizers or metal fertilizers [16].

NPs can enter into cell by direct diffusion, endocytosis, and channel process [4]. A key factor in NP delivery could be the electrical gradient across the cell membranes [17]. The efficacies of passage are related to several properties, namely particle size, hydrophobicity, structure, charge, and shape [18]. NPs also can transfer from the cell to the tissues via the apoplastic or symplastic route in foliar/shoots or roots [19]. The entry of NPs into plant cells can facilitate via the plasmodesmata [20], aquaporins [21], ion channels [22], cuticle membrane and stomata [23], vasculature [24]. For example, gold NPs (AuNPs) can be transported through plasmodesmata [25].

Positive impacts of NPs in plants can be achieved via foliar spray, root exposure, and seed priming to improve plant performance under biotic and abiotic stress conditions [17, 18]. For example, foliar use of ZnO nanoparticles and TiO2 in sunflower can induce physiological responses and increase resistance to drought and water depletion [18, 26]. Recent research has indicated that interfacing plant seeds with NPs has positive impacts on field crops under stress [5, 27].

3. Nanoparticles as seed priming agents (seed nanopriming)

Pre-treatment of seed and plant with chemical and biological agents can enter plants to the primed state (PS), which allows deploying faster and stronger responses compared with a non-primed [28]. Seed priming is pre-treating seeds before planting the seeds for a certain period of time in salt solutions (halo-priming), water (hydro-conditioning), osmotic agents (osmo-priming), plant hormone solutions (hormonal priming), valuable microbe solutions (bio-priming), under a magnetic field (magneto-priming), and solutions containing NPs (NPs) (nanopriming) [4]. In seed priming, various biochemical changes occur in the seed that increments the germination rate, consistency of development, abdicate, and resistance of seedlings against unfavorable natural conditions [3, 29]. Seed priming results in actuating chemicals dependable for fetus advancement and mining of the bland endosperm via increased water content. In addition, seed priming can initiate biochemical reactions of cell repair, increment RNA substance, and improve DNA replication. Seed priming can increase the activity of antioxidant enzymes such as superoxide dismutase, catalase, and glutathione reductase for improving the defense system [30]. Priming increases seed yield, crop uniformity, and germination, improves performance under various environmental conditions, and helps overcome dormancy. This causes variations in seed water content, regulation of cell cycle, and alteration of seed ultrastructure. Seed priming and foliar application reduce the stress response during seed development and seedling establishment [31].

Seed nanopriming, pre-treatment of seed with NPs, is an emerging method for seed priming [27]. Nanopriming involves soaking seeds in nanosuspensions or nanoformulations, and the seeds may or may not absorb the NPs [27, 32]. NPs are mostly absorbed, but mostly remain on the seed surface as coatings [27]. Seed nanopriming can promote seed germination via organization of nanopores in the seed coat for increasing uptake of water [3, 33]. The nanoparticle introduces reactive oxygen species (ROS) to the seed, makes aquaporin genes active, alters starch degradation enzymes, and alters the metabolism of seed tissue [3]. Seed coat uptake of NPs results in the aggregation of reactive oxygen species (ROS), resulting in a chain reaction [34]. ROS localization is important for the communication between cells in endosperm, as well as for the breakdown of glycosidic links between polysaccharides [35]. Superoxide dismutase (SOD) allows the interplay between H₂O₂ and the phytohormone gibberellic acid (GA). GA activates alpha-amylase to stabilize the hydrolysis of starch into highly soluble sugars to support embryo development and ultimately seed germination and thus seedling vigor [3, 36] (Figure 1). The absorption and transfer of nanoparticles into the seed compartment is affected by the anatomy of the seed coat. Fewer parenchyma cell layers and larger intracellular voids lead to faster uptake and translocation of NPs into seed compartments, i.e., seed coat, cotyledon, and radicle [27]. There have been several studies concerned with the application of NPs (NPs) as seed pre-treatment agents, including metal-based NPs (e.g., Ag NPs, Au NPs, Cu NPs, Fe NPs, FeS2 NPs, TiO2 NPs, Zn NPs, and ZnO NPs), carbon-based NPs (e.g., fullerene and carbon nanotubes), and polymeric NPs.

Figure 1.

Seed nanopriming can regulate abiotic stress tolerance via different mechanisms. Seed nanopriming can lead to the creation of nanopores and facilitate the uptake of nanoparticles (NPs) and water. NPs can enhance the expression of aquaporin genes and change metabolism. Nanopriming increases oxidative activity and produces reactive oxygen species (ROS, e.g., superoxide radical (O₂.−), hydrogen peroxide (H₂O₂)). NPs can activate antioxidant enzymes (e.g., SOD), and the conversion of ROS to H₂O₂. Diffusion of H₂O₂ to embryo and interaction with phytohormone gibberellic acid (GA) lead to GA activating, its impact on α-amylase to stabilize starch hydrolysis to highly soluble sugars to support embryo development and ultimately seed germination and thus seedling vigor.

3.1 Polymeric nanoparticles

Natural and synthetic polymer nanoparticles are used for controlled release of fertilizers and pesticides in precision agriculture. For example, synthetic polysuccinimide polymeric NPs (PSI-NPs) were detailed to have awesome potential focusing on conveyance of anti-microbial in plants with negligible effect on soil quality. Recently, the Impacts of PSI-NPs on seed germination and seedlings of maize (Zea mays L.) demonstrate that PSI-NPs could mitigate the influence of the heavy metals stress (e.g. Cu) and phytotoxicity with the increase of antioxidant enzyme activities and storage of copper as Cu-PSI complexes [37].

Seed priming with natural chitosan nanoparticles (CSNP) increased salt tolerance in milk thistle seedlings by improving physiological mechanisms such as photosynthetic pigment synthesis, antioxidant enzyme activity, and free proline content [38]. Nanopriming of maize (Z. mays L.) seeds with chitosan NPs containing copper particles (NPCu) combined the properties of chitosan with the essentiality of Cu2+, advancing the enzymatic antioxidant reaction [39]. The result of distinctive concentrations of CSNPs appeared that adsorption of CSNPs on the surface of wheat seeds can initiate the auxin biosynthesis and increment seed germination and seedling development of wheat [40]. Seed priming of Vicia faba seeds cv. Sakha 1 study shows that the moderately low concentration of chitosan NPs improved the defense system of seeds by expanding total phenols and antioxidant enzyme activities [41].

3.2 Metallic nanoparticles

Metallic NPs (MNPs) consist of a metal core consisting of an inorganic metal or metal oxide [42]. Metallic nanomaterials in seeds can improve stress tolerance in plants. Seed nanopriming with Fe-NPs [43], TiO2-NPs [44], AgNPs [45], poly (acrylic acid)-coated cerium oxide NPs (PNC) [5], ZnO NPs [46] can induce defense responses to stressors. For example, it is demonstrated that priming seeds with PNC in cotton (Gossypium hirsutum L.) were associated with ROS, and Ca2+-related signaling pathways in salinity tolerance [5]. Similarly, nanopriming with TiO2 mitigates the salinity injury in maize via improving germination indexes, ion hemostasis, relative water content (RWC), non-enzymatic/enzymatic antioxidants as compared to non-primed [44]. Among the metal oxide NPs, zinc oxide NPs have attracted owing to unique photocatalytic and photo-oxidizing capacity against chemical and biological species the attention of many researchers [47]. For example, ZnO NPs alleviated the toxic impacts of cobalt (Co) by reducing its absorption and conferred stability to plant ultra-cellular structures and photosynthetic apparatus [46]. It has been demonstrated that nanoprimed seeds with solutions containing AgNPs can loosen seed coat cell walls and the endosperm, which in turn will induce seed germination [48].

3.3 Carbon nanoparticles

Carbon NPs (CNPs), such as single-walled carbon nanotubes (SWCNTs), multi-walled carbon nanotubes (MWCNTs), graphene (GR), and fullerenes, can stimulate a variety of positive responses owing to their unique chemical and physical properties, including accelerated growth and development, improved performance, and greater tolerance of stress [49]. It is known that CNTs can penetrate thick seed coats and support water absorption inside seeds, and may affect tomato seed germination and growth [50]. The penetration of MWCNTs into the seed coats of corn, barley, and soybean can induce the expression of genes encoding of water channel proteins [51]. MWCNTs functionalized with carboxylic acids can help to resolve seed dormancy in boreal forests by modulating lipid metabolism in cell membranes [52]. A significant increase in drought tolerance was achieved with SWCNTs at low concentrations by modifying water absorption and activating plant defense mechanisms, including up-regulating starch hydrolysis processes and reducing oxidative damage markers (e.g., H₂O₂, malondialdehyde concentrations) and electrolyte leakage [53]. A microscopic observation of seeds of Sorbus luristanica Bornm revealed seed endocarp abrasion and oxygen and moisture infiltration during MWCNT-priming [54].

The results indicate that MWCNTs enhanced tolerance of plant under Cd toxicity by active antioxidant enzymes (peroxidase (POD), superoxide dismutase (SOD), and catalase (CAT) activities) and reduced the malonaldehyde (MDA) [55]. The data presented demonstrate that sCNPs treatments can improve seed germination in plant species, including boreal forest native species, green alder, and lettuce [56, 57]. It was shown that fullerene nanopriming in wheat increments growth and productivity under salt stress [58]. Under drought stress, nanopriming of Caucasian alder seeds demonstrated that MWCNTs can be utilized to increment seed and seedling tolerance [59]. When tomato plants are subjected to salt stress, carbon nanomaterials can be added to seed by priming, modifying the bioactive compounds in the fruit and improving the antioxidant defenses. As a result, the plant may be protected from the negative effects of salinity stress [60].

Seeds treated with SWCNTs showed improved drought tolerance, and the combination of SOD, CAT, and POD activity can be responsible for improved antioxidant capacity under drought conditions [61].

4. Effects of seed nanopriming on plants

Nanopriming can improve the seed germination, stability, growth, and physiology of plant species by changing absorption, biochemical processes, antioxidants, photosynthesis [62, 63]. Various investigations demonstrate that nanoprimed seeds can better maintenance of cell balance and photosynthetic capacity [47, 62], increasing nutrient uptake and photosynthetic efficiency [59, 62], increased chlorophyll capacity and antioxidant activity, defense mechanisms (e.g., changes in osmotic pressure, stomatal movements) [64, 65]. It also removes the absorption of heavy metals (copper, cadmium, and zinc) and thus reduces toxicity [66].

Seed priming by NPs was discovered as a novel approach for regulating antioxidant enzymes in plants [67]. Plant antioxidant systems include non-enzymatic compounds and various enzymes, such as catalase (CAT), peroxidase (POX), ascorbate peroxidase (APX), superoxide dismutase (SOD), phenylalanine ammonia lyase (PAL), and glutathione. Priming of corn seeds with sodium metasilicate increased the activities of SOD, CAT, and POX under salt stress [68]. Similarly, maize seeds primed with TiO2 NPs increased SOD, CAT, and PAL activity [44]. Priming rice seeds with ZnO NPs enhances SOD and POD activity [67]. In addition, priming of Egyptian roselle (Hibiscus sabdariffa L.) seeds with Al2O3 NPs enhanced SOD, CAT, POD, and APX functions [69]. Priming of lavender (Lavandula angustifolia Mill.) by silver nanoparticles improved the performance of APX, POX, and SOD [70]. Wheat seeds primed with Si NPs increased SOD, POD, and CAT functions in cadmium stress [71]. Antioxidants produce ROS in response to environmental stressors. Antioxidant enzymes determine how ROS indirectly helps germination of nanoprimed seeds [72]. However, studies on the modulation of antioxidant enzymes by NPs priming are very few.

ROS as a by-product has a signaling role in germination and reducing seed dormancy [73]. This can occur by activating GA synthesis [74]. The accumulation of ROS such as superoxide (O2•-), hydrogen peroxide (H₂O₂), and hydroxyl radicals (OH) causes oxidative stress [73, 75]. Seeds generally receive NPs as extrinsic factors [72], and accumulation in the seed coat causes ROS production [34]. The increase of ROS in non-primed seeds is connected to the increase of abscisic acid (ABA), which caused disruption of seed dormancy and seed germination [76]. Furthermore, nanopriming increased ROS levels in plant cells, disrupted seed endosperm cell wall junctions, and promoted rapid and healthy seed germination [77]. Nanopriming can regulate ROS under normal and stress conditions, and seed nanopriming can regulate ROS production for faster seed germination. Under conditions, seeds accumulate ROS, and nanopriming can regulate ROS hemostasis via increased antioxidant activity for faster seed germination and improve plant stress tolerance [3]. Similarly, priming of maize seeds with copper NPs reduced ROS levels to drought stress [78]. Furthermore, Lathyrus odoratus seeds primed with Si-NPs reduced ROS and MDA levels under salt stress [79].

Stress and accumulation of ROS can affect membrane lipids, leading to lipid peroxidation, and loss of quality, germination, and seed viability [80, 81]. In stress conditions, an important lipid peroxidation reagent is malondialdehyde (MDA) [47, 82]. Studies have demonstrated that nanoparticle treatment by reducing lipid peroxidation stabilizes the cell membrane in various plants under abiotic stress [47], which is caused by the increased activity of antioxidant enzymes [83]. However, further research is necessary to elucidate the regulatory role of nanoparticle priming in ROS and membrane damage repair in different plants.

5. Seed nanopriming in abiotic stress mitigation

Due to the increase in pollution and climate changes, seeds are exposed to biotic and abiotic stress, which has a negative effect on their growth and development [83]. These stressors can cause physicochemical changes in various cellular levels. Stress can sense via cellular compartments such as cell wall and membrane, cytoplasm, chloroplast, mitochondria, endoplasmic reticulum, and peroxisomes [84]. In response to stress, gene transcription, transcription, translation, and post-translational modifications (PTMs) of proteins are altered, leading to the production and modification of proteins that play various roles in stress response [84].

In non-stressed conditions, the seed activates the GA signaling pathway and the transcription factors of hydrolytic enzymes by absorbing water; both processes break down the endosperm and release soluble sugar for seed growth, whereas, in stress conditions, the seed is unable to absorb water. In contrast, it activates the ABA signaling pathway, overproduces ROS, and prevents endosperm breakdown, which directly either slows down or delays seed germination [27]. In stressful conditions, nanoparticles can reduce seed ROS levels and thus seed cell damage due to increased activity of enzymes such as superoxidase dismutase, catalase [14].

5.1 Seed nanopriming under salt stress

Salinity is abiotic stress that threatens to impede plant growth and thereby affect crop yield [85]. Salinity in seeds causes osmotic and oxidative stress, which is associated with slowing down and prolonging the germination period [27]. Seed priming with Mn nanoparticles increases root length, alters the redistribution of macro-/micronutrients including Mn, Na, and Ca, and increases salt tolerance of Capsicum annuum [10]. However, under the pressure of salinity, maize seeds and Paeonia suffruticosa were enhanced germination by TiO2, vigor index, shoot and root length, seedling biomass, RWC, total phenol, antioxidant enzyme function [44, 67]. In addition, priming rapeseed with cerium oxide increased germination, water absorption, SOD, POD, α-amylase activities, total soluble sugar content, and Na+/K+ ratio while reducing accumulation of ROS and improved salt tolerance [86, 87, 88]. Additionally, lentil seeds containing iron nanochelates [89], cucumber seeds containing NPs from water treatment residues [90], and milk thistle containing NPs of chitosan [38] reduced salt stress by enhancing physiological salt stress. Latef et al. (2017) showed that priming of lupine seed with ZnO NPs increased photosynthetic pigments, total phenols, Zn and APX, POD, SOD, and CAT activities, and decreased MDA content and Na + under salt stress conditions [91]. Similarly, ZnO nanopriming improved wheat salt tolerance by activating the antioxidants to reduce oxidative explosion and increased photosynthetic electron transport efficiency and sucrose production in plants under stress [9]. Priming lettuce seeds with water-soluble carbon NPs (CNPs) increased seed germination and Chl content under salt stress [57].

5.2 Seed nanopriming in drought stress

Drought stress inhibits plant growth and reduces crop yields [92]. NP-mediated priming had a great effect on the growth of different plants to reduce drought stress. Seed priming with multi-walled carbon nanotubes increased the germination rate, root index, and root-shoot growth of alnus subcordata (Caucasian alder) under dry conditions [93]. In addition, Cape (Catharanthus roseus L.) seeds under drought stress with chitosan nanoparticles improved aggregation, membrane integrity, and plant growth [94]. In addition, corn seeds prepared with Cu nanoparticles increased RWC, Chl, and carotenoid and anthocyanin content and decreased ROS accumulation during drought stress [78]. Priming marigold seeds (Calendula officinalis L.) with silicon NPs increased quercetin, total flavonoid content, and antioxidant activity under drought stress conditions [95]. Nanozymes, Fe₃O₄ magnetite, and γ-Fe₂O₃ magnetite are magnetic nanoparticles that are effective in the development of plant growth under drought stress. For example, γ-Fe₂O₃ nanoparticles in rapeseed reduced H₂O₂ and lipid peroxidation and increased growth under drought stress. It has been reported that nanozymes reduce plant stress by removing ROS and increasing enzyme capacity [96].

5.3 Seed nanopriming in heavy metal stress

Metal toxicity is one of the abiotic stressors that disrupts plant growth. NP priming reduces the accumulation of toxic metals and adverse effects in various agricultural productions. For example, in sunflower seeds primed with green synthetic sulfur under Mn stress (Helianthus annuus L.), it activates antioxidant enzymes and reduces ROS and lipid peroxidation [97]. Under cadmium (Cd) stress, priming of zinc nanoparticles increased amylase, POD and SOD activities, and seedling growth in rice [67]. Furthermore, wheat seeds pretreated with TiO₂ enhanced germination rate, seedling growth, and water holding capacity under Cd stress. In maize seed priming with zinc oxide nanoparticles under cobalt stress, ROS and MDA decreased and plant growth, biomass and photosynthesis were improved [46]. In general, NPs reduce the adverse effects of HM by modulating plant physiological and biochemical parameters [98].

6. Conclusion

Seed nanopriming is an effective perspective that enables us to provide seeds with nanoform micronutrients at the seed level that acts as initial fertilizers for seed and increases the seed germination process, plant growth, and yield. The nanopriming can modulate molecular mechanisms affecting plant morphology, and physiological and biochemical responses. More research is necessary to test the performance of nanopriming in plants under stress conditions. In this regard, the precise cascade of molecular changes and the specific genes induced to produce such an effect remain to be further elucidated. However, several issues such as nanotoxicity on cells, tissues, and organs, as well as long-term effects of NPs exposure still need to be studied.