Abstract
Main conclusion
Advances in nanotechnology make it an important tool for improving agricultural production. Strong evidence supports the role of nanomaterials as nutrients or nanocarriers for the controlled release of fertilizers to improve plant growth. Scientific research shows that nanotechnology applied in plant sciences is smart technology.
Abstract
Excessive application of mineral fertilizers has produced a harmful impact on the ecosystem. Furthermore, the projected increase in the human population by 2050 has led to the search for alternatives to ensure food security. Nanotechnology is a promising strategy to enhance crop productivity while minimizing fertilizer inputs. Nanofertilizers can contribute to the slow and sustainable release of nutrients to improve the efficiency of nutrient use in plants. Nanomaterial properties (i.e., size, morphology and charge) and plant physiology are crucial factors that influence the impact on plant growth. An important body of scientific research highlights the role of carbon nanomaterials, metal nanoparticles and metal oxide nanoparticles to improve plant development through the modulation of physiological and metabolic processes. Modulating nutrient concentrations, photosynthesis processes and antioxidant enzyme activities have led to increases in shoot length, root development, photosynthetic pigments and fruit yield. In parallel, nanocarriers (nanoclays, nanoparticles of hydroxyapatite, mesoporous silica and chitosan) have been shown to be an important tool for the controlled and sustainable release of conventional fertilizers to improve plant nutrition; however, the technical advances in nanofertilizers need to be accompanied by modernization of the regulations and legal frameworks to allow wider commercialization of these elements. Nanofertilizers are a promising strategy to improve plant development and nutrition, but their application in sustainable agriculture remains a great challenge. The present review summarizes the current advance of research into nanofertilizers, and their future prospects.
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Introduction
Plant and agriculture biotechnology faces important challenges to mitigate the current problems derived from the need to improve food supply, and from the adverse effects of climate change on crop production (Moshelion and Altman 2015; Tyczewska et al. 2018). Unfortunately, the intensive application of chemical fertilizers has led to serious environmental problems such as pollution, salinization and loss of soil biological health (Tyczewska et al. 2018). The low nutrient efficiency of conventional fertilizers, combined with global challenges like the scarcity of water and the limited land available for farming, are the major problems facing agriculture (Shah and Wu 2019). These problems are intensified by the exponential growth rate of the world’s population, projected to exceed 9.7 billion people by 2050 (United Nations 2017). In this context, nanotechnology applied in plant sciences is a promising strategy to increase crop yields and mitigate environmental disruption. The inefficient use of resources and energy, associated with the overuse of conventional fertilizers and synthetic plant growth inducers, can be resolved using nanotechnology in plant growth management (Parisi et al. 2015). Nanotechnology science is defined by the US Environmental Protection Agency in ISO/TS 27687: 2008. The European Union defines nanomaterials (NMs) as “material containing particles in an unbound state, agglomerate or aggregate, where 50% or more of the particles are in the range of 1–100 nm” (Off. J. European Union. L 275/38 (Nov. 20, 2011).
The application of nanotechnology in plant science systems is defined as “Phytonanotechnology” (Wang et al. 2016a; Fincheira et al. 2019). Great emphasis has been placed on NMs due to their efficiency in modulating plant growth during seed germination, seedling and mature plant stages (Kamle et al. 2020). NMs are an efficient tool due to their chemical, thermal and physical properties (surface composition, density of sites and reactivity), which trigger a better plant response than do conventional fertilizers (Mukhopadhyay 2014). These particles constitute a smart technology focused on improving nutrient use efficiency and controlled release, minimizing losses in the ecosystem (Solanki et al. 2015). The application of NMs in plants can improve the target-specific delivery and time-controlled release of nutrients to modulate their physiological and metabolic responses. Furthermore, NMs are characterized by their low-cost formulation, biodegradability, low toxicity and greater activity, allowing large-scale production for application in agriculture (Aslani et al. 2014; Kalia et al. 2020). Therefore, NMs contribute to the efficiency of crop management by modulating nutrient delivery and plant system growth, improving sustainable agricultural production (Duhan et al. 2017; Shang et al. 2019). Specifically, nanofertilizers (NFs) are NMs that can serve either directly as nutrients or as carriers of conventional fertilizers to enhance nutrient utilization (Ditta and Arshad 2016).
Despite these advances and numerous studies of the contribution of nanotechnology to improving plant growth and development, most of these products with potential for use in agriculture have not yet reached the global market, and only a few products have been commercialized (Parisi et al. 2015). In this context, we have collected current information on advances in knowledge about the role of promising NFs as nutrients and carriers to improve plant growth and crop productivity. Here we offer an overview of (1) principal techniques for NM characterization, (2) exposure route and transportation of NM into plant tissue, (3) recent advances in NFs to induce plant growth, (4) knowledge of the principal nanocarriers used for the controlled release of conventional fertilizers; and (5) we discuss current experience in the application of NFs.
Current techniques used for nanomaterial characterization
Scientific evidence has indicated that NFs are highly efficient in improving plant nutrition and growth, with similar experimental work being carried out by various investigations. In the first stage, the characterization of NMs that compose NFs is essential to determine their properties. The main techniques used to evaluate NMs are: (1) nanoparticle tracking analysis (NTA), which allows the size distribution and concentration to be determined; (2) UV spectrophotometer, allowing their chemical nature to be characterized and identified; (3) dynamic light scattering (DLS), which allows their size, polydispersity index and surface charge to be determined; (4) differential scanning calorimetry (DSC), for characterizing their thermal stability; (5) transmission electron microscopy (TEM), which shows their morphological structure; and (6) inductively coupled plasma (ICP), which allows quantification of the NM inside biological matrices (Ma et al. 2018).
The physical characteristics of NMs—such as size, shape, surface, charge and elemental composition—influence the uptake, translocation and accumulation processes in plants. Size is closely related to the absorption capacity of plant roots and determines the transport process into a plant cell or cell organelles. The size of the NM is the greatest limitation on entry into the plant, the exclusion limit being 5–20 nm (Schwab et al. 2016). Particle shape influences agglomeration and reactivity on the surface of cells and structures. Meanwhile, the surface of the particle provides important information on its interaction with the plant surface (Pérez-de-Luque 2017; Fincheira et al. 2019). The charge of particles determines the fixation of the NM to the plant surface due to the negative charge of plant cells (Pérez-de-Luque 2017). Otherwise, plant responses to NFs are focused on genetic, metabolomic, and morphological analyses, during seed, seedling and plant stages (Fig. 1). The above characteristics show the importance of the physical–chemical properties of NMs in modulating plant growth.
Nanomaterials in plants: exposure route, uptake and transportation processes
The application of NFs at root or leaf level is crucial for stimulating plant growth. The effect of NF irrigation in the soil is influenced by soil processes such as homo-aggregation, hetero-aggregation, interaction with organic matter, chemical transformation, dissolution, and biotransformation (Zhang et al. 2020). Soil biological parameters like microorganisms and nematodes can influence the efficient plant uptake of NFs (Fig. 2). Furthermore, root exudates can improve the mobilization of NFs into plant roots and their transportation through the different channels and pores. Meanwhile, mucilage present on the surface of the plant root can restrict the entry of NFs into the plant. On other hand, NFs can penetrate by foliar application, being disseminated through nano-pores, open-stomata, hydathodes, lenticels and the cuticle. Once the NFs penetrate inside the plant, they may move through the apoplastic or symplastic pathways (Pérez-de-Luque 2017). Apoplastic transport occurs outside the plasma membrane in extracellular spaces, cell walls of adjacent cells, and xylem vessels. Apoplastic pathways play an important role in the movement of water and nutrients to reach the root’s central cylinder, where processes like endocytosis, pore formation and carrier proteins have been studied to determine their importance (Pérez-de-Luque 2017). Symplastic transport, on the other hand, occurs in specialized structures named plasmodesmata. In general, the physiological effects produced by NFs are related principally to photosynthesis, nutrient and water uptake, production of antioxidant enzymes, stress tolerance, cell wall modifications, and the CO2 assimilation rate (Fig. 3) (Schwab et al. 2016; Su et al. 2019; Verma et al. 2019). The specific effects of NFs on physiological changes in plants are described below.
Fertilizers based on nanomaterials
Carbon NMs (CNM)
The application of CNMs to plants has emerged recently in agriculture (Al-Rekaby 2018). CNMs are a class of engineering NM with electrical, optical and thermal characteristics that improve their properties. CNMs are classified based on their geometrical structure, with particles shaped like tubes (carbon nanotubes), horns (nano-horns), spheres, or ellipsoids (fullerenes) (Zaytseva and Neumann 2016). The literature shows that CNMs can have positive or negative effects on plant growth, depending on their type and concentration and on the species and growth conditions of the plants (Mukherjee et al. 2016). Carbon nanotubes (CNTs) are the principal CNM studied for the purpose of stimulating plant growth. Physical properties of CNTs, such as their length, diameter and solubility, are important parameters that control the extent of NM penetration inside the plants (Husen and Siddiqi 2014; Joshi et al. 2020). It has been reported that the degree of CNT uptake by plants is inversely proportional to NM size, suggesting that size is an important parameter for triggering optimal response in plant growth. Larger size probably prevents NM uptake by plant tissue. Furthermore, chemical functionalization of the NM surface with carboxylic and hydroxyl groups enhance CNT interaction with a plant cell. In experiments performed under controlled conditions, CNT can be acquired from growth media and translocated into the plant tissue, leading to increased plant growth parameters and crop yield (Mukherjee et al. 2016; Das et al. 2018).
CNTs can interact with biomolecules, leading to the functioning of nanosystems that act at the morphological, cellular, genetic and molecular levels (Al-Rekaby 2018). It is worth mentioning that CNTs are classified into two categories single-walled-carbon-nanotubes (SWCNTs) and multi-walled-carbon-nanotubes (MWCNTs)—depending on the layers present in the structure. SWCNTs contain a single layer of graphene with diameter from 0.4 to 2 nm, and length from 0.2 to 5 μm, whereas MWCNTs contain a multilayer of graphene with a length of 0.2 μm, inner layer diameter of 1–3 nm and outer layer diameter of 2–100 nm (Patel et al. 2020). A brief description of the impact of CNT on plant growth stimulation is presented in Table 1.
It has been observed that MWCNTs act as growth regulators during the seed and seedling stages of plants through the regulation of gene expression, cell division, nutrient and water transport and cell wall formation (Taha 2016). Smirnova et al. (2011) observed that MWCNTs can penetrate the cell wall of Onobrychis arenaria seedlings, and are then transported from the root to the stem and leaves through the plant’s vascular system. Similarly, MWCNTs at a dose of 100 μg mL−1 improved growth parameters during seed and seedling stages of Ricinus communis L. grown under controlled conditions (Fathi et al. 2017). These authors found that MWCNTs induce seed germination through NM penetration into the seed, enhancing water absorption. Al-Rekaby (2018) tested different doses of MWCNTs in combination with Delfan plus (biostimulator); the highest dose (MWCNT: 1000 mg L−1 and Delfan plus: 10 mg L−1) increased growth parameters in Hibiscus sabdariffa L. The results indicated that MWCNTs regulate the genes related to cell division and cell wall formation, and modulate nutrient uptake. Das et al. (2018) reported that the acquisition of MWCNTs by roots of Lactuca sativa is strongly dependent on the concentration applied.
It has also been observed that the MWCNTs had an important effect on the growth and yield of Avena sativa L. after application to seeds by the priming method (Joshi et al. 2018). Microscope photography revealed that primed seeds presented holes in their microstructure, indicating the probable mechanism by which MWCNTs entered the seeds. The increase in the relative water content indicated good water status of the leaves, which is related with an increase in the length and number of roots, and higher numbers of stomata in the leaves. MWCNTs may create new pores for water permeation and augment the capillary action of water. Anatomical analysis revealed that the number of epidermal cells, cortex cell length in stems, and the diameter of xylem vessels all increased in seedlings primed with MWCNTs. Furthermore, concentrations in the range from 50 to 150 mg L−1 improve the performance of Catharanthus roseus by increasing leaf width, leaf area and root length, and the activities of antioxidant enzymes such as catalase, peroxidase and phenylalanine ammonia-lyase (Ghasempour et al. 2019). This study highlighted the importance of MWCNTs in stimulating both secondary metabolism and the activity of antioxidant enzymes to induce the plants’ defense system. C. roseus treated with MWCNTs showed improved callus initiation, suggesting an effect on proliferation and differentiation processes.
Recently, Cao et al. (2020) reported that the application of 5 mg L−1 of MWCNTs increased lateral root formation both in number and length in seedlings of Solanum lycopersicum, reaching ~ 4.7 and ~ 23 mm respectively in test seedling−1, versus ~ 1.4 ~ 3 mm in control seedling−1. The data indicated that the action of MWCNTs is triggered by nitric oxide (NO) production, in turn triggered by nitrate reductase. This suggests that root development is mediated by NO due to its action in root organogenesis. Interestingly, it was reported that priming rice seeds with MWCNTs stimulated the growth and yield parameters by improving the water uptake and increasing root development and photosynthetic efficiency (Joshi et al. 2020). The authors suggested that MWCNTs lead to an increase in root hair, root development, and number of stomata, improving leaf water status and plant growth. Furthermore, Arabidopsis thaliana treated with Single-Walled-Carbon-Nanohorns (SWCNHs) presented strong root development, promoting primary root growth and lateral root formation through a direct effect in the meristematic and elongation zones (Sun et al. 2020). This study reported that the up-regulation of biosynthesis and responsive genes of auxin played an important role in increasing root development and reprogramming the production of secondary metabolites.
MWCNTs are an effective tool to mitigate the harmful effects on plants subjected to abiotic stress. MWCNTs play an important role in enhancing the expression of aquaporin proteins in the root, and the creation of new pores in the plasma membrane. In consequence, the water transport and nutrient use efficiency increased during salt stress conditions to improve plant growth. The homeostasis of ions and water is essential to maintain efficient physiological processes in plants. Martínez-Ballesta et al. (2016) reported that MWCNTs can be an important strategy to mitigate salt stress in Brassica oleracea, influencing the water and nutrient uptake through the retention of Na+ in the root (favoring a water diffusion gradient). The plant can change its water gradient through the symplastic pathways. Further, important evidence shows that MWCNTs mixed with sodium nitroprusside as NO donor improved the performance of Hordeum vulgare L. grown under salt conditions (NaCl 100 and 200 mM) (Karami and Sepehri 2018); this study showed that 500 mg kg−1 of MWCNTs increased photosynthesis, relative water content, growth parameters and antioxidant enzyme activities under saline stress. The authors noted that MWCNTs can enhance the water content through stimulation of root length and root dehydrogenase. Similarly, MWCNTs and graphene (5–200 μg mL−1) reduce growth suppression at root and shoot level in Sorghum bicolor L. under saline conditions (100 mM NaCl) (Pandey et al. 2018). Likewise, both carbon materials reduce the adverse effect of the saline medium in the germination of Panicum virgatum L. These results are strong evidence that MWCNTs represent an important tool for plants, improving their growth and tolerance to saline stress. Yousefi et al. (2017) reported that doses from 50 to 100 mg L−1 of MWCNTs improve the performance of Dodonaea viscosa L. during seed and seedling stages under drought stress, suggesting the role of dehydrogenase in enhancing cell elongation. More recently, it has been evidenced that MWCNTs improve the metal tolerance (CdCl2: 200 μM or Pb (NO3)2: 500 μM) of Brassica napus L, Helianthus annuus L. and Cannabis sativa L. (Oloumi et al. 2018).
Metal nanomaterials
Different metal NMs have been studied to improve plant growth and nutrition. Table 2 shows the experimental conditions used to evaluate the plant growth stimulation produced by silver, iron and zinc nanoparticles, which are described below.
Silver nanoparticles (Ag-NPs)
Ag-NPs have been highly studied in recent years in the food and agriculture industries (Budhani et al. 2019). The impact of Ag-NPs in plants depends on the route of exposure, growth conditions, duration of experiments, plant species, and chemical properties of NMs (Castro Gonzalez et al. 2019; Cvjetko et al. 2017). Juarez-Maldonado et al. (2013) observed that Ag-NPs applied in nutritive solution had better effects in comparison with foliar spray on the growth of Allium cepa L. Likewise, improvement in the growth of Trigonella foenum-graecum L. were observed after two applications of 200 μL of 1 μg mL−1 of Ag-NPs (Jasim et al. 2017). Further, beneficial effects of Ag-NPs are observed within vascular bundles, epidermal stem cells, and intermembrane spaces at the root level in the growth of Stevia rebaudiana B (Castro-González et al. 2019). It was suggested that Ag-NPs probably increase the concentration of N, Mg, and Fe, which are related to chlorophyll biosynthesis. Furthermore, interesting results were obtained in seed and seedlings of Solanum lycopersicum after the application of Ag-NPs, including weight, yield, number of leaves, and height (Noshad et al. 2019). Again, important physiological effects of Ag-NPs at 40 mg L−1 were obtained in T. foenum-graecum, where the concentration of photosynthetic pigments, indoleacetic acid, tannins, flavonoids, carbohydrates and proteins were increased (Sadak 2019). The results suggest that growth promotion could be related to photosynthesis, which is a product of changes in the N metabolism of plants and the increase in chemical energy efficiency. It noteworthy that the information about the application of Ag-NPs in the propagation of bulbous plants is scarce; Salachna et al. (2019) reported that Ag-NPs at 100 mg L−1 had an important effect on Lilium L. by increasing the concentration of N, K, Ca and S, accelerating the flowering stage.
It should be noted that Ag-NPs must be evaluated before application to prevent a possible toxic effect due to the contradictory effects in plant response. It was demonstrated that Ag-NPs can be more toxic than silver ions (Ag+) at 3 mg L−1 in A. thaliana, showing an inhibitory effect on root length and disruption of the thylakoid membrane (Qian et al. 2013). The negative impact is produced in the transcription of genes associated with antioxidant activity and aquaporin. The results suggested that the growth inhibition is due to the decrease in photosynthesis or the limitation in nutrient availability. Phytotoxic effects of both AgNO3 and Ag-NPs at concentrations in the range from 1 to 3 mM in Brassica sp. were detected by the inhibition of photosynthesis and the induction of oxidative stress (Vishwakarma et al. 2017).
Nanoscale zero valent iron (nZVI)
nZVI is an important industrial material synthesized to remove pesticides and heavy metals, but few studies have focused on studying its impact on plants. nZVI can generate H2O2 and OH radicals by Fenton reaction. Inside plants, apoplastic OH radicals play an important role in root cell-wall loss, which is an essential process in elongation for root growth. In consequence, the oxidation capacity of nZVI is proposed to increase root elongation. nZVI at 0.5 g L−1 increased root elongation in A. thaliana by 150–200% through the degradation of pectin-polysaccharides in roots and the capacity to release H2O2, which lead to OH radical-induced cell-wall loss (Kim et al. 2014). Low concentrations of nZVI (10–320 μmol L−1) promoted embryonic growth in seeds and germination of Arachis hypogaea (Li et al. 2015). Specifically, 40 μmol L−1 of nZVI increased the length and weight of seedlings, and 80 μmol L−1 of nanoparticles improved root development. Many studies have been carried out in hydroponic culture media but few studies use soil as a substrate. The application of 500 mg kg−1 of nZVI in soil increased the dry mass and leaf area of A. thaliana (Yoon et al. 2019). Interestingly, nZVI application improved the CO2 assimilation rate, stomatal conductance, intracellular CO2 concentration, and transpiration rate. Higher concentrations of starch and soluble sugars were detected, which can be attributed to the increase of the photosynthesis process. It was suggested that nZVI can produce Fe3O4 and Fe2O3, which have been reported as non-toxic or having a positive effect in other plant species either directly, due to their importance in Fe availability, or indirectly, in the increase of phytohormone and antioxidant activities.
Zinc nanoparticles (Zn-NPs)
Zn is an essential nutrient that protects the plant against low temperatures and other environmental stresses (Tarafdar et al. 2014). Zn contributes to the biosynthesis of cytochrome and leaf cuticle, and to plasma membrane integrity. Zn-NPs at a dose of 50 mg L−1 increase the concentration of chlorophyll and carotenoids in Triticum aestivum, but not in Solanum lycospersicum (Amooaghaie et al. 2017). The authors attributed this to the fact that the size of NPs and the dissolution of Zn2+ ions can play an important role in the differential response. The results also indicated that Zn-NPs at 100 mg L−1 increase the concentration of H2O2 and proline in both T. aestivum and S. lycospersicum. Another study reported that Zn-NPs produce changes in the radicle and plumule length of seeds of Oryza sativa L. (Upadhyaya et al. 2017). Zn-NPs activated the antioxidant activities of enzymes such as catalase, superoxide dismutase, glutathione reductase and guaiacol peroxidase. These results indicate that Zn-NPs protect seeds of O. sativa from ROS damage through the increase of antioxidant activities, contributing to better germination.
Metal oxide nanomaterials
The applications of metal-oxide NMs have been studied as plant growth stimulants in different species; the principal results indicate an important effect on seed, seedling and plant stages. The main metal-oxide NMs studied are described below, and greater detail is presented in Table 3.
Cerium oxide nanoparticles (CeO2-NPs)
Currently, there is limited information on the impact of the application of CeO2-NPs to plants grown in soil, and more studies are required. The application of 100 and 400 mg kg−1 of CeO2-NPs during the life cycle of T. aestivum under field conditions showed increases of 24.8 and 32.6% in grain protein content (Du et al. 2015). On the other hand, 400 mg kg−1 of CeO2-NPs decreased the chlorophyll concentration, and both concentrations tested altered the cellular ultra-structure of the leaves and roots. Micrographs showed that plants treated with CeO2-NPs had chromatin condensation attributed to signal stress. Interesting results showed that 100 mg kg−1 of CeO2-NPs increased shoot and root biomass of L. sativa (Gui et al. 2015). It was found that CeO2-NPs at 1000 mg kg−1decreased the soluble sugar content and the enzymes related to the antioxidant system (superoxide dismutase, peroxidase and malondialdehyde) in the root of L. sativa, indicating that a higher concentration produces phytotoxic effects in plants.
Organic matter present in the soil can play an important role in determining the behavior of CeO2-NPs in porous media. Differential effects of CeO2-NPs were observed in Phaseolus vulgaris grown in soil with different organic matter contents, and a higher translocation of Ce was found in plants in soil with high organic matter (Majumdar et al. 2016). The leaves of P. vulgaris grown in soil with high organic matter presented an increase in the stomatal conductance and the transpiration rate. In another study, it was determined that the stimulation or toxicity caused by CeO2-NPs in A. thaliana depends on the concentration applied (Yang et al. 2016). 500 mg L−1 of CeO2-NPs stimulate root and shoot growth, whereas higher concentrations (1000–3000 mg L−1) produce alterations in the photosynthesis process and antioxidant activity. It was reported that CeO2-NPs at doses from 300 to 2000 mg L−1 increase shoot and root length in Fragaria × ananassa by improving efficiency in the absorption of water and nutrients (Dai et al. 2020). These authors detected that CeO2-NPs are translocated from mother root to daughter root, and their concentration was lower in the leaf and fruit compared with the stem and root. Recently, it was observed that CeO2-NPs stimulated growth in Zea mays by enhancing leaf biomass, stomatal conductance and root development, but exposure of the plant to Cd decreased the leaf dry weight (Fox et al. 2020). Nevertheless, CeO2-NPs can produce adverse effects, it was reported that doses of 125 and 500 mg kg−1 affected the nutritional status of Triticum aestivum L. grown in soil (Rico et al. 2017). This result indicated that CeO2-NPs produce alterations in plant metabolism and uptake in T. aestivum.
Copper oxide nanoparticles (CuO-NPs)
CuO-NPs have been extensively studied in biomedical and industrial applications due to their high efficiency. One study showed that CuO-NPs play an important role in the organogenesis process of O. sativa because they impart antimicrobial properties to crops (Anwaar et al. 2016); the results indicated that CuO-NPs with a size of 40 nm produce callus induction up to the concentration of 10 mg L−1. Moreover, concentrations from 0.8 to 798.9 mg L−1 of CuO-NPs increase the root diameter of L. sativa and Daucus carota, however root length decreased after the same treatments (Margenot et al. 2018). Root thickening was a physiological response to physical stress and Cu2+ dissolved in the medium. Another study reported that 20 ppm of CuO-NPs is an efficient concentration to increase the growth and the photosynthetic pigments in Lycopersicon esculentum (Ananda et al. 2019). Increasing the concentration of CuO-NPs enhances the activity of superoxide dismutase and glutathione peroxidase, which lead to lipid peroxidation. Recent evidence indicates that the application between 0.01 and 0.025 mg mL−1 of CuO-NPs increases the seed germination, root length and seedling vigor index in Lens culinaris (Sarkar et al. 2020). CuO-NPs at 0.025 mg mL−1 induced the activation of defense enzymes such as peroxidase, polyphenol oxidase and phenylalanine ammonia-lyase. The higher concentrations of antioxidant enzymes indicated an increase in resistance to oxidative stress (Sarkar et al. 2020). In one work, 50 mg L−1 of CuO-NPs increased the root weight of O. sativa, but the high concentrations tested produced phytotoxic effects in early seedling growth (Wang et al. 2020). Opposite effects were found by Da Costa and Sharma (2015), who reported that germination and the growth of O. sativa L. decreased at 50–100 mg L−1 of CuO-NPs. Photosynthesis was affected by a decrease in the number of thylakoids per granum, stomatal conductance and photosynthetic pigments, caused by the accumulation of CuO-NPs.
Iron oxide nanoparticles
Iron (Fe) is an essential element for the growth and development of plants; it is also an important constituent of the photosynthetic system and antioxidant enzymes. 100 μg g−1 of Fe3O4-NPs increased the protein content, photosynthetic efficiency, chlorophyll concentration and nutrient status of Ca and Fe in the shoots and seeds of Z. mays (Jalali et al. 2016). The effect was attributed to the improvement of homeostasis in the plant redox system produced by the increased ferritin concentration. Similarly, γ-Fe2O3-NPs (200–800 mg L−1) increase Fe2+ in the tissue of S. lycopersicum (Shankramma et al. 2016). The application of 50 mg L−1 of γ-Fe2O3-NPs in Citrus maxima increased the chlorophyll content and root activity; it also induced ferric reductase and genes associated with the transportation of Fe to improve Fe acquisition (Hu et al. 2017). Another study demonstrated that Fe3O4-NPs (1–1.5 mg L−1) improve embryogenesis and rhizogenesis in Linum usitatissimum L. (Kokina et al. 2017).
The application of 1000 and 2000 mg L−1 of Fe3O4-NPs in the soil of P. vulgaris improved the nutrition status of soil and plant, evidencing higher nutrient uptake by roots from the soil (de Souza et al. 2019). Likewise, α-Fe2O3-NPs increased shoot length, weight and seed vigor index of S. lycopersicum (Abusalem et al. 2019). Furthermore, doses at 50 and 75 mg L−1 of Fe3O4-NPs improved the antioxidant enzyme activities (peroxidase, ascorbate peroxidase and catalase) and flavonoid contents to confer protection on Dracocephalum kotschyi (Nourozi et al. 2019). It may also be noted that the application of Fe3O4-NPs increases pharmaceutical compounds such as rosmarinic acid and xanthomicrol; moreover, 1 mg L−1 of Fe3O4-NPs increases the germination percentage, biomass and shoot growth of Eruca sativa (Plaksenkova et al. 2019). The same study reports that concentrations between 1 and 4 mg L−1 confer plant protection against environmental stresses. It has recently been reported that 4 mg L−1 of Fe3O4-NPs increase the root length and chlorophyll content of Medicago falcata L (Kokina et al. 2020).
Of particular interest are studies reporting that iron oxide nanoparticles improve plant tolerance to abiotic stresses. Fe2O3-NPs confer salt tolerance in Mentha piperita, inducing an increase in plant weight and nutrient contents (Ca, Fe, Zn, P and K) (Askary et al. 2017). The antioxidant activities of enzymes such as catalase, guaiacol peroxidase and superoxide dismutase were increased in plants grown under 150 mM of NaCl. Likewise, 20 mg L−1 of Fe3O4-NPs mitigate stress triggered by CdCl2 (100–200 μM) in seedlings of S. lycopersicum, improving their growth and nutritional status at shoot and root level (Rahmatizadeh et al. 2019). Otherwise, studies have described both negative and positive impacts depending on the size and concentration of nanoparticles. For example, Fe3O4-NPs with particle size of 5–10 nm (3 and 10 mg L−1) decrease shoot and root length in Nicotiana tabacum (Alkhatib et al. 2019); photosynthetic rate, stomatal conductance and transpiration rate all decreased after the application of different concentrations or sizes of Fe3O4-NPs. On the other hand, Fe3O4-NPs of 10 nm and at 3 mg L−1 increased the concentration of chlorophyll and leaf area of N. tabacum. The protein content increased after applying particles of 5 nm at a concentration of 30 mg L−1.
Silicon dioxide nanoparticles (SiO2-NPs)
Silicon (Si) is the second most abundant element on the Earth, and is of great importance in alleviating deleterious effects produced by abiotic stresses. This protective role of Si can be attributed to the fortification of the cell wall (Luyckx et al. 2017). Recently, Li et al. (2020) showed that SiO2-NPs ameliorated the toxic effects in Glycine max grown in a medium with mercury (Hg) contamination, increasing seedling growth and reducing the translocation and accumulation of Hg. Nevertheless, a different study demonstrated that SiO2-NPs at doses in the range from 10 to 2000 mg L−1 had a toxic effect on Bt-transgenic cotton, decreasing the plant height and biomass (Nhan et al. 2014).
Titanium dioxide nanoparticles (TiO2-NPs)
TiO2 is beneficial to plant growth and development; in particular, application at low concentrations has been reported to increase crop performance (Chaudhary and Singh 2020). TiO2-NPs increase the growth and antioxidant enzyme activities of Lemna minor at a concentration of 1000 mg L−1 (Song et al. 2012). A comprehensive study showed that 0.01% of TiO2-NPs confer salt tolerance (NaCl: 180 mM) on Vicia faba L. by improving soluble sugar, total amino acids and proline concentrations (Abdel Latef et al. 2018). As the concentration of applied TiO2-NPs increases, the concentration of antioxidant enzymes such as superoxide dismutase, ascorbate peroxidase, catalase and peroxidase decreases. Important evidence showed that TiO2-NPs improve the photosynthesis process and antioxidant defense, increasing plant growth. Simultaneous application of TiO2-NPs and sodium nitroprusside (nitric oxide donor) promotes growth during seed and seedling stages of T. aestivum grown under Cd stress conditions, constituting a novel approach to counteract the adverse effect on plant development (Faraji and Sepehri 2018). Recently, Gohari et al. (2020) reported the important effects of TiO2-NPs to alleviate salt stress in seedlings of Dracocephalum moldavica L., by improving the photosynthetic parameters. Specifically, 100 mg L−1 of TiO2-NPs improves the antioxidant enzymes and the essential oil production.
Zinc oxide nanoparticles (ZnO-NPs)
ZnO-NPs are among the most used and consumed NPs. They are reported as biocompatible with the human system according to the US Food and Drug Administration (FDA) (Ali et al. 2018). ZnO-NPs improve the root growth, seed germination and indoleacetic acid (IAA) production of Cicer arietinum (Pandey et al. 2010). It has been reported that ZnO-NPs produce morphological and biochemical changes to activate the antioxidant system in cotton plants (Priyanka and Venkatachalam 2016). Furthermore, ZnO-NPs and P supplementation increase the growth, soluble protein and antioxidant enzyme activity in Gossypium hirsutum (Venkatachalam et al. 2016). An important study demonstrated that ZnO-NPs increase polyphenol oxidase and dehydrogenase in Carthamus tinctorius L. (Hafizi and Nasr 2018). Faizan and Hayat (2019) reported that 50 ppm of ZnO-NPs was the optimal dose to increase chlorophyll content, photosynthetic rate, leaf protein content and antioxidant enzymes in Lycopersicon esculentum; this study also reported an increase in lycopene and β-carotene content. The positive effect is attributed to the interaction of ZnO-NPs with meristematic cells, stimulating biochemical pathways related to plant development. Interestingly, a dose from 0.2 to 1 μM of ZnO-NPs improves the performance status of N. tabacum by increasing growth and stimulating the production of metabolites such as auxin, flavonoids and phenolic compounds (Mazaheri et al. 2019). Furthermore, ZnO-NPs increased the activity of enzymes such as catalase, ascorbate peroxidase, superoxide dismutase and polyphenol oxidase, conferring protection on N. tabacum. Pérez Velasco et al. (2020) showed that ZnO-NPs coated with maltodextrin improve the growth of S. lycopersicum by increasing the height and the diameter of the stem and root. Nevertheless, an adverse effect of ZnO-NPs was found by Khan et al. (2019), who reported phytotoxic effects modulated by ethylene pathways in A. thaliana exposed to 50 to 300 mg L−1. Likewise, ZnO-NPs applied at a dose between 200 and 300 mg L−1 reduced growth, photosynthesis and leaf stomatal conductance in A. thaliana (Wang et al. 2016b). It was observed recently that ZnO-NPs are found inside the leaves of V. faba, decreasing photosynthetic parameters like stomatal conductance, the quantum efficiency of photosystem II and the coefficient of photochemical quenching in the steady state; particles of 25 nm were more harmful than particles of 70 nm (Pedruzzi et al. 2020).
As discussed above, diverse NMs of essential or non-essential elements helped to induce plant growth through modulation of photosynthesis, the antioxidant system and other biochemical pathways. Nanotechnological tools have likewise been applied for the development of nanocarriers to allow controlled release of conventional fertilizers containing nitrogen, phosphorus and potassium, to improve the efficiency of nutrient use.
Nanocarriers for the controlled release of conventional fertilizers
Nowadays, agricultural practices are based on the use of chemical fertilizers to increase crop yield; however, poor efficiency in nutrient use and large losses produced by lixiviation and volatilization constitute the main limitations of this practice (Kah et al. 2019). In consequence, an innovative approach has been developed through the development of nanocarriers for the controlled release of nutrients (Table 4). According to the literature, the main research works are focused on macronutrients like nitrogen, phosphorus and potassium, which are the principal nutrients for adequate performance in crops. Below we describe the main nanostructured materials used for the encapsulation of fertilizers.
Nanoclays
Nanoclays constitute one of the main nanocarriers used for the controlled release of fertilizers. Nanoclays are layered hydrates of aluminosilicates with two-dimensional platelets, characterized by a thickness at nanometric scale and micrometric length. Nanoclays can exchange cations and intercalate neutral molecules between their layers by interaction with water (Pereira et al. 2012; Biswas et al. 2019). Synthetic nanozeolite/nanohydroxyapatite can act as a P-fertilizer, stimulating the growth of Matricaria chamomilla (Mikhak et al. 2016). Phosphate-exchanged layered double hydroxides (LDH) showed promising results in mitigating P-deficient soil compared to conventional fertilizer (Everaert et al. 2016). Another work showed that synthesized LDH containing phosphate ions produced P release similar to that of reactive P sources (Benicio et al. 2018). These nanoparticles have also been used to synthesize hydrotalcite-like LDH ([Mg–Al]-LDH) containing phosphate, which is an efficient system that prolongs release more than tenfold compared to KH2PO4 (Bernardo et al. 2018). Furthermore, the experiment with T. aestivum showed that LDH ([Mg–Al]-LDH) provided the same level of nutrition as conventional fertilizer (KH2PO4) using oxisol soil as substrate. Nitrogen is an important nutrient for plant growth, being essential to the production of biomass and fiber in agriculture. Considering the monetary cost, nitrogen fertilizer has the highest cost due to the large percentage lost in the environment. Montmorillonite is an abundant mineral belonging to the smectite group with the capacity to intercalate urea to produce granules with slow nitrogen release. Pereira et al. (2012) showed that nanocomposites containing urea (50–80 wt %) with montmorillonite (20 wt %) presented a slow-release behavior in urea dissolution.
Hydroxyapatite nanoparticles
Hydroxyapatite [Ca10(PO4)6(OH)2] is a biocompatible material of great interest for the controlled release of nutrients (Guo et al. 2018). Hydroxyapatite is insoluble in water, and therefore its involvement in chemical reactions with the soil, such as precipitation and adsorption on colloids is reduced; as a result it presents improved uptake by plant roots. Soliman et al. (2016) showed that hydroxyapatite-NPs improve the growth of Adansonia digitata by increasing the concentration of carotenoids, chlorophyll, total carbohydrates, proteins, vitamin C and phenols. It was observed that hydroxyapatite-urea in a ratio of 6:1 provides slow release of nitrogen due to the reduction of urea solubility (Kottegoda et al. 2017). Additionally, in a comparison with H3PO4, synthetic nano-hydroxyapatite at the rate of 200 mg kg−1 presented the best results in improving phosphorus nutrition in L. sativa grown on low and high calcareous soil, increasing the dry weight and the P concentration in plant tissue (Burak et al. 2018). Application of three different hydroxyapatite-NPs with different surface charge + 22.1 (+), − 1.37 (0), and − 18.8 (−) mV showed that all NPs increase the biomass in Helianthus annus; the NP (−) produced a 16.5-fold improvement in shoot biomass in ultisol soils (Xiong et al. 2018). Subsequently, Marchiol et al. (2019) observed that hydroxyapatite-NPs stabilized with carboxymethylcellulose stimulated root elongation in S. lycopersicum without phytotoxic effects in hydroponic culture. Interestingly, Pradhan et al. (2020) showed that urea loaded on hydroxyapatite-NPs improved the growth of O. sativa, increasing length, dry weight and fresh weight. The NPs were twice as efficient as conventional P and N fertilizers. Application of P-nanofertilizer obtained by the blinding of humic substances and hydroxyapatite-NPs had an improving effect on Z. mays seedlings (Yoon et al. 2020). The results showed that multifunctional P fertilizer increases both early plant growth and productivity.
Mesoporous silica nanoparticles and other silicates
Mesoporous silica nanoparticles (MSN) are non-toxic and biocompatible with large-area surfaces. MSN has stable mesoporous structures that contain porous channels; they can immobilize, carry and release plant nutrients, stabilizing the availability of elements for plant uptake. Thus, MSN can be an ideal nanofertilizer through loading or coating with nutrients for slow release. Synthesized MSN able to entrap urea granules revealed two sustained release stages which led to a fivefold increase in efficiency (Wanyika et al. 2012). It was observed that commercial MSN increased the rate of establishment of Zoysia japonica grown under high and low fertility conditions, suggesting that MSN improves the release of nutrients with limited availability, thus enhancing the growth rate (Adams et al. 2020). Shen et al. (2019) formulated a polyacrylate/silica nanoparticle hybrid emulsion for coating with urea granules, which strongly delayed the release of urea through the increase of wear resistance. A direct relationship was found between the silica concentration and the solubility percentage. More recently, Naseem et al. (2020) reported on a mesoporous nanocomposite of zinc aluminosilicate (ZnAl2Si10O24) loaded with urea to simultaneously release both zinc and urea. The results indicated that urea loaded on ZnAl2Si10O24 presented more efficient nitrogen recovery due to the slow release, supplying the N demand of O. sativa.
Chitosan nanoparticles (CHT-NPs)
CHT is a natural polymer obtained from the deacetylation of chitin: it is a major component of crustaceans, insects and fungi. CHT is non-toxic, biocompatible and biodegradable (Malerba and Cerana 2019); it also has important physical, chemical and biological properties (i.e., antimicrobial and antioxidant), providing plant protection and growth stimulation (Table 4) (Malerba and Cerana 2016). Strong evidence has been reported indicating that CHT is an efficient encapsulator of different agrochemicals to induce plant growth, minimizing the negative impact of active compounds, decreasing their toxicity and improving their efficiency. For example, Abdel-Aziz et al. (2016) showed that CHT-NPs loaded with NPK fertilizer enhance the harvest index and crop yield of T. aestivum, decreasing the life-cycle of nano-fertilized plants from 170 to 130 days. CHT-NPs applied at foliar and soil level increased the growth of Hordeum vulgare in parameters such as leaf area, grain yield and harvest index (Behboudi et al. 2018); furthermore, plants exposed to drought stress presented increased relative water content, proline content, grain weight and antioxidant activity (catalase and superoxide dismutase).
CHT-NPs containing low doses of NPK fertilizer can increase the concentration of proteins in P. sativum. Nevertheless, a reduction was observed in root elongation, as well as a genotoxic effect possibly produced by direct nanoparticle application to the roots (Khalifa and Hasaneen 2018). Chau Ha et al. (2019) reported that CHT-NPs with NPK increased the growth of coffee plants grown in soil, improving the nutrient uptake (N: 17.04%; P: 16.31%; K: 67.50%); the photosynthesis process and chlorophyll concentration increased by 71.7 and 30.6% respectively. Similarly, CHT-NPs presented a great capacity to entrap and slowly release the NPK mix during 168 h at room temperature, using urea, calcium phosphates and potassium chloride as nutrient sources (Kazemi and Salimi 2019). Furthermore, CHT-NPs loaded with K improve the root biomass production in Z. mays grown in soil, which can be attributed to the improvement of soil properties such as water conductivity, porosity and microbiological activity (Kubavat et al. 2020). Recently, Sharma et al. (2020) reported that CHT-NPs are an efficient carrier for Cu and salicylic acid to improve the growth of Z. mays; their results indicated an increase in the vigor index, chlorophyll content and antioxidant enzyme activities, and a reduction in the malondialdehyde content.
CHT-NPs have been used as an effective carrier for other compounds that act as signaling agents to induce plant growth. In particular, nitric oxide (NO) is a signaling molecule involved in the modulation of plant growth and response to abiotic stress (salinity, drought and heavy metals) (Asgher et al. 2016). For that reason, the application of NO donors encapsulated in CHT-NPs protects this compound against degradation, allowing controlled and prolonged release. CHT-NPs containing S-nitroso-mercaptosuccinic acid (S-nitroso-MSA, a NO donor) are more efficient than non-encapsulated NO donors in decreasing the negative impact of salinity stress on Z. mays (Oliveira et al. 2016). The results showed that MSA-CHT-NPs mitigate salinity stress, improving the photosystem II efficiency, chlorophyll content and growth rate. Similarly, the NO donor S-nitrosoglutathione (GSNO) encapsulated into CHT-NPS ameliorates water stress in sugarcane, improving photosynthetic efficiency and plant growth (Silveira et al. 2016). Recently, Lopes-Oliveira et al. (2019) showed that MSA-CHT-NPs can be applied in tree species during their acclimatization in the nursery.
Despite the large number of studies that describe a positive impact of nanoparticles on inducing growth in plants, there is little knowledge about the regulations. General information about the legal framework will be provided in the next point.
Regulations and legal framework for the use of nanofertilizers in agriculture
The regulation and legislation of products derived from nanotechnology play an important role in the commercialization of nanoproducts, due to the unique physical and chemical properties found at the nano-scale. Important scientific evidence has shown that the application of nanotechnology in agriculture results in greater efficiency compared to the currently commercialized analogs. Nevertheless, nano-products may have a negative impact on human health and the ecosystem, thus their application must consider a balance between efficacy and toxicity (Jain et al. 2016; Mitter and Hussey 2019). Regulatory arrangements should be set up to allow the development of nanotechnology in agriculture; recommendations by international entities like the EU Commission, the US Food and Drug Administration (FDA), the US Environmental Protection Agency (EPA) and the Royal Academy of Engineering have played an important role in researching the risks of nano-products (Jain et al. 2016; He et al. 2019). The European Union in particular has provided specific provisions for materials derived from nanotechnology, including Regulation (EC) 1333/2008 (food additives) and Regulation (EC) 450/2009 (materials contacted with food), among other documents for nano-regulation (Jain et al. 2016).
Duhan et al. (2017) collected information on NF products currently marketed in agriculture, indicating that various nano-products are marketed by a number of companies. This study reported that products based on biodegradable polymers, nano-sized nutrients, macronutrients loaded in polymer matrices, and nanoemulsion are commercialized for inducing growth in plants. In the same year, Prasad et al. (2017) presented a review of some commercialized NFs such as Nano Green (Nano Green Sciences, Inc., India), Nano-Ag Answer® (Urth Agriculture, CA, United States), Biozar Nano-Fertilizer (Fanavar Nano-Pazhoohesh Markazi Company, Iran) and Master Nano Chitosan Organic Fertilizer (Pannaraj Intertrade, Thailand). Furthermore, a literature review by He et al. (2019) reported on a series of commercial NFs such as NanoPro™ (Aqua-Yield® Operations, LLC) and NovaLand-Nano (Land Green & Technology). Nevertheless, the scientific community highlights the importance that must be attached to ensuring that commercializing companies inform consumers of the presence and composition of NFs. Despite the strong evidence supporting the efficiency of the application of nanoparticles in agriculture, there is a wide debate about their advantages versus the analog products already in the market.
Conclusion and future perspectives
Nowadays, scientific studies support the proposal that nanotechnology is an important strategy to improve food production and security, helping to mitigate the negative impact of the application of agrochemicals. Nanotechnology is considered a promising field for promoting plant growth and nutrition through site-specific delivery of fertilizers or active compounds. Moreover, nanoencapsulation techniques allow the prolonged, sustained release of nutrients or growth inducers, giving better penetration and uptake of nutrients by plant roots. Thus nanotechnology provides environmentally friendly, efficient and innovative tools to promote resilient agriculture. Specifically, it has been proposed that nanotechnology applied in horticulture could be an important strategy for nutrition and growth in vegetables through the precise application of smart NFs. However, the interaction between NM-plant-soil needs to be analyzed to enable us to understand the implications of applying nanotechnology in the agriculture ecosystem. Additionally, the potential toxicity of NMs must be studied to determine their impact on food, environmental ecosystems and human health. It should be noted that their long-term effects on biological systems and human health is unknown so far, thus there is an urgent need to determine the impact of NMs before expanding the application of NFs. Most experiments to date have been carried out under controlled conditions, making it difficult to determine their toxicity and implications for plant nutrition or the environment. A study model must be established that allows evaluation of both the immediate and long-term effects on plant systems and the ecosystem in order to obtain advanced knowledge of possible nanotoxic effects in agriculture. According to the studies reviewed for this work, the application of NMs can trigger different types of response depending on plant species and age, exposure period, and the concentration and physical–chemical characteristics of NMs. Research is therefore needed into the screening and optimization of the application of NMs in plant systems that will efficiently stimulate plant growth and nutrition. Furthermore, the importance of establishing regulatory guidelines to potentiate the application of nanotechnology in agriculture and environmental sciences should be noted. It has been argued that the regulatory framework established by the EU can create a degree of uncertainty for both traders and consumers, affecting public perception; nevertheless, the public has shown a positive disposition to nanotechnological products. Based on this evidence, it is concluded that the development of NFs constitutes an important strategy to minimize the negative impact produced by chemical fertilizers and growth inducers on the ecosystem. Nevertheless, model studies should be incorporated into nanotechnology research to determine the real implications of the application of NFs under greenhouse and field conditions to contribute to knowledge and potential application.
Author contribution statement
All authors contributed to conceptualization of review. PF writing- original draft preparation, reviewing and editing. AQ, GT and OR contributed to the supervision, reviewing, and editing. MCD and ABS contributed to the reviewing.
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Acknowledgements
This study was supported for the project financed by ANID/CONICYT FONDECYT/POSTDOCTORADO N°3180279, ANID/FONDAP/15130015, FAPESP (2018/08194-2), CNPq (404815/2018-9, 313117/2019-5). This research was partially funded by the Dirección de Investigación-Universidad de La Frontera.
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Fincheira, P., Tortella, G., Seabra, A.B. et al. Nanotechnology advances for sustainable agriculture: current knowledge and prospects in plant growth modulation and nutrition. Planta 254, 66 (2021). https://doi.org/10.1007/s00425-021-03714-0
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DOI: https://doi.org/10.1007/s00425-021-03714-0