Nanoparticles Based on Essential Metals and Their Phytotoxicity

Ruttkay‑Nedecky et al. J Nanobiotechnol (2017) 15:33 DOI 10.1186/s12951‑017‑0268‑3 REVIEW Nanoparticles based onessential metals andtheir phytotoxicity Branislav Ruttkay‑Nedecky1,2, Olga Krystofova1,2, Lukas Nejdl1,2 and Vojtech Adam1,2* Abstract Nanomaterials in agriculture are becoming popular due to the impressive advantages of these particles. However, their bioavailability and toxicity are key features for their massive employment. Herein, we comprehensively summa‑ rize the latest findings on the phytotoxicity of nanomaterial products based on essential metals used in plant protec‑ tion. The metal nanoparticles (NPs) synthesized from essential metals belong to the most commonly manufactured types of nanomaterials since they have unique physical and chemical properties and are used in agricultural and biotechnological applications, which are discussed. The paper discusses the interactions of nanomaterials and vascu‑ lar plants, which are the subject of intensive research because plants closely interact with soil, water, and atmosphere; they are also part of the food chain. Regarding the accumulation of NPs in the plant body, their quantification and localization is still very unclear and further research in this area is necessary. Keywords: Agriculture, Fertilizers, Nanomaterials, Essential metal nanoparticles, Nanoparticles uptake, Phytotoxicity © The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Background The main issues, of which agriculture worldwide have been facing to, are loss of fertile land due to pollution, desertification and climate changes. Due to unique and outstanding properties of nanomaterials it is not surprising that an effort to improve the agrarian sector using nanotechnology and nanomaterials has been developing [1–11]. Particularly, the use of various types of nanomaterials made of metal oxides, ceramics, silicates, magnetic materials, semiconductor quantum dots (QDs), lipids, polymers, dendrimers, and emulsions [12–15] aims to reduce the applied amount of plant protection products (PPP), to minimize the loss of nutrients during fertilization, and increase revenues through optimized nutrient management in agriculture [3, 4, 16–18]. Greater utilization of nanoparticles (NPs) in agriculture depends on several factors including well known effects, monitored fate as well as their potential toxicity and levels of overdosing. NPs may interact with their environment and plants are a fundamental part of all ecosystems. It can therefore be assumed that NPs will interact with plants and these interactions, such as income and their accumulation in plant biomass, will affect their fate and transport in the environment. NPs may also adhere to the roots of the plants and cause physical or chemical toxicity to plants. Interaction with microorganisms in the soil cannot be excluded because they can positively interact with plants [19–22]. Based on these fact it is clear that there is an ability of nanomaterials to penetrate live plant tissues, but it has ramifications for their accumulation in the food chain and for their utility as smart delivery systems in living plants. Our ability to evaluate these impacts requires an understanding of how NPs are transported within a plant. It is important to understand whether intact NPs can be taken up by plants and transported to other plant tissues. In this area, it was found that NPs can enter plant tissues through either the root tissues or the aboveground organs and tissues (e.g., cuticles, trichomes, stomata, stigma, and hydathodes), as well as through wounds and root junctions (Fig.1). Only several studies have reported ‘direct’ uptake, translocation, and localization of NPs in plants using various insoluble NPs including mesoporous silica NPs [23], silica NPs (SNPs) [24], carbon nanotubes [25], fullerenes (C70) [26], QDs [27], Open Access Journal of Nanobiotechnology *Correspondence: vojt[email protected] 1 Department of Chemistry and Biochemistry, Mendel University in Brno, Zemedelska 1, 613 00 Brno, Czech Republic Full list of author information is available at the end of the article Page 2 of 19 Ruttkay‑Nedecky et al. J Nanobiotechnol (2017) 15:33 Au-NPs [28], titanium dioxide NPs (TiO2 NPs) [29, 30], iron (II, III) oxide (Fe3O4) NPs [31, 32], and virus-based NPs [33]. The toxicity of NPs in plants has been discussed several times [8, 34–37]. The conclusions showed that not all plants treated with nanoparticles exhibit toxic effects; substantially more studies showed positive or no consequential effects on plants. Nanotoxicity mechanisms remain unknown, however, it can be assumed to be closely related to the chemical composition, chemical structure, size, and surface area of nanoparticles. The presence of nanoparticles on the root surface can change the surface chemistry of the roots and consequently affect the uptake of nutrients into the plant root [21, 22], thus, these have to be taken into consideration too. Generally, the toxicity of nanoparticles is attributable to two different steps: (1) chemical toxicity based on chemical composition, for example the release of (toxic) ions, and (2) stress stimuli caused by surface, size, or shape of the particles. In the review, first we describe the basic methods for phytotoxicity testing, then we provide an overview of the most common techniques for detecting and imaging nanoparticles in plants, and then we will focus on the benefits of using essential metal nanoparticles (Zn, Cu, Fe, Mn, and their oxides) in agriculture and current knowledge on their potential phytotoxicity. Methods fortesting the phytotoxicity ofmetal nanoparticles Phytotoxicity tests There are no specific test guidelines for nanotoxicity so EPA48 or OECD49 directives from the US for chemical testing are currently used [38]. Phytotoxicity tests generally use plants recommended by these guidelines. These are mostly species of crops, and include both monocotyledonae and dicotyledonae [38]. Species that are recommended most are bean (Phaseolus vulgaris), cabbage (Brassica oleracea), carrot (Daucus carota subsp. sativus), cucumber (Cucumis sativus), lettuce (Lactuca sativa), maize (Zea mays subsp. mays), oat (Avena sativa), onion (Allium cepa), radish (Raphanus sativus), rice (Oryza sativa), ryegrass (Lolium perenne L.), soybean (Glycine max), tomato (Solanum lycopersicum), and wheat (Triticum aestivum). Recently, research model species such as the well characterized thale cress (Arabidopsis thaliana) were also included [39]. Phytotoxicity tests are carried out in two stages of plant development: (1) during germination, when the germination percentage is measured, where the seeds must be exposed to the test solution for the duration of germination (preferably at least 4days) [38], and (2) during seedling growth, in which root/shoot elongation and dry weight are frequently used variables to assess the effects of plant exposure to harmful substances [40]. The aforementioned protocols have been applying for testing the Fig. 1 Pathways by which nanoparticles (NPs) are absorbed in plants (Adapted and modified from Dietz et al. [110] and Wang et al. [111]) Page 3 of 19 Ruttkay‑Nedecky et al. J Nanobiotechnol (2017) 15:33 effects of nanoparticles in water, wastewater, sediment, and slurry. For phytotoxicity testing different media for the growth of plants are used. The simplest medium is water (Fig.2). Other applications include soft gels or agars, which better represent the soil, and finally soil itself is also often used [39]. Nanoparticles tend to adsorb to soil matrix and aggregate in the natural environment which reduces their mobility and bioavailability (Fig.2). Also, the study of the interactions of nanoparticles with plants in alternative substrates does not take into account the potential interaction of nanoparticles with soil and the associated water phase [41]. For example, nanoparticles in soil can influence the growth of soil bacteria, which may then indirectly affect the plant growth [42]. Rico etal. [36] and Peralta-Videa etal. [43] are the pioneers of studies dealing with the effects of nanoparticles on vascular plants. The most common monitored parameters include the germination rate and root/stem growth rate. Recently, the number of leaves [44] and chlorophyll content [45, 46] of exposed plants were included as new monitored parameters for phytotoxicity tests. In addition, the cytotoxicity and genotoxicity of nanoparticles are assessed [39, 47], which is also indicated in Fig.2. Nanomaterials based onessential metals andtheir use inagriculture Essential metal nanoparticles are chosen because they are essential metals for plants, and are nontoxic in wide concentration range. This group of metals involves nanoparticles based on Zn, Cu, Fe, Mn, and their oxides. From these, zinc oxide (ZnO) and copper oxide (CuO) nanoparticles (NPs) are used in numerous commercial applications including antimicrobial formulations. Recent studies suggest the use of these NPs as fungicides in agriculture and in the food industry, whereas treatments with ZnO or CuO NPs inhibit the growth of fungal plant pathogens such as Botrytis cinerea, Penicillium expansum, Fusarium graminearum, and Phytophthora infestans [48–50]. Consequently, although NPs may be formulated for use in agriculture as crop protectants, their impact on nontarget soil microbes is not fully known. Both CuO and ZnO NPs cause bacterial cell death at doses that vary with the microorganism [42, 51, 52]. Nanoscale zerovalent iron (Fe0) and bimetallic Ni0–Fe0 nanoparticles have emerged as effective redox media for the detoxification of organic and inorganic pollutants in aqueous solutions. These nanomaterials (10–100 nm) have larger surface areas and reactivity than bulk Fe0 particles [53–55]. Mn deficiency has been widely reported all over the world, especially in soils with higher pH (>6.0) or in calcareous, sandy, peat, or muck soils [56]. Therefore, Mn fertilization is very important to improve Fig. 2 Important considerations when designing phytotoxicity studies and endpoints in phytotoxicity studies (Adapted and modified from Miralles et al. [39]) Page 4 of 19 Ruttkay‑Nedecky et al. J Nanobiotechnol (2017) 15:33 agronomic production [56]. Manganese nanoparticles (MnNPs) have been also proposed as a suitable alternative to commercially used manganese salts MnSO4 (MS) for nanobiotechnology based crop management studies [57]. Nanomaterials based onZn Zinc nanoparticles (NPs) are spherical or polished metal particles with a high specific surface area. The applications of zinc nanocrystals include antimicrobial, antibiotic and antifungal agents, which are a part of painting buildings, dressing materials, nanofibers, plastics, and textiles [58]. Moreover, ZnO NPs are widely used in personal care products such as sunscreens, cosmetics, textiles, lipsticks, and hair dyes. In industrial products they are used in floor coatings, solar cells, as an antibacterial agent, and with optical and electronic materials [59–61]. These sprays are one of the direct routes of ZnO NPs into the environment. ZnO NPs are also present in agricultural spraying as a protecting material against UV radiation [62], where ZnO contributes together with an organic filter for the protection of photosensitive pesticides, is used directly for crop protection against UV radiation [63]. In addition, ZnO NPs have been also studied as a nutrient to increase the efficiency of plant fertilization, but the larger surface area of nanoparticles do not ensure improved solubility or even higher availability of Zn2+ for plants [64]. One may suggest that the solubility of Zn2+ in Zn fertilizers plays an important role in the agronomic effectiveness of the fertilizer. On the basis of thermodynamics, ZnO NPs should dissolve faster and to a greater extent than bulk ZnO particles (equivalent spherical diameter>100nm). These novel solubility features of ZnO NPs might be exploited to improve the efficiency of Zn fertilizers. In this field, coated monoammonium phosphate granules show greater Zn solubility and faster dissolution rates in sand columns compared to coated urea granules, which may be related to pH differences in the solution surrounding the fertilizer granules. The kinetics of Zn dissolution was not affected by the size of the ZnO NPs applied for coating of either fertilizer type, possibly because solubility was controlled by the formation of the same compounds irrespective of the size of the original ZnO NPs used for coating [64]. In another study ZnO NPs were investigated for their use as a Zn supplement. Seeds of several plants (Z. mays, G. max, Cajanus cajan and Abelmoschus esculentum) were coated with ZnO NPs. The germination test carried out with coated and uncoated seeds indicated a better germination percentage (93–100%) due to the ZnO coating when compared to uncoated seeds (80%). A pot culture experiment was conducted with coated seeds and this also revealed that the crop growth with ZnO coated seeds was similar to that observed with soluble Zn treatment applied as zinc sulfate heptahydrate [47]. Besides supplementation by Zn, ZnO NPs, synthesized by soil fungi in a concentration 10mgL−1, has been shown to enhance the mobilization of native phosphorus in the mung bean (Vigna radiata) rhizosphere. The analyses made by authors showed that they synthesized ZnO NPs with average diameter as 22.4nm as they claimed to have stable nanoparticles due to insitu corona formation by fungal extracellular protein used in the synthesis procedure. Zn acts as a cofactor for phosphorus-solubilizing enzymes such as phosphatase and phytase, and ZnO NPs increased their activity. The level of resultant phosphorus uptake in V. radiata increased by 10.8%. In addition, biosynthesized ZnO NPs also improved plant plienology such as stem height, root volume, and biochemical indicators such as leaf protein and chlorophyll contents [65]. Not only the effect but also the way of application was considered by authors as they choose foliar application on 2-week-old mung bean plants. The concentration of the ZnO suspension was 10mgL−1, where a total of 25mL of suspension ZnO NPs was sprayed on each plant by an atomizer generating droplets. In spite of the foliar application, the aforementioned positive effects have been evidenced. Next, the fungicide activity of ZnO NPs against F. graminearum was investigated, too. Wheat plants were inoculated with F. graminearum and treated with ZnO NPs (100mM). When the wheat plants reached maturation, the grains were harvested and evaluated for Fusarium (number of colonies, CFUg−1). ZnO NPs showed a reduction in number of CFU of F. graminearum when compared to the control [66]. In another work, ZnO NPs were shown to have interactive effects on Pseudomonas chlororaphis O6 (PcO6) to inhibit the plant pathogen F. graminearum. ZnO NPs were commercial ones with diameter less than 100nm. Growth of F. graminearum was significantly (p=0.05) inhibited by the inclusion of ZnO NPs in a mung bean both in mung bean agar and in sand tested in the presence and also in no presence of PcO6. The treatment itself lasted for 7days. The ZnO NPs were significantly more inhibitory to fungal growth than micro-sized particles of ZnO, although both types of particles released similar levels of soluble Zn, indicating size-dependent toxicity of the particles [49]. Thus, one can say that low concentrations of ZnO NPs are beneficial to plants. Positive effects of ZnO NPs are manifested in promoting germination, stem and root growth, increase in phosphorus mobilizing enzymes, phosphorus uptake, and antifungal properties. The observed positive effects of ZnO NPs on plants are summarized in Table1. Page 5 of 19 Ruttkay‑Nedecky et al. J Nanobiotechnol (2017) 15:33 Table 1 The observed positive effects ofZnO NPs onplants Plant Particle size (nm) Particle concentration Comment Observed effect References Vigna radiata 22.4 ± 1.8 10 mg L−1NPs were synthesized by soil fungi Increase in stem height and root length. Increase in phosphorus mobilizing enzymes and phosphorus uptake by 10.8% [65] Zea mays, Glycine max, Cajanas cajan, Abelmoschus esculentus <100 25 or 50 mg Zn g−1 seed Seeds were coated with ZnO NPs Improved germination [47] Coated seeds 93–100% Uncoated seeds 80% Triticum aestivum 30 100 mM Zn Wheat plants were inoculated with Fusarium graminearum Reduction in number of CFU of F. graminearum [66] Page 6 of 19 Ruttkay‑Nedecky et al. J Nanobiotechnol (2017) 15:33 Nanomaterials based oncopper Cu/CuO NPs are used in optoelectronics, catalysis, solar cells, as semiconductors, as they are also used as pigments, and fungicides [50, 67, 68]. Copper as fungicide is especially used in vineyards and in organic farming [62]. The ability of copper ions to prevent spore germination of fungi has been known for a long time, but to achieve this effect it is necessary to apply a large amount of copper (500–1500gha−1). Of note, it is certainly worth a patent of the BASF company [69]. Subject to the patent is the nanoparticulate amorphous Cu2+ salt, which forms by a reaction with polymer CuNPs within the size from 1 to 200nm. Compared with commonly used non-nano product containing cupric hydroxide (Cuprozin, Spiess Urania Chemicals), the same dose of copper in the form of nanoparticles improves efficiency by 8% against a phytopathogenic fungus on vines [62]. This is an example of how the nanoparticle form can reduce the amount of Cu discharged into the environment. Recently, one study demonstrated that CuNPs absorbed in chitosan hydrogel had positive effects on tomato growth and quality [70]. During this process, the activity of some enzymes can increase such as catalase, or decrease in the case of ascorbate peroxidase [71]. It is believed that the stimulatory effects of CuNPs are related to the induction of antioxidant activity [72]. The positive effect of CuNPs on S. lycopersicum is shown in Table2 in the same way as in the case of Zn NPS. Nanomaterials based oniron Iron nanoparticles (INPs) represent a new generation of environmental remediation technologies that could provide cost-effective solutions to some of the most challenging environmental issues. Because of large surface areas and high surface reactivity [73], INPs have found their main application in remediation [71]. This method is relatively cheap and uses both free (soil application, where INPs can penetrate ground water) and into matrix fixed nanoparticles (cleaning water or air) [54]. In the greatest extent INPs are used to decompose substances such as chlorinated hydrocarbons (e.g. trichloroethylene), organochlorine pesticides, and polychlorinated biphenyls [54]. Besides decomposing, INPs can be further applied to bind, for example, to a significant pollutant, arsenic ions [74]. Materials composed of nanoscaled iron particles exhibit high absorbency and a second advantage is their response to external magnetic fields by which they can be, even with bound arsenic compounds, removed. The mentioned procedure can also be used for other metals such as mercury or lead [75]. In agriculture, Fe2O3 NPs may be used instead of Fe fertilizers [76]. Rui etal. evaluated the effectiveness of iron oxide nanoparticles (IONPs; Fe2O3 NPs) as a fertilizer to replace traditional Fe fertilizers [77]. The effects of the Fe2O3 NPs and a chelated-Fe fertilizer (ethylenediaminetetraacetic acid-Fe; EDTA-Fe) on the growth and development of peanut (Arachis hypogaea), a crop that is very sensitive to Fe deficiency, were studied in a pot experiment. The results showed that Fe2O3 NPs increased root length, plant height, biomass, and soil plant analysis development (SPAD) values of peanut plants. The Fe2O3 NPs promoted the growth of peanuts by regulating phytohormone contents and antioxidant enzyme activity. The Fe contents in peanut plants with Fe2O3 NPs and EDTAFe treatments were higher than the control group. The next study was conducted to examine the effect FeNPs (prepared by reduction with a gum kondagogu) on the growth of a mung bean (V. radiata). The radical length and biomass was increased in seeds exposed to FeNPs in comparison with the ions [78]. In the following study, the uptake of iron oxide (Fe2O3) nanoparticles by spinach (Spinacea oleracea) via hydroponics was demonstrated and its effects on the growth rate and productivity of the spinach plant were examined. The experimental studies such as plant growth (stem and root length) and biomass analysis revealed a dose and time dependent increase due to the uptake of Fe2O3 [19]. In the next study, TrujilloReyes et al. showed that iron NPs, unlike CuNPs, did not affect the chlorophyll content, plant growth, catalase (CAT), and ascorbate peroxidase (APX) activities of lettuce (L. sativa) [71]. In another work, INPs after foliar application had significant effect on yield, leaf Fe content, stem Mg content, plasma membrane stability, and chlorophyll content of Vigna unguiculata [79]. In the following study, Alidoust etal. investigated the effect of 6-nm IONPs and citratecoated IONPs (IONPs-Cit) on photosynthetic characteristics and root elongation during germination of a soybean (G. max L.) [20]. Plant physiological performance was assessed after foliar and soil IONPs fertilization. No adverse impacts at any growth stage of the soybeans were observed after the application of IONPs. Table 2 The observed positive effects ofCuNPs onSolanum lycopersicum Plant Particle size (nm) Particle concentration Comment Observed effect Reference Solanum lycopersicum <100 15, 30, 60, 150 mg L−1CuNPs were adsorbed on chi‑ tosan hydrogels Application of chitosan hydro‑ gels with CuNPs was favorable to tomato growth and quality [70] Page 7 of 19 Ruttkay‑Nedecky et al. J Nanobiotechnol (2017) 15:33 The Fe2O3 nanoparticles produced a significant positive effect on root elongation, particularly when compared to the bulk counterpart (IOBKs) suspensions of concentrations greater than 500mgL−1. In the next study of Ghafariyan etal. [80] seed germination of a soybean exposed to superparamagnetic iron oxide nanoparticles (SPIONs) was investigated. It was found that SPIONs, which were entered and translocated in the soybean, increased chlorophyll levels with no trace of toxicity. Furthermore, it was found that physicochemical characteristics of the SPIONs had a crucial role in the enhancement of chlorophyll content in subapical leaves of soybeans. The equivalent ratio of chlorophyll a to b in all treatments with conventional growth, medium iron chelate, and SPIONs (as iron source) indicated no significant difference on the photosynthesis efficiency. An overview of the positive effects of INPs and iron oxide nanoparticles (IONPs) on plants is shown in Table3. Nanomaterials based onmanganese Manganese (Mn) is an essential micronutrient for growth regulation and the development of plants [81]. It plays a pivotal role in oxygenic photosynthesis both directly and indirectly. The major drawbacks associated with Mn deficiency are plant nutritional disorders [81]. To circumvent this nutritional disorder of plants, nanoparticle mediated crop management has of late found potential applications [57]. In a study by Pradhan etal. the effect of manganese nanoparticles (MnNPs) on nitrogen uptake in mung bean plants (V. radiata) was investigated [82]. The objective of this study was to determine the response of manganese nanoparticles (MnNP) in nitrate uptake, assimilation, and metabolism compared with the commercially used manganese salt, manganese sulfate (MS). MnNPs were modulated to affect the assimilatory process by enhancing the net flux of nitrogen assimilation through NR-NiR and GS-GOGAT pathways. This study was associated with toxicological investigation on invitro and invivo systems to promote MnNPs as a nanofertilizer and can be used as an alternative to MS. In another study from the same research group [57] MnNP-treated chloroplasts showed greater photophosphorylation, oxygen evolution with respect to control, and MnSO4-treated chloroplasts as determined by biophysical and biochemical techniques. Positive effects on root and shoot elongation was observed. MnNP-treated plants did not trigger oxidative stress. In the next study, Liu etal. [83] investigated the effects of laboratory-prepared MnOx NPs on the germination of lettuce (L. sativa) seeds in a water medium. MnOx NPs only slightly reduced the germination percentage from 84% (control) to 63% even at a high concentration of 50mg L−1 and was not significantly different from that of the control. Furthermore, MnOx NPs specifically improved the growth of lettuce seedlings by enhancing root elongation. For example, the 5-day root length of the seedlings increased by 68%. Similarly, 10and 5-mgL−1 NPs also significantly increased the elongations by 41.6 and 53.9%, respectively. An overview of the positive effects of MnNPs and manganese oxide nanoparticles (MnOx NPs) in plants is shown in Table4. Phytotoxicity ofZnO, Cu (CuO), andiron oxide nanoparticles A good understanding of the mechanisms of the nanoparticle phytotoxicity is important for the targeted application of nanoparticles [84]. Essential metal NPs can cause phytotoxicity via the dissolution and release of higher concentration of essential ions [85, 86] such as Zn2+ and Cu2+ or the production of excess reactive oxygen species (ROS) through redox cycling and the Fe2+-mediated Fenton reaction [87]. Phytotoxicity ofnanoparticles based onZnO Ecotoxicity studies on ZnO NPs are most abundant in bacteria and are relatively lacking in other species [88]. These studies suggest relative high acute toxicity of ZnO NPs (in the low mgL−1 levels) to environmental species, although this toxicity is highly dependent on test species, physicochemical properties of the material, and test methods. Particle dissolution to ionic zinc and particleinduced generation of ROS represent the primary modes of action for ZnO NPs toxicity across all species tested, and photo-induced toxicity associated with its photocatalytic property may be another important mechanism of toxicity under environmentally relevant UV radiation [85]. ZnO NPs have been shown to induce oxidative stress in soybean (G. max) seedlings in a concentration of 500mgL−1. Plant growth, rigidity of roots, and root cell viability were markedly affected by ZnO NPs stress. Oxidation–reduction cascade related genes, such as GDSL motif lipase 5, SKU5 similar 4, galactose oxidase, and quinone reductase were down-regulated in ZnO NPs treatment [89]. In the next study, Mukherjee etal. [90] investigated the impact of different zinc oxide (ZnO) NPs on green pea plants (Pisum sativum L.). Pea plants were grown for 65days in soil amended with commercially available bare ZnO NPs (10nm), 2 wt% alumina doped Al2O3/ZnO NPs (15 nm), or 1 wt% aminopropyltriethoxysilane coated KH550/ZnO NPs (20nm) at 250 and 1000mg NPs.kg−1 soil inside a greenhouse. Although all treated plants showed higher tissue Zn content than controls, those exposed to Al2O3/ZnO NPs at 1000mgkg−1 had greater Page 8 of 19 Ruttkay‑Nedecky et al. J Nanobiotechnol (2017) 15:33 Table 3 The observed positive effects ofiron/iron oxide NPs onplants Plant Particle size (nm) Particle concentration Comment Observed effect References Arachis hypogaea γ‑Fe2O3, 20 nm 2, 10, 50, 250, 1000 mg kg−1 of soil Fe2O3 NPs were applied into soil and compared with a chelated‑Fe fertilizer Fe2O3 NPs increased root length, plant height, biomass, and SPAD values of peanut plants. Fe2O3 NPs adsorbed onto sandy soil and improved the avail‑ ability of Fe to the plants. Fe2O3 NPs can replace traditional Fe fertilizers in the cultivation of peanut plants [77] Vigna radiata FeNPs 2–6 nm +0.2% gum, +0.4% gum 1 mM Fe2+ions Natural biopolymer gum kondagogu as reducing and capping agent was used The radical length and biomass was increased in seeds exposed to Fe NPs in comparison to Fe2+ ions. The α‑amylase activity was increased in the seeds exposed to Fe NPs [78] Spinacea oleracea α‑Fe2O3 50 nm 100, 150, 200 mg kg−1 of soil Experiments were performed in a solid hydroponic medium consisting of sawdust and coco peat and adequate amounts of water Positive effects on spinach plant due to uptake of Fe2O3 nanoparticles such as increase in stem and root lengths, biomass production and magnetic properties were observed [19] Lactuca sativa Core–shell NPs Fe/Fe3O4 13/9 nm 10, 20 mg L−115‑days treatment of hydroponically grown lettuce The nano‑Fe/Fe3O4 at 10 and 20 mg L−1 and FeSO4·7H2O at 10 mg L−1 did not affect lettuce growth and chlorophyll content [71] Vigna unguiculata <100 nm 25, 500 mg L−1The elements were applied 56 and 72 days after sowing over the leaves, and data was collected after day 85 Iron had significant effect on yield, leaf Fe content, stem Mg content, plasma membrane stability, and chlorophyll content, probably as a result of more efficient photosynthesis [79] Glycine max γ‑Fe2O3 (IONPS) and citrate coated IONPs 6 nm 500, 1000 mg L−1Plant physiological performance was assessed after foliar and soil IONPs fertilization IONPs produced a significant positive effect on root elongation. IONPs‑Cit significantly enhanced photosynthetic parameters when sprayed foliarly. More pronounced positive effects of IONPs via foliar application than by soil treat‑ ment was observed [20] Glycine max Superparamagnetic iron oxide NPs (SPIONs) 8–12 nm 200, 400, 1000 and 2000 mg L−1Seed germination of soybean exposed to SPIONs was investigated SPIONs, which were entered and translo‑ cated in the soybean, increased chloro‑ phyll levels, with no trace of toxicity [80] Page 9 of 19 Ruttkay‑Nedecky et al. J Nanobiotechnol (2017) 15:33 Table 4 The observed positive effects ofMnNPs onplants Plant Particle size (nm) Particle concentration Comment Observed effect References Vigna radiata MnNPs 50, 100, 500, 1000 mg L−1Leaf and root enzyme extract was analyzed for use as nanofertilizer Nitrogen uptake, its assimilation, and metabolism was increased after MnNPs soil application [82] Vigna radiata MnNPs 50, 100, 500, 1000 mg L−1Leaf and root enzyme extract was analyzed. Chloroplasts from leaves were isolated and analyzed for their level of photophosphorylation and oxygen evolution MnNP‑treated chloroplasts showed greater photophos‑ phorylation, oxygen evolution with respect to control and MnSO4‑treated chloroplasts. Positive effects on root and shoot elongation was observed [57] Lactuca sativa MnOx NPs 5–15 nm 0.25, 0.5, 5, 10, mg L−1Overall, the data suggests that MnOx NPs can be used as an Mn fertilizer (better than their soluble or bulk solid counterparts) for crop growth improvement MnOx NPs specifically improved the growth of lettuce seedlings by enhancing root elongation [83] Page 16 of 19 Ruttkay‑Nedecky et al. J Nanobiotechnol (2017) 15:33 many questions still remain unanswered such as the fate and behavior of nanoparticles in plant systems, or the role of surface area or activity of nanoparticles on phytotoxicity, and the role of plant cell walls in the internalization of nanoparticles. In a study of phytotoxicity nanoparticles, the most urgent need is to build a connection between the characteristics of nanoparticles (surface area, particle size, surface tension) and phytotoxicity. Equally important is the need to understand the role of plant species and composition of the nanoparticles phytotoxicity. Finally, most studies on phytotoxicity and uptake of nanoparticles plants were performed in a hydroponic setup. Hydroponic studies do not reflect the interaction of nanoparticles with soil and soil microorganisms. Finally, it can be concluded that the nanoparticles prepared from essential heavy metals and their oxides have proven to be suitable for use in the agriculture. The least phytotoxic of these appear to be nanoparticles made of iron oxides and manganese oxides. Abbreviations ABA: abscisic acid; APX: ascorbate peroxidase; CAT: catalase; DHA: dehydro‑ genase activity; GDSL: motif consensus amino acid sequence of Gly, Asp, Ser, and Leu around the active site Ser; GDSL motif lipase 5: serine esterase and lipase with GDSL sequence motif; GS‑GOGAT pathway: glutamine synthetase‑ glutamate synthase pathway; IAA: indole‑3‑acetic acid; ICP‑OES: inductively coupled plasma optical emission spectrometry; MDA: malondialdehyde; NPs: nanoparticles; NR‑NiR pathway: nitrate reductase‑nitrite reductase pathway; POD: peroxidase; ROS: reactive oxygen species; SKU5 similar 4: multi‑copper oxidase type I family protein expressed in plant roots; SOD: superoxide dis‑ mutase; SPIONs: superparamagnetic iron oxide nanoparticles. Authors’ contributions BRN and LN reviewed the literature, drafted and wrote significant portions of the manuscript. OK and VA created the reviews’ concept and edited the manuscript. All authors critically reviewed the manuscript. All authors read and approved the final manuscript. Author details 1 Department of Chemistry and Biochemistry, Mendel University in Brno, Zemedelska 1, 613 00 Brno, Czech Republic. 2 Central European Institute of Technology, Brno University of Technology, Technicka 3058/10, 616 00 Brno, Czech Republic. Acknowledgements Not applicable. Competing interests The authors declare that they have no competing interests. The authors are entirely responsible for the content of the review of the opinions contained within it. Funding This research has been financially supported by the Ministry of Education, Youth and Sports of the Czech Republic under the project CEITEC 2020 (LQ1601) and by IGA_MENDELU_Tym003. Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in pub‑ lished maps and institutional affiliations. Received: 11 February 2017 Accepted: 11 April 2017 References 1. Knauer K, Bucheli TD. Nano‑materials: research needs in agriculture. 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