State of the art of polymeric nanoparticles as carrier systems with agricultural applications: a minireview

  • Mônica Pascoli
  • Patrícia Juliana Lopes-Oliveira
  • Leonardo Fernandes Fraceto
  • Amedea Barozzi Seabra
  • Halley Caixeta Oliveira
Original Article
  • 119 Downloads

Abstract

Polymeric nanoparticles have been developed as carrier systems for agrochemicals aimed at pest control and increased crop yields. This minireview summarizes the recent progress and challenges in the design and application of polymeric nanoparticles loaded with herbicides, fungicides, insecticides and plant growth regulators. The many advantages of these nanoagrochemicals are discussed including: (1) the availability, biocompatibility and biodegradability of many polymers, (2) the decreased impact on non-target organisms, (3) the protection of the active compounds against degradation, (4) their increased solubility, (5) modified release, and (6) an improved efficacy of the active ingredients. We also discuss the major gaps and obstacles in this area, such as the large-scale production of these systems and the need for investigations of the toxicity to non-target organisms.

Keywords

Agrochemicals Nanotechnology Pesticide Plant growth regulator Polymers 

Abbreviations

γ-PGA

Poly(γ-glutamic acid)

GA3

Gibberellic acid

LC50

Lethal concentration 50%

NO

Nitric oxide

PCA

Poly(citric acid)

PCL

Poly(epsilon-caprolactone)

PEG

Polyethylene glycol

PGA

Polyglutamic acid or polyglycolides

PGR

Plant growth regulators

PLGA

Poly(lactide-co-glycolides)

PVA

Poly(vinyl alcohol)

S-Nitroso-MSA

S-Nitroso-mercaptosuccinic acid

1 Introduction

Agriculture has a vital worldwide importance as one of the greatest providers of food resources as well as one of the main drivers of the economy of many countries. Agribusiness is estimated to be a US$ 2.9 trillion industry in global investment by 2030 (World Bank 2013). The use of agrochemicals, such as fertilizers, pesticides and plant growth regulators, plays a pivotal role for the maximization of agricultural production facing innumerable challenges including, weeds, phytopathogenic fungi, herbivorous insects and other pests, and abiotic stresses driven by climate changes (Sekhon 2014; Mishra et al. 2017). The worldwide consumption of agrochemicals is huge with approximately 2.5 million tons of pesticides consumed per year (FAO 2012). However, the indiscriminate use of agrochemicals can contribute to environmental contamination, leading to hazards to non-target organisms (humans, soil microbiota, native fauna and flora) and to pest resistance (Tilman et al. 2002; Oliveira et al. 2014).

Nanotechnology is the control and restructuring of matter at the dimension of roughly 1–100 nm, where new phenomena enable new applications (Lindquist et al. 2010). According to the European Union law, the acceptable definition of “nanomaterial” is: “a natural, incidental or manufactured material containing particles, in an unbound state or as an aggregate or as an agglomerate and where, for 50% or more of the particles in the number size distribution, one or more external dimensions is in the size range 1–100 nm” (European Commission 2011). Nanoparticles are particles that are unique in their size, with large surface area which enables unique features that are absent in bulk materials or larger particles (Lee et al. 2015). In this sense, some authors consider that the nanoparticle definition is not necessarily limited on the exact particle size, but rather on whether nanoparticles have different properties compared with non-nanoparticles of the same material (Lee et al. 2015).

Nanotechnology has an enormous potential to benefit agriculture, making the agro industry more eco-friendly with its current annual growth rate of 25% (US$ 1.08 billion) (Sabourin 2015). In addition to nanoparticles, nanomaterials that can be used in agriculture include nanoclays, nanogels, and carbon nanotubes (Choudhary et al. 2017; Sadeghi et al. 2017). Nanoclays are layered mineral silicates nanomaterials that provide well-dispersed and interactive surfaces upon exfoliation (Hetzer and Kee 2008). Nanogels are highly crosslinked polymers at nanosize scale able to retain a significant amount of water and biological fluids, proving a reservoir to hold biomolecules and active drugs (Sonzogni et al. 2018). Carbon nanotubes are materials composed of carbon atoms linked in hexagonal shapes, with each carbon atom covalently bonded to three other carbon atom (a cylinder fabricated of rolled up grapheme sheet) (Eatemadi et al. 2014).

In general, nanoparticles are developed with the goal of providing a controlled release system for agrochemicals, improving the solubility of products or protecting the bioactive compounds against premature degradation (Shang et al. 2013; Perez and Francois 2016). Nanoparticles may, therefore, increase the efficacy of the agrochemicals, offering better results with lower doses and number of applications, as well as they may decrease the risk of environmental contamination and the toxicity to humans and other non-target organisms (Saharan et al. 2015; Chhipa 2017; Choudhary et al. 2017).

1.1 Polymeric nanoparticles

Different types of nanoparticles can be used in agricultural systems, such as silica, metallic, metal oxide, lipid and polymeric nanoparticles (Sabir et al. 2014), for carrying many classes of agrochemicals, including herbicides, insecticides, fungicides, acaricides, fertilizers and plant growth regulators (Grillo et al. 2016; Mishra et al. 2017).

Polymeric nanoparticles are considered the simplest form of soft-materials for drug delivery applications owing to their facile synthesis and wide applicability across all aspects of the field (Bobo et al. 2016). Polymeric nanoparticles, which are the subject of this minireview, have been one of the most important nanostructured systems used for the controlled release of pharmaceuticals with satisfactory results (Mallakpour and Behranvand 2016; Pelegrino and Seabra 2017; Seabra and Durán 2017). These nanoproducts are particularly suitable as carriers for agrochemicals due to their biocompatibility, biodegradability and low toxicity (Grillo et al. 2012). Polymeric nanoparticles have the ability to efficiently encapsulate agrochemicals, which protects them from the surrounding environment and controls their release (Kashyap et al. 2015; Perez and Francois 2016).

Considering environmental aspects, green nanotechnology can contribute desalination treatment, wastewater remediation, generation of alternative clean energy, combat of drug-resistant pathogens, sustainable chemical synthetic routes, and sustainable agriculture and food production (Villasenor and Ríos 2018). Nanotechnology might permit the precise control of manufacturing and novel nanotechnological materials have been available for improving farming sustainable practices (Villasenor and Ríos 2018). In agricultural applications, the sustained release of active chemicals from the nanomaterial might avoid temporal overdose, decreasing the levels of chemicals and reducing the input and waste, in an economical feasible manner. Furthermore, the synthesis of nanomaterials under environmental-friendly conditions can reduce the environmental impact of the products and toxicity (Sanchez-Mendieta and Vilchis-Nestor 2012). To this end, “green” approaches to synthesize nanomaterials are desirable, such as the absence of organic solvents and hazardous chemicals and avoid the uses of high energy input. Green approaches include the use of non-toxic chemicals, biodegradable, biocompatible and natural materials, among other environmental-friendly tools (Seabra and Durán 2015).

Polymeric nanoparticles can be synthesized using different types of biodegradable synthetic or natural polymers. As green reagent, it should be highlighted polymeric polysaccharides, which have been extensively employed in bio-applications due to their low cost, biocompatibility, and biodegradability (Kollarigowda 2017). In agriculture, chitosan and pectin are natural polymers that are widely used for the development of nanoparticles (Kheiri et al. 2016; Sun et al. 2014; Chauhan et al. 2017; Gabriel Paulraj et al. 2017; Sandhya et al. 2017).

Chitosan is obtained by the N-deacetylation of chitin, a natural and ubiquitous polysaccharide, obtained from the exoskeleton of crustaceans, insects, and fungi (Elieh-Ali-Komi and Hamblin, 2016). Chitosan is the most popular biopolymer used in drug delivery due to its low cost, biodegradability, biocompatibility, antimicrobial and insecticidal activities, high permeability, high drug-loading ability, and muco-adhesive properties (Kashyap et al. 2015; Khan et al. 2017; Pelegrino et al. 2017c). In agricultural applications, chitosan has emerged as one of the promising natural polymers for successful delivery of agrochemicals, enhancing the stability of the loaded active drug (Kashyap et al. 2015). In addition, chitosan has the ability to chelate inorganic compounds for controlled delivery in plants (Saharan et al. 2015). Encapsulation of agrochemicals in chitosan-based nanoparticles has the following advantages: (1) the ability of chitosan to absorb to plant surfaces prolongs the contact time between the agrochemical and the plant absorptive surface (e.g., epidermis of stems or leaves), (2) chitosan itself plays an important role in plant defense against pathogens, (3) chitosan might stimulate plant development, inducing biotic and abiotic stress responses making plants more tolerant to pathogens (Kashyap et al. 2015; Malerba and Cerana 2016; Khan et al. 2017). Similar to chitosan, the polysaccharide pectin is biocompatible and biodegradable and extensively employed in the food industry, biomedical applications and agriculture (Kollarigowda 2017). Pectin is suitable for agricultural applications because it is a constituent of plant cell walls. It is rich in 1,4-linked 2-d-galactosyluronic acid residues (Luo and Wang 2014; Santos and Grenha 2015) (Fig. 1).
Fig. 1

Major agriculture applications of polymeric nanoparticles

Among the synthetic polymers used for nanoagroparticle formulations, we can cite poly (lactide-co-glycolides) (PLGA), poly(epsilon-caprolactone) (PCL), polyglutamic acid or polyglycolides (PGA), poly (vinyl alcohol) (PVA), poly(citric acid) (PCA), and polyethylene glycol (PEG) (Yang et al. 2009; Forim et al. 2013; Pradhan et al. 2013; Memarizadeh et al. 2014; Pereira et al. 2014; Oliveira et al. 2015a; González et al. 2016; Mondal et al. 2017; Pasquoto-Stigliani et al. 2017; Tong et al. 2017). Figure 2 represents the structure of the most important polymers used for the preparation of polymeric nanoparticles.
Fig. 2

Schematic representations of typical polymeric nanoparticles used in agriculture applications. The figure showed the nanospheres (matrix system) and nanocapsules (reservoir systems), as well as the chemical structure of some important polymers used to prepare carriers systems to agri-applications

Polymeric nanoparticles can be synthesized from preexisting polymers or by the direct polymerization of monomers (Rao and Geckeler 2011). They are classified as nanocapsules or nanospheres according to their physical composition (Fig. 2). While nanocapsules have a polymeric vesicular structure and internal oil phase, nanospheres present a solid matricial organization with the polymeric chains (Soppimath et al. 2001).

When designing a nanostructured delivery system, the control of the particle size, charge, chemical surface, and other physico-chemical properties is necessary to allow the desirable penetration, solubility and release pattern of the bioactive from the polymeric nanoparticle, in order to target the selected action to a specific site at a particular time (Bennett and Littlejohn 2014). The properties of many polymers, such as great availability, bioactive compound protection, biocompatibility and easy biodegradability in non-toxic metabolites, allow them to be used in the development of nanocarriers for different types of agrochemicals. Here, we will discuss the recent progress and challenges in the design and uses of polymeric nanoparticles as carrier systems for herbicides, fungicides, insecticides and plant growth regulators (Table 1).
Table 1

Summary of the studies describing the development of nanoparticles loaded with agrochemicals and their major biological effects

Class

Active ingredient(s)

Nanomaterials

Major biological effectsa

Active compound doses

Reference

Herbicide

Ametryn, atrazine or simazine

PCL nanocapsules

Reduced genotoxicity in Allium cepa chromosome aberration and human blood Comet assays

A. cepa assay: 100 mg mL−1; Comet assay: 100 mg mL−1

Grillo et al. (2012)

Herbicide

Atrazine

PCL nanocapsules and nanospheres

Reduced genotoxicity in Allium cepa assays. Effective pre-emergent control of Brassica sp. (seedling emergence). No effects on the growth of non-target Zea mays

A. cepa assay: 0.7–56.7 µg mL−1; Phytotoxicity: 2.5 kg ha−1

Pereira et al. (2014)

Herbicide

Paraquat

Chitosan/tripolyphosphate nanoparticles

Reduced genotoxicity in Allium cepa assays. Effective post-emergent control of Brassica sp. and Zea mays (visual symptoms). Reduced cytotoxicity in mammalian cell viability assays

A. cepa assay: 0.38 mg mg mL−1; Cytotoxicity: 0.0048 and 0.12 mg mL−1; Phytotoxicity: 2 kg ha−1

Grillo et al. (2014)

Herbicide

Atrazine

PCL nanocapsules

Increased post-emergent herbicidal activity against Brassica juncea (visual symptoms, induction of oxidative stress, inhibition of growth and photosynthesis). No persistent deleterious effects on non-target Zea mays

Phytotoxicity: 2 kg ha−1

Oliveira et al. (2015a, b)

Herbicide

Diuron

Carboxymethyl chitosan nanoparticles

Increased pre-emergent herbicidal activity against Echinochloa crusgalli (growth analysis). No effect on the growth of non-target Zea mays

Phytotoxicity: 3 kg ha−1

Yu et al. (2015)

Herbicide

Imazapic and imazapyr (co-loaded)

Alginate/chitosan and chitosan/tripolyphosphate nanoparticles

Reduced genotoxicity in Allium cepa assays. Reduced toxicity to mammalian cells. Herbicidal activity against Bidens pilosa was sustained

A. cepa assay: 0.5 mg mL−1; Cytotoxicity assay: 0.1 mg mL−1; Phytotoxicity: 400 g ha−1

Maruyama et al. (2016)

Herbicide

Metsulfuron methyl

Pectin nanocapsules

Increased post-emergent herbicidal activity against Chenopodium album (visual symptoms). Reduced toxicity to mammalian cells

Phytotoxicity: 0.05 g L−1; Cytotoxicity: 2 and 4 µg mL−1

Kumar et al. (2017a, b)

Herbicide

Metolachlor

PCL and PLGA nanoparticles

The nanoparticles internalized the roots of rice, decreased seed and roots size of Oryza sativa and Digitaria sanguinalis

Cytotoxicity: 10–400 mg L−1

Tong et al. (2017)

Fungicide

Chitosan

Chitosan nanoparticles

Increased chitosan antifungal activity against Fusarium graminearum

Antifungal activity: 100–5000 ppm

Kheiri et al. (2016)

Fungicide

Carbendazim and Tebuconazole

Polycaprolactone nanocapsules

Decreased phytotoxicity in Phaseolus vulgaris and cytotoxicity in animal cells

Phytotoxicity: 0.05–0.7 g kg−1; Cytotoxicity: 31.25–250 µg mL−1

Campos et al. (2015)

Fungicide

Azomethine

PCL nanoparticles

Increased antifungal activity and yields of plants in the treatment against Sclerotium rolfsii, Rhizoctonia bataticola and Rhizoctonia solani

Antifungal activity: 3.9–250 µg mL−1

Mondal et al. (2017)

Fungicide

Carbendazim

Chitosan/pectin nanoparticles

Increased antifungal activity against Fusarium oxysporum and Aspergillus parasiticus. Increased germination and root length of the maize, cucumber and tomato seeds

Antifungal activity: 0.5 and 1 ppm; Phytotoxicity: 0.5–1 mg L−1

Sandhya et al. (2017)

Fungicide

Hexaconazole

Chitosan nanoparticles

Increased effectiveness against Rhizoctonia solani. Lower toxicity to non-target cell lines.

Antifungal activity: 0.1–1 ppm; Cytotoxicity: 10 and 20 ppm

Chauhan et al. (2017)

Insecticide

Garlic essential oil

PEG nanoparticles

Increased insecticidal activity against Tribolium castaneum

Insecticidal activity: 2000–8000 mg kg−1

Yang et al. (2009)

Insecticide

Neem essential oil

PCL nanocapsules

Increased toxicity against Plutella xylostella

Insecticidal activity: 4000 and 5000 mg kg−1

Forim et al. (2013)

Insecticide

Acephate

PEG nanoparticles

Increased insecticidal activity against Sitophilus oryzae. Decreased oral toxicity in mice and human fibroblast cell lines

Insecticidal activity: 180–300 ppm; Toxicity in mice: 0.5–2 g kg−1; Cytotoxicity: 25–200 ppm

Pradhan et al. (2013)

Insecticide

Imidacloprid

PCA and PEG nanoparticles

Increased mortality of Glyphodes pyloalis larvae and decreased LC50 in non-target organisms

Insecticidal activity: 25–300 ppm

Memarizadeh et al. (2014)

Insecticide

Methomyl

Chitosan nanocapsules

Increased efficacy against armyworms

Insecticidal activity: 50 and 100 ppm

Sun et al. (2014)

Insecticide

Geranium and bergamot essential oils

PEG and chitosan nanoparticles

Increased acute and residual larvicidal activity on Culex pipiens

Insecticidal activity: 1–20 mg cm−2

González et al. (2016)

Insecticide

Neem essential oil

Chitosan nanoparticles

Decreased Helicoverpa armigera feeding, larval activity, and pupal weight

Insecticidal activity: 0.1–0.3%

Gabriel Paulraj et al. (2017)

PGR

S-Nitroso-mercaptosuccinic acid

Chitosan/tripolyphosphate nanoparticles

Improved protection of Zea mays plants against salt stress

Plant protection: 50 and 100 µM

Oliveira et al. (2016)

PGR

Gibberellic acid

Alginate/chitosan and chitosan/tripolyphosphate nanoparticles

Increased leaf area and photosynthetic pigment content of Phaseolus vulgaris

Plant growth: 0.012–0.05%

Pereira et al. (2017a)

PGR

Gibberellic acid

γ-Polyglutamic acid/chitosan nanoparticles

Enhancement of germination rate, root development and leaf area in Phaseolus vulgaris

Plant growth: 0.07–2.1 µg/g of seeds

Pereira et al. (2017b)

aIn comparison with the non-nano bioactive compound

2 Methodology

This article is a minireview of polymeric nanoparticles as carrier systems in agricultural applications. Papers on polymeric nanoparticles in agriculture, active compound protection, efficacy against weeds, insects and fungi, plant growth regulation, phytotoxicity, genotoxicity, and cytotoxicity were identified through a comprehensive survey in the electronic databases PubMed, ISI and Science Direct. The search was performed in the period from 2001 to 2017. The following terms were used to identify the documents that composed this review: polymeric nanoparticles, nanocapsules, agriculture, herbicides, insecticides, fungicides, plant growth regulators, natural insecticides, neem oil, biological effects and toxicity study. Also, all terms were used in English and as Booleans descriptors it has been used AND or OR.

3 Polymeric nanoherbicides

Herbicides are applied in agricultural fields for the control of weeds, which compete with crops for water, light and nutrients. Despite the importance of herbicides in maximizing crop yield, the indiscriminate use of these compounds has been associated with the contamination of water resources and intoxication of non-target organisms, with deleterious effects to the environment and human health (Albuquerque et al. 2016). With the aim of reducing the environmental impacts of herbicides, polymeric nanoparticles have been successfully developed as efficient carrier systems for some of these agrochemicals. This section highlights the recent progress in the use of polymeric nanoparticles containing herbicides.

Reports have shown that nanoherbicides have many advantages over conventional formulations. For example, the nanoencapsulation of diuron, imazapic + imazapyr, paraquat and triazines resulted in a slower release profile of the herbicides, which could significantly help to minimize herbicide losses and environmental contamination (Grillo et al. 2012, 2014; Pereira et al. 2014; Yu et al. 2015; Maruyama et al. 2016). Moreover, atrazine-loaded PCL nanoparticles, metsulfuron methyl-loaded pectin nanoparticles, and chitosan nanoparticles co-loaded with imazapic and imazapyr were less toxic to non-target organisms than the respective non-nanoherbicides, as demonstrated through in vitro toxicity assays using Allium cepa and/or mammalian cell lines (Grillo et al. 2014; Pereira et al. 2014; Maruyama et al. 2016; Kumar et al. 2017a, b).

At the same time, the nanoencapsulation of herbicides maintained or even increased the herbicidal activity against target plants, whereas deleterious effects on the growth of non-target plants were not observed. A notable example is the atrazine-loaded PCL nanocapsule. The analysis of parameters related to growth, photosynthesis and oxidative stress of mustard (Brassica juncea) plants showed an increased post-emergent herbicidal activity of this nanoherbicide compared to the conventional atrazine (Oliveira et al. 2015a). Thus, the atrazine-loaded PCL nanocapsule allowed for a ten-fold reduction of the atrazine application dose without compromising the biological activity of the herbicide, which would reduce the amount of highly contaminating atrazine in the environment (Oliveira et al. 2015a). In addition, atrazine-loaded PCL nanocapsules did not persistently affect the physiological parameters of maize (Zea mays) plants, thereby having no effects on the growth of this non-target crop (Oliveira et al. 2015b). An efficient pre-emergent herbicidal activity of atrazine-containing PCL nanocapsules was also reported, which was associated with the reduced soil sorption and greater bioavailability of the nanoherbicide compared with the conventional atrazine (Pereira et al. 2014).

Recently, PEG and PLGA nanoparticles were synthesized as a carrier system for metolachlor, which improved the water solubility of this hydrophobic herbicide (Tong et al. 2017). The metolachlor-loaded nanoparticles were internalized into root cells. Thus, this nanoformulation increased the metolachlor utilization by rice (Oryza sativa) and hairy crabgrass (Digitaria sanguinalis) plants, resulting in a higher herbicidal activity than the conventional herbicide and a lower toxicity to non-target human cells (Tong et al. 2017).

4 Polymeric nanofungicides

Fungal diseases are recognized as a general threat to plants, the environment and food health and are responsible for extensive losses in agriculture affecting levels as high as 90% of the crop production (Chen and Yada 2011). Fungicides are natural or synthetic compounds often used in agriculture to prevent the penetration or development of pathogenic fungi in plants and also to control fungal diseases. Nanotechnology can increase the efficiency of fungicides by lowering the amounts of the chemicals required as well as by reducing their environmental impact (Campos et al. 2014). This section describes important papers based on the use of polymeric nanoparticles (particularly chitosan-based nanomaterials, due to chitosan intrinsic antimicrobial activity) containing fungicides.

Polymers have unique properties that make them particularly promising for the development of nanofungicides. In addition to their suitability for the design of nanocarriers for fungicides, some polymers per se have fungicidal activity, such as chitosan (Kashyap et al. 2015). Interestingly, chitosan nanoparticles have higher antifungal activity against Fusarium graminearum than non-nano chitosan, as demonstrated in tests of inhibition of radial mycelial growth (Kheiri et al. 2016). Chitosan was also used to synthesize hexaconazole-loaded nanoparticles. In comparison with the free bioactive compound, the nanoformulation was much more effective in controlling Rhizoctonia solani, whereas the toxicity toward non-target cell lines was reduced (Chauhan et al. 2017). In addition to a reduced cytotoxicity, the nanoencapsulation of carbendazim and tebuconazole into PCL nanocapsules was associated with a lower phytotoxicity against common bean (Phaseolus vulgaris) compared to the conventional fungicides (Campos et al. 2015).

In a recent study, chitosan-pectin nanoparticles containing carbendazim showed higher antifungal activity against Fusarium oxysporum and Aspergillus parasiticus than the pure fungicide (Sandhya et al. 2017). Moreover, these carbendazim-loaded nanoparticles interfered less in seed germination and root growth in assays with maize, cucumber (Cucumis sativus), and tomato (Lycopersicum esculentum) (Sandhya et al. 2017). In another recent study, azomethine was encapsulated into PEG nanoparticles (Mondal et al. 2017). The in vitro inhibitory activities against Sclerotium rolfsii, Rhizoctonia bataticola and Rhizoctonia solani were significantly increased by azomethine nanoencapsulation. Moreover, in vivo tests using mung bean (Vigna radiata) plants contaminated with the fungi demonstrated that the application of the nanofungicide resulted in lower plant mortality and higher plant growth compared to conventional azomethine (Mondal et al. 2017).

5 Polymeric nanoinsecticides

Insects are one of the main contributors to crop damage, reducing productivity due to losses in the field and during food storage. Thus, insecticides are widely applied to control unwanted insects and to guarantee crop quality (Spencer et al. 2014). However, insecticides are often highly toxic to non-target organisms, which emphasizes the importance of developing modified release systems to improve their effectiveness toward target insects (Gogos et al. 2012). This section describes the recent progress in the design and uses of polymeric nanoparticles containing insecticides. According to the literature, PEG and PCL are the most employed polymers for this goal.

Poly(citric acid) (PCA) and PEG were used to load imidacloprid into nanoparticles. Imidacloprid nanoencapsulation was associated with increased mortality of Glyphodes pyloalis larvae and a reduced LC50 compared to the same parameters of the free insecticide (Memarizadeh et al. 2014). Similarly, Sun et al. (2014) showed that the efficacy of methomyl-loaded chitosan nanocapsules against armyworm larvae was higher than that of the conventional insecticide.

Pradhan et al. (2013) also used PEG to nanoencapsulate acephate and found excellent insecticidal activity against Sitophilus oryzae, as indicated by the high mortality of the larvae, pupae malformation and inhibition of acetylcolinesterase activity. In addition, acephate nanoencapsulation decreased acute oral toxicity in a mouse model and in vitro cytotoxicity in a human fibroblast cell line (Pradhan et al. 2013).

Given the adverse impacts of synthetic insecticides, there are intense efforts to replace them with natural products. Botanical insecticides (i.e., insecticidal biomolecules derived from plants) have advantages such as low toxicity to non-target species, low residual activity and low development of resistance by target organisms. However, the rapid degradation by sunlight and low persistence in the environment can hamper crop protection. Nanotechnology can, thus, provide a solution to allow for more intensive use of botanical insecticides (Oliveira et al. 2014).

For example, PEG nanoparticles have been developed as carrier systems for the essential oil of garlic (Allium sativum) (Yang et al. 2009). These authors have reported increased insecticidal activity of this nanoformulation against the red flour beetle (Tribolium castaneum) over the non-nano garlic essential oil. PEG and chitosan were also used to synthesize polymeric nanoparticles loaded with geranium (Geranium maculatum) and bergamot (Citrus bergamia) essential oils, which showed high acute and residual larvicidal activity on mosquitoes (Culex pipiens) (González et al. 2016).

Neem essential oil is one of the most applied botanical insecticides due to its wide range of effectiveness against insects and low toxicity to humans and non-target organisms. It is extracted from Azadirachta indica and is used in agriculture to control insects by acting as an insecticide and repellent (Campos et al. 2016). Chitosan nanoparticles containing PONNEEM® were associated with decreased Helicoverpa armigera feeding and larval activity and pupal weight (Gabriel Paulraj et al. 2017). Similarly, neem oil-loaded PCL nanocapsules were more effective against Plutella xylostella in comparison with the conventional essential oil (Forim et al. 2013).

Despite these promising results for the use of these nanomaterials, there is still a need for extensive evaluation of potential toxicity to non-target organisms, including plants. Pasquoto-Stigliani et al. (2017) have reported that exposure of maize plants to PCL nanocapsules containing oleic acid and neem oil resulted in a decrease in CO2 assimilation and stomatal conductance. These nanoformulations also showed increased toxicity against Allium cepa and mammalian cell lines. On the other hand, these increased adverse effects were not induced by PCL nanocapsules containing only neem oil.

The macrocyclic lactone, emamectin benzoate, is employed for the control of insect pests on a variety of crops worldwide (Ishaaya et al. 2002). In order to increase the photostability of emamectin benzoate, the active ingredient was conjugated with polyacrylate nanoparticles by emulsion polymerization. The resultant nanoparticles protected the decomposition of the pesticide (Shang et al. 2013).

6 Polymeric nanoparticles containing plant growth regulators

Plant growth regulators (PGR) are a class of natural or synthetic compounds that behave as plant hormones or affect the plant hormonal balance. PGRs usually act at low concentrations and are applied in agriculture to modulate plant growth and development, to increase crop yield, to ameliorate the quality of agricultural products, and to induce the plant response to stresses (Rademacher 2015). Auxins, cytokinins, gibberellins, ethylene, abscisic acid, brassinosteroids and nitric oxide (NO) are examples of PGRs (Nambara 2013).

One of the main pitfalls of PGR application in agriculture is the rapid degradation of these compounds under conditions of light and temperature found in the field, resulting in the loss of biological activity (Kah and Hofmann 2014). Moreover, most PGRs may be phytotoxic when applied at high concentrations, which makes the development of controlled release systems for PGRs highly desirable (Campos et al. 2014). Nevertheless, only a few studies have reported the development of modified release systems for PGRs, which include brassinosteroid-loaded chitosan microspheres (Quiñones et al. 2010), O-naphthylacetyl chitosan (Tao et al. 2012) and gibberellin-chitosan conjugates (Liu et al. 2013). The conjugation of gibberellic acid (GA3) with chitosan also led to an increase in the bioactive solubility and to a protection against photo and thermal degradation (Liu et al. 2013).

There is a recent pioneering study regarding the use of polymeric nanoparticles as carrier systems for PGRs (Oliveira et al. 2016). In this study, chitosan/tripolyphosphate nanoparticles containing the NO donor S-nitroso-mercaptosuccinic acid (S-nitroso-MSA) were more efficient than the non-encapsulated NO donor in the protection of maize plants against salt stress (Oliveira et al. 2016). The improved bioactivity of NO was associated with the sustained release of this molecule by the polymeric nanoparticles (Oliveira et al. 2016). NO donors have been successfully encapsulated into chitosan/tripolyphosphate nanoparticles for anti-cancer (Pelegrino et al. 2017a), anti-bacterial (Cardozo et al. 2014) and anti-parasitic activities (Seabra et al. 2015), to enhance NO delivery to human skin (Pelegrino et al. 2017b), and more recently to protect plants from abiotic stress (Oliveira et al. 2016). The NO donor molecule has strong electrostatic interactions with the chitosan backbone leading to a high encapsulation efficiency of this molecule (Pelegrino et al. 2017c), allowing for the versatile application of NO-containing chitosan nanoparticles in several biomedical and agricultural applications.

In a recent study, Pereira et al. (2017a) described the development of alginate/chitosan and chitosan/tripolyphosphate nanoparticles as controlled release systems for GA3. In assays of biological activity using common bean plants, GA3-loaded alginate/chitosan nanoparticles were more effective in increasing leaf area and the levels of photosynthetic pigments than the free hormone or the chitosan/tripolyphosphate nanoparticles (Pereira et al. 2017a). In another approach, GA3-loaded γ-PGA/chitosan nanoparticles also presented a sustained release of the plant hormone (Pereira et al. 2017b). In addition, the nanoencapsulation of GA3 into γ-PGA/chitosan nanoparticles resulted in an enhancement of the biological activity of GA3 toward common bean plants, inducing higher germination rates, root development and leaf area than the free hormone. As described in this section, chitosan is the most employed polymer for preparation of PGR-containing nanoparticles.

7 Conclusions, challenges and perspectives

There are an increasing number of scientific publications based on the synthesis, characterization and application of nanoparticles (particularly polymeric nanocarriers) in agriculture. Overall, the encapsulation of agrochemicals promoted a sustained and site-specific release of the bioactive compound and enhanced the desired effect. Polymeric nanocarriers are able to control the delivery of active ingredients to plants and reduce excess run-off (Chhipa 2017). In fact, encapsulation of agrochemicals into polymeric nanoparticles might reduce undesirable toxic effects on non-target organisms and enhance the thermal and photochemical stability of the encapsulated active ingredient (Cicek and Nadaroglu 2015). In this sense, the use of agrochemical-containing nanoparticles is expected to decrease the required dosage for efficacy and to ensure a sustained drug delivery (Nair et al. 2010; Kashyap et al. 2015; Oliveira et al. 2016). The use of nanotechnology in agriculture aims to maximize agriculture output (crop yields) and simultaneous minimizing input (such as herbicides, pesticides, and fertilizers).

What are the main challenges to propose the realistic use of nanomaterials in agriculture? Although significant progress has been made at laboratory settings in the investigation of potential uses of polymeric nanoparticles carrying agrochemicals, compared to biomedical and pharmaceutical applications, the use of nanoparticles in agriculture is still in its infancy. To enhance the research employed in the field the following important issues must be addressed:
  1. 1.

    The nanotoxicity of the agrochemical-containing polymeric nanoparticles requires further investigation to determine the environmentally relevant concentrations of the nanoparticles, their toxicity in acute and long-term exposure to plants, the environment, animals and humans (Sadeghi et al. 2017). In this regard, there are investigations attempting to determine the possible toxicity of nanoparticles in agriculture, their environmental behavior, phytotoxicity in plants and soil biota in order to establish the safe use of these promising materials (Iavicoli et al. 2017; Kah 2015; Tripathi et al. 2017).

     
  2. 2.

    The characterization of the potential risks resulting from the interactions of nanoparticles with biological systems must be reviewed in detail. Although there has been important progress on the knowledge about the uptake, distribution and bioavailability of polymeric nanoparticles in plants, there are still some important gaps to be overcome (Pérez-de-Luque 2017).

     
  3. 3.

    Although polymeric nanoparticles are mainly composed of biodegradable and biocompatible materials (such as chitosan and pectin), the nanoparticle internalization in plant cells and their accumulation require further investigation. Nanoparticles can be easily internalized, translocated, and accumulated in different plant cell compartments, leading to diverse and/or unexpected responses. Nanoparticles that accumulate in plant organs may act as sinks, or they may be translocated to other (undesirable) parts of the plant, in a similar fashion reported for animals.

     
  4. 4.

    Importantly, physical and chemical properties of engineered polymeric nanoparticles are dependent on a range of variables, including: size distribution, surface chemistry, surface charge, morphology, reactivity, concentration, hydrophobicity, target organism, composition of test media, and aggregation state. The behavior of the polymeric nanoparticle depends on the medium in which the nanoparticle is applied. Chemical and physical soil and/or water parameters (such as pH, temperature, and ionic strength) might interfere to the behavior of polymeric nanoparticles containing agrochemicals.

     
  5. 5.

    Another important issue is the cost and industrial production of nanoparticles. In this regard, chitosan-based polymeric nanoparticles are an ideal material for this task, owing to their low cost, biocompatibility and biodegradability.

     
  6. 6.

    For the appropriate transfer from laboratory setting to realistic agricultural applications, important studies on the production scheduling of the nanoparticles, their long-term stability and effects need to be addressed.

     
  7. 7.

    Finally, consumers are still unfamiliar with nanotechnology and they can distrust agrochemical-containing nanoparticles similar to the situation with transgenic crops. Hence, these gaps in knowledge need to be filled so that polymer nanoparticle technology can jump from the laboratory bench to field applications (Pérez-de-Luque 2017).

     

As reported in this minireview, the use of polymer nanoparticles in agriculture is recent but is steadily increasing, which demands the need for the evaluation of the toxicity and phytotoxicity of these materials. It is important to note that insecticide nanoformulations in particular are evaluated only on target organisms and rarely on non-target organisms, mainly in plants. We hope that this minireview inspires new avenues in this exciting field.

Notes

Acknowledgements

The authors would like to thank Coordination for the Improvement of Higher Education Personnel (PJLO) and São Paulo State Science Foundation (ABS, 2016/10347-6; LFF, 2015/15617-9; MO, 2015/17120-4). The authors also thank Proof-Reading-Service for the English revision of the text.

Compliance with ethical standards

Conflict of interest

On behalf of all author, the corresponding authors states that there is no conflict of interest.

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© Joint Center on Global Change and Earth System Science of the University of Maryland and Beijing Normal University and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Mônica Pascoli
    • 1
  • Patrícia Juliana Lopes-Oliveira
    • 2
  • Leonardo Fernandes Fraceto
    • 1
  • Amedea Barozzi Seabra
    • 3
  • Halley Caixeta Oliveira
    • 2
  1. 1.Laboratory of Environmental Nanotechnology, Institute of Science and Technology of Sorocaba (ICTS)São Paulo State University (UNESP)SorocabaBrazil
  2. 2.Department of Animal and Plant BiologyUniversidade Estadual de Londrina (UEL)LondrinaBrazil
  3. 3.Center for Natural and Human SciencesUniversidade Federal do ABC (UFABC)Santo AndréBrazil

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