The Use of Nanoparticles and Nanoformulations in Agriculture

Yuri S. Pestovsky∗ and Agustino Martínez-Antonio∗ Biological Engineering Laboratory, Genetic Engineering Department, Center for Research and Advanced Studies of the National Polytechnic Institute (Cinvestav), Campus Irapuato. Km. 9.6 Libramiento Norte Carretera Irapuato-León 36821, Irapuato, Guanajuato, México

In this review, the main potential applications of nanoparticles in agriculture, viz. nanofertilizers or plant growth stimulants, nanopesticides, carriers of conventional pesticides, and antibacterial agents are described. The information is grouped by possible applications of nanoparticles, and inside each section, where data is available, the chemical nature of nanoparticles is presented. The evaluation of the effect of nanoparticles in ﬁeld is emphasized, but preliminary data in vitro are also included. It is revealed that the great majority of publications in the theme deal with plant production, looking for beneﬁcial effects. It is possible that large-scale application of nanoparticles can lead to precision agriculture, a remarkable enhancement in agricultural productivity, and at the same time its cost would be diminished. Some envisioned risks associated with this practice are mentioned, and phytotoxicity of nanoparticles is discussed in a separated section. The main technical data, about nanoparticles characteristics,IP: 192.168.39.211 from all On: the reviewedSat, 02 Oct literature 2021 is04:35:08 compiled in a table. Copyright: American Scientific Publishers Keywords: Nanoparticles, Nanofertilizers,Delivered Nanopesticides. by Ingenta

CONTENTS 3.10. Copper Oxide Nanoparticles ...... 8705 1. Introduction ...... 8700 3.11. Zinc Oxide Nanoparticles ...... 8705

2. Nanoparticles as Fertilizers or as Plant Growth Stimulants ....8701 3.12. ZnO@SiO2 Nanoparticles ...... 8706

2.1. Silica Nanoparticles ...... 8701 3.13. Fe3O4/ZnO/AgBrNanoComposite...... 8706 2.2. Selenium Nanoparticles ...... 8701 3.14. Titanium Dioxide Nanoparticles ...... 8706 2.3. Gold Nanoparticles ...... 8701 3.15.ReducedGrapheneOxideNanoSheets...... 8706 2.4. Silver Nanoparticles ...... 8702 3.16. Chitosan Nanoparticles ...... 8706 2.5. Copper Nanoparticles ...... 8702 4. Nanoparticles as Pesticide Carriers ...... 8707 2.6. Copper Oxide Nanoparticles ...... 8702 4.1. Silica Nanoparticles ...... 8707 2.7. Palladium Nanoparticles ...... 8702 4.2. Gold Nanoparticles ...... 8707 2.8. Manganese Nanoparticles ...... 8702 4.3. Silver Nanoparticles ...... 8707 2.9. Zinc Oxide Nanoparticles ...... 8702 4.4. Zinc Oxide Nanoparticles ...... 8707 2.10. Ferric Oxide Nanoparticles ...... 8703 4.5. Ferrihydrite Nanoparticles ...... 8707 2.11. Titanium Dioxide Nanoparticles ...... 8703 4.6. Calcium Alginate Nanoparticles ...... 8707 2.12. Hydroxyapatite Nanoparticles ...... 8703 4.7. Calcium Alginate-Chitosan Nanoparticles ...... 8707 2.13. Other Nanofertilizers ...... 8703 4.8. Chitosan Nanoparticles ...... 8707 3. Nanoparticles as Nanopesticides ...... 8703 4.9. Polyethylene Glycol Nanoparticles ...... 8708 3.1. Silica Nanoparticles ...... 8703 4.10. Nanoparticles of Polymers of Ethylene Glycol and 3.2. Sulfur Nanoparticles ...... 8704 Isophthalic Acid Methyl Ester ...... 8708 3.3. Gold Nanoparticles ...... 8704 4.11. Methoxypolyethyleneglycol-Poly(lactide-co-glycolide) 3.4. Silver Nanoparticles ...... 8704 Nanoparticles ...... 8708 3.5. Ag2O/Ag Nanoparticles ...... 8705 4.12. Nanoparticles of Poly(citric acid)-Poly(ethylene 3.6. Ag3O4 Nanoparticles ...... 8705 glycol)-Poly(citric acid) with Encapsulated Titanium 3.7. Nickel Nanoparticles ...... 8705 Dioxide Nanoparticles ...... 8708 3.8. Platinum Nanoparticles ...... 8705 4.13. Nanoparticles of Polyethylene Glycol Grafted 3.9. Copper Nanoparticles ...... 8705 onto Alkoxyisophthalate ...... 8708 4.14. Nanoparticles of Polymers of Polyethylene ∗Authors to whom correspondence should be addressed. GlycolandDiacids...... 8709

J. Nanosci. Nanotechnol. 2017, Vol. 17, No. 12 1533-4880/2017/17/8699/032 doi:10.1166/jnn.2017.15041 8699 The Use of Nanoparticles and Nanoformulations in Agriculture Pestovsky and Martínez-Antonio

4.15. Poly(epsilon-caprolactone) Nanoparticles ...... 8709 developed at least 11 different types of resistance mech- 4.16. Solid Lipid Nanoparticles ...... 8709 anisms interfering with all stages of pesticide action.3 4.17.Nano-Liposomes...... 8709 Post-harvest pathogens can also develop multiple pesticide 4.18. Pesticide Nanoparticles Stabilized with Polymers ...... 8709 resistance.4 5. Other Uses of Nanoparticles in Agriculture ...... 8710 5.1. Gold Nanoparticles ...... 8710 Feeding the soil with fertilizers is also a cornerstone of 5.2. Silver Nanoparticles ...... 8710 modern organic agriculture, but it is extremely wasteful 5.3. Titanium Dioxide Nanoparticles ...... 8710 and inefficient. For example, less than 20% of phosphorus 6. Phytotoxicity of Nanoparticles ...... 8710 applied as fertilizers remains in the final agricultural prod- 6.1. Silica Nanoparticles ...... 8710 ucts, and the rest accumulates in soil and then leaks 6.2. Gold Nanoparticles ...... 8710 into the ground waters contributing to the widespread 6.3. Silver Nanoparticles ...... 8710 5 6.4. Copper Nanoparticles ...... 8711 eutrophication. The world cereal-grain nitrogen use effi- 6.5. Copper Oxide Nanoparticles ...... 8711 ciency is estimated to be only 33%, and a 1% of increase 6.6. Zinc Oxide Nanoparticles ...... 8711 in this efficiency for grain production worldwide would 6.7. Iron Oxide Nanoparticles ...... 8726 lead to $234 million savings.6 With micronutrients, the 6.8. Titanium Dioxide Nanoparticles ...... 8726 situation is even worse: the highest uptake efficiency is 6.9. Alumina Nanoparticles ...... 8726 17–23% for boron, 0.5–14.5% for molybdenum, 8.5% for 6.10. Cerium Dioxide Nanoparticles ...... 8726 7 7.Conclusion ...... 8726 zinc and 0.35% for copper. Acknowledgments...... 8727 Nanoparticle entrapment of drugs allows their enhanced ReferencesandNotes...... 8727 and prolonged delivery to, or uptake by, target cells and/or reduction of toxicity compared to their equivalent free drug.8 This same concept can be used in agriculture as 1. INTRODUCTION well. Moreover, nanoparticles have a highly reactive sur- Agriculture is the largest interface between humans and face; therefore, they are biologically active themselves.9 the environment, and is a major cause of soil and ecosys- Some nanoparticle-containing products aimed at agricul- 1 tem modification. Despite the extensive use of chemi- tural use are already in the market.10–12 cals, direct yield losses caused by pathogens, animals, Here, we will focus on the reported attempts of using and weeds, are altogether responsible for losses rang- nanoparticles as fertilizers or plant growth stimulants, 2 3 ing between 20 and 40% or evenIP: 192.168.39.211 over 50% of global On: Sat,antibacterial 02 Oct 2021 agents, 04:35:08 pesticides and carriers of conventional agricultural productivity. The progressCopyright: of intensification American Scientificpesticides. Publishers Considering using nanoparticles in agricul- of agricultural production was halted by theDelivered evolution byture, Ingenta one must remember potential adverse effects, there- of resistance against pesticides in pest populations. Such fore phytotoxicity of nanoparticles will also be briefly resistance including to numerous combinations of pesti- discussed. Although nanosensors1 13–15 and nanoparticle- cides has been reported by now, and pest species have mediated delivery of genes in plants1 15 are also considered

Yuri S. Pestovsky works in the group of Dr. Agustino Martínez-Antonio where he studies nanoencapsulation of bioactive molecules in cyclodextrins. He studied chemical enzy- mology at Moscow State University (Russia) and has Ph.D. in physical chemistry. He subsequently worked at Russian Science Based Technologies, Ekolit LLC (Russia) and National Sun Yat-sen University (Taiwan) before moving to Cinvestav in 2016.

Agustino Martínez-Antonio obtained his Ph.D. in biochemical sciences from the México National Autonomous University (UNAM). After postdoctoral research at UNAM and INSERM (France), he is currently a professor at the Center for Research and Advanced Studies of the National Polytechnic Institute (Cinvestav), where he directs the Biological Engineering Laboratory.

8700 J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 Pestovsky and Martínez-Antonio The Use of Nanoparticles and Nanoformulations in Agriculture for agricultural use, we will focus only on the application Oryza sativa vegetative stage, slightly increased spikelet of nanoparticles in agriculture, in its most common sense, number per panicle, plant height and straw weight, and for nutrition and for phytopathogens control. The main increased the percentage of filled spikelets by ∼1.5 times. technical data from all the literature reviewed is presented This pronounced effect was more than 2.5 times if the in a table, and characteristics of the nanoparticles are also solution was applied consistently during the reproductive provided there, if available from the literature cited. stage. The addition of silicic acid during the ripening stage caused a slight acceleration of ripening.23 2. NANOPARTICLES AS FERTILIZERS OR 2.2. Selenium Nanoparticles AS PLANT GROWTH STIMULANTS The treatment of Zea mays seeds with selenium nanopar- One should consider that the route of nanoparticles to ticles (0.1 g/ha) increased crop yield and the concentra- the plants is determined by the method of their application of starch and proteins in the seeds.24 In contrast to tion. Airborne (sprayed) nanoparticles will be attached to this report, a treatment with a selenium fertilizer (10 g leaves and other aerial parts of plants whereas roots will Se per kg, mixed with calcium ammonium nitrate, triple interact with soil-material-associated nanoparticles.16 After superphosphate and muriate of potash) at doses between application of nanoparticles to plants there is a theme, 5–25 g [Se]/ha had no positive effects in Zea mays.25 It is not studied at all, about how to eliminate the absorbed not clear whether selenium as nanoparticles was responsi- nanoparticles. For instance, washing with distilled water ble for the positive effect in the first case or the quantity or sanitizer Tsunami 100 containing peroxyacetic acid and combination with additional components made the dif- and hydrogen peroxide (200 mg/liter chlorine) of spinach ference in the second case. leaves previously treated with silver nanoparticles (40 nm, 40 mg/liter) did not remove all the nanoparticles. Clorox, 2.3. Gold Nanoparticles a sanitizer containing sodium hypochlorite (80 mg/liter Gold nanoparticles at concentration 0.013% (w/w) when peroxyacetic acid), only converted silver nanoparticles to applied in soil perturbed neither the soil microbial commu- AgCl nanoparticles having size 162 ± 51 nm and to larger nity nor germination of Lactuca sativa seeds but increased or smaller nanoparticles. Therefore, current factory wash- the ratio of shoot to root length.20 The treatment of Ara- ing methods for fresh products may not be effective on bidopsis thaliana seeds and seedlings with gold nanopar- the cleaning up of nanoparticles,17 and it can be a problem IP: 192.168.39.211 On: Sat,ticles 02 Oct at 802021g/ml 04:35:08 increased their germination rate and for agricultural use of nanoparticles because they can be a Copyright: American Scientificseed yield, Publishers accelerating the plant growth. Treated plants risk for humans consuming these products.18 Delivered by Ingenta were observed to flower earlier than the control ones, and the pods lengths were higher. The expression pat- 2.1. Silica Nanoparticles terns of several miRNAs was also observed to change. It was demonstrated that tomato (Lycopersicon esculen- The antioxidant potential, expressed as free radical scav- tum Mill. cv. Super Strain B) seedlings grew faster after enging capacity, and the levels of antioxidant enzymes treatment with fumed silica nanoparticles. The applica- were also increased,26 but the question of possible oxidation of the nanoparticles was made before and after tive stress caused by the applied nanoparticles was not germination. The percentage of Lycopersicon esculen- raised. Brassica juncea cv. Pusa jaikisan seeds treated tum seed germination was also improved. All the effects with gold nanoparticles germinated more rapidly, and the were dose-dependent in the concentration interval between growth of the seedlings was accelerated. Chlorophyll and 2–14 g/liter, with a maximum at 8 g/liter.19 The silica sugar content, seed yield, seed oil content and the num- nanoparticles did not perturb the soil microbial community ber of pods per plant increased as well. Brassica juncea or germination of Lactuca sativa seeds but increased the plants sprayed with the nanoparticles reduced the num- ratio of shoot to root length at concentration 0.066% (w/w) ber of primary branches, while the average number of in soil.20 secondary branches increased. The number of leaves per Colloidal silica exists in equilibrium with molecularly plant increased, but the average leaf area did not change. dispersed silica.21 This soluble silica exists as monomers In the case of Brassica juncea the maximum effect was and oligomers. They can undergo a series of dissociation observed at 10 ppm (except for sugar content which had a reactions, and the resulting ions can be hydrolyzed by maximum at 25 ppm). The oxidative stress occurred only breaking down of their siloxane bonds. A preparation of between 50–100 ppm.27 In the cases of Cucumis sativus ∼2.2 nm of silica nanoparticles at 0.2–0.4 M (expressed and Lactuca sativa, seeds treatment with gold nanopar- as monomeric SiO2) is soluble in 0.3 M of tetrapropylam- ticles had major effect on root elongation than on root monium hydroxide at 30 C. However, at pH ≤ 10 soluble weight. It should be noted that the nanoparticles were silica is negligible because silica can self-assembly at crit- claimed as stable in the presence of 22% NaCl.28 But ical aggregation concentration, and gelation occurs.22 citrate-capped gold nanoparticles readily precipitate in the The addition of 100 ppm of silicic acid to Kimura B presence of phosphate buffered saline solution, although solution (pH ∼ 5.5), applied once a week during only the it contains much smaller amount of salts.29 According to

J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 8701 The Use of Nanoparticles and Nanoformulations in Agriculture Pestovsky and Martínez-Antonio our observations, citrate-capped gold nanoparticles instan- levels of all these phytohormones increased, especially taneously precipitate even in the presence of 0.9% NaCl.30 those of gibberellin and abscisic acid, in Vicia sativa and of all these phytohormones except cytokinin in Triticum 2.4. Silver Nanoparticles aestivum, i.e., at 100 g/ha the nanoparticles proved to be Treatment of Triticum aestivum L. seeds with patented toxic for both plants, but had beneficial effect on Triticum silver nanoparticles at 10 mg/liter results in the aestivum at 1 g/ha.37 In the case of Zea mays L. somatic concentration-dependent uptake of the nanoparticles embryogenesis it was shown that the expression of several between 0.01–10 mg/liter. Triticum aestivum seed germi- miRNAs was responsive to auxin concentration.39 Since nation percentage was increased, and at 0.01 mg/liter, an the level of indole acetic acid can be affected by nanopar- increase in shoot and root dry weight was observed.31 ticles, the levels of miRNAs can also be expected to be Both silver nanoparticles at 20–60 ppm and silver nitrate affected, and further studies may show their role as medi- at 100 ppm sprayed on Borago officinalis L. decreased ators of effects of nanoparticles on plants. seed abscission and therefore increased seed yield. Other parameters, viz. leaf number, plant height, leaf length and 2.7. Palladium Nanoparticles width, dry weight of plant and of inflorescence, also had Aluminum hydroxide embedded palladium nanoparticles increased values. The concentration of silver in the form at concentration 0.013% (w/w) in soil did not perturb of nanoparticles needed for the given effect was less than soil microbial community neither germination of Lac- those in the form of nitrate. Total silver uptake by Borago tuca sativa seeds, but increased the ratio of shoot to officinalis was found to be concentration-dependent in the root length after 15 days of application.20 It should be rank of 20–60 ppm of the nanoparticles and 100–300 ppm noted that soluble biologically active alumina species can 32 40 of AgNO3. be released from the nanoparticles, and it is not clear Treatment of Brassica juncea seeds with silver nanopar- whether these released species were responsible for the ticles (25 and 50 ppm) proved to increase shoots and root mentioned effects. lengths.33 Treatment of Raphanus sativus seeds with silver nanoparticles at 13.5 mg/liter also caused root length 2.8. Manganese Nanoparticles increase.34 In other study, 100 M of silver nanoparti- These nanoparticles applied to the Vigna radiata seeds cles added to the growth medium promoted root growth and then added to the growth medium enhanced nitrogen in Arabidopsis. The treatmentIP: also 192.168.39.211 positively affected On: Sat, 02 Oct 2021 04:35:08 Copyright: American Scientificmetabolism Publishers by enhancing the activity of several enzymes cell division, chloroplast development and carbohydrateDelivered byinvolved Ingenta in this pathway. Although the total nitrate levels metabolism.35 in the plant tissue were not changed.41 The same nanoparticles also enhanced the activity of electron transport chain 2.5. Copper Nanoparticles in photosynthesis. The treatment of Vigna radiata with Copper nanoparticles increased the ratio of shoot to root the nanoparticles increased the levels of chlorophyll a length on Lactuca sativa at concentration of 0.066% (w/w) and b as well as of carotenoid and CP43 protein con- in soil.20 On the other hand, Helianthus annuus plants tents. The main cause of photosynthesis augmentation grown from seeds which had been treated with copper seemed to be due to plasmon enhancement of chloro- nanoparticles (0.5 g/ha) produced more seeds than the phyll molecules. Fresh and dry weight, rootlet number control ones. Protein, oil and ash content in the seeds as well as root and shoot length of the treated Vigna increased after treatment, as did the content of oleic radiata plants were significantly increased. Although the acid in the oil. Total copper content increased, but no nanoparticles released manganese ions, the Mn content in attempt to determine the presence of nanoparticles in the the leaf showed only a slight enhancement. Nanoparti- 36 seeds was made. In another study, irrigation with copper cles worked as a better micronutrient than MnSO4.The nanoparticles (1 g/ha) enhanced gibberellin, cytokinin and effects were not accompanied by oxidative stress or plant indole acetic acid levels of Vicia sativa L., and decreased morphological alterations. The nanoparticles were biosafe the abscisic acid levels, thus stimulating plant growth.37 toward the beneficial soil microorganism Trichoderma In another case, 0.03 and 0.05 g/ha of copper nanoparti- viride.42 Bioavailability experiments showed no induction cles result in a dose-dependent beneficial effect on wheat of hemolysis of human red blood cells. Small cytotoxicity germination, plant survival rate, fresh and dry weight as for mice and for human lymphocytes was observed only well as on productivity.38 at concentrations 1–25 mg/liter, far exceeding the concentration used for plant treatment41 (0.05 mg/liter).41 42 2.6. Copper Oxide Nanoparticles The irrigation with CuO nanoparticles at 1 g/ha decreased 2.9. Zinc Oxide Nanoparticles cytokinin levels in Vicia sativa but increased the levels Attempts were made to supplement fertilizer with Zn, but of indole acetic acid, gibberellin, abscisic acid and, espe- results of ZnO nanoparticles (uncoated, nearly spherical, cially, cytokinin in Triticum aestivum. At 100 g/ha the 20 nm, surface charge +15.7 mV) and bulk ZnO were not

8702 J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 Pestovsky and Martínez-Antonio The Use of Nanoparticles and Nanoformulations in Agriculture significantly different. Supposedly, the equal results were nanoparticles at 0.25% were also demonstrated to protect due to the aggregation of ZnO nanoparticles and formation Spinacia oleracea chloroplasts from ageing induced by of the same insoluble zinc-containing substances suppress- long time illumination by increasing the levels of super- ing the release of zinc ions.43 44 Even after dissolution of oxide dismutase, catalase, and peroxidase. The membrane the fertilizer granule, the zinc species remained near its structure of the treated chloroplasts was more stable than original location. If urea is present, high pH on the granule that of the control.51 The presence of phosphate enhanced surface is due to urea hydrolysis and might prevent ZnO the stability of 1 g/liter 50 nm anatase nanoparticles by sur- dissolution. Mass flow of water from the soil towards the face assimilation, giving it a negative charge (∼−40 mV hygroscopic fertilizer granule, in the opposite direction to at 2 mM phosphate). Therefore, phosphate promoted the zinc diffusion, could also restrict the plant uptake of zinc transport of anatase nanoparticles through quartz sand. ions.44 Sodium nitrate, a background electrolyte, promoted aggregation of anatase nanoparticles and decreased electrostatic 2.10. Ferric Oxide Nanoparticles repulsion between nanoparticles and sand particles, facili- Arachis hypogaea root dry biomass and chlorophyll tating their retention in soil.52 content with application of 1 g/kg -Fe2O3 nanoparticles and 45.87 mg/kg EDTA-Fe in soil had comparable 2.12. Hydroxyapatite Nanoparticles results, although significantly higher than the control. The The addition of hydroxyapatite nanoparticles at nanoparticles slightly increased the level of reactive oxy- 21.8 mg/liter (equivalent to phosphorus) to the growth gen species serving as growth promoters, i.e., hormesis medium enhanced Glycine max growth even more than effect was observed. Changes in the levels of plant hor- the application of regular phosphate fertilizer did. Dry mones also promoted growth. The advantage of nanoparti- biomass as well as seed yield were higher than for fertil- cles might be due to their ability to be adsorbed onto sandy izer without phosphorus. The application of nanoparticles soil particles improving their availability for plants.45 was expected to cause minimal risk of superficial water 53 Assayed -Fe2O3 nanoparticles (spherical and hexago- eutrophication, although it was not investigated. nal, 8 nm but agglomerated, 100 mg/liter) were found to release 20 ± 5% of their iron content at pH 1 for 30 min. 2.13. Other Nanofertilizers 3+ Moreover, a significant fraction of these Fe ions was Zeolite microparticles sieved to 60 mesh size activated 46 strongly associated with the nanoparticleIP: 192.168.39.211 surface. On: Sat,with 02 Oct hydrofluoric 2021 04:35:08 acid and then modified with amino- Copyright: American Scientificpropyltrimethoxysilane Publishers became charged and nanoporous Delivered by Ingenta 2.11. Titanium Dioxide Nanoparticles having 7.74 nm pore size and surface area 5.488 m2/g. TiO2 nanoparticles accelerated the germination of Triticum These were used to release encapsulated urea for aestivum at 10 ppm. Shoot and seedling lengths were 120 min.54 higher only in the presence of 1–500 ppm nanoparticles.47 It was recommended to sonicate Linum usitatissi- Rutile nanoparticles at 0.25–2.5‰ accelerated the germi- mum seeds after treatment with nanofertilizer to decrease nation of Spinacia oleracea.48 Growth of the seedlings their surface moisture content and to increase fertilizer of both plants was also improved by the nanoparticles absorption,55 56 this is assumed to happen by inducing 47 48 in comparison to bulk TiO2 and untreated control. microdamages of the seed surface allowing more intensive The treatment of Spinacia oleracea seeds with rutile uptake of the nutrients.55 nanoparticles increased the germination index, photosyn- thetic rate,48 49 chlorophyll48 49 and Rubisco activities.48 On the other hand, anatase nanoparticles applied to the 3. NANOPARTICLES AS NANOPESTICIDES seeds and then sprayed onto seedlings at 0.25% increased Nanoparticles can be potentially used as fungicides or nitrate and protein content in Spinacia oleracea seedlings, insecticides, as in the examples described below. this could be due to the activity of nitrate reductase, glutamate dehydrogenase, glutamate synthase and glutamic– 3.1. Silica Nanoparticles pyruvic transaminase activities, which were augmented.50 Silica nanoparticles were used to protect Oryza sativa Dry and fresh weights were increased by both types of grains against weevils (Sitophilus oryzae) at 0.5 and 1 g/kg 48–50 TiO2 nanoparticles, i.e., rutile nanoparticles gradually (nanoparticles/grains). In comparison, bulk-sized silica accelerated photosynthesis with their concentration ris- caused much less mortality of weevils. No new progeny of ing from 0.05% to 0.25%. They promoted photophos- weevils was found after Oryza sativa grain treatment with phorylation related to photosystem II more significantly any of these concentrations of silica nanoparticles.57 than that related to photosystem I;49 anatase nanoparticles As discussed earlier, silica nanoparticles can release sil- enhanced nitrogen metabolism but reduced or did not influ- icate ions, although in very small quantities. The ‘insecti- ence ammonium content, possibly because it was inten- cidal’ effect of silicate ions may actually involve not the sively consumed by enzymes.50 Surprisingly, root dry mass pests but the grain itself. One way is by reinforcement of 47 increase was more pronounced with bulk TiO2. Rutile the cell wall by deposition of solid silica, and another way J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 8703 The Use of Nanoparticles and Nanoformulations in Agriculture Pestovsky and Martínez-Antonio is by promotion of the biosynthesis of defense compounds, against Alternaria alternata, Botrytis cinerea, Curvularia probably by becoming a ligand of organic metabolites.58 lunata, Macrophomina phaseolina, Rhizoctonia solani and Sclerotinia sclerotiorum between 5–15 mg/plate of 3.2. Sulfur Nanoparticles potato dextrose agar.68 The homemade silver nanoparti- Two types of sulfur nanoparticles caused dose-dependent cles at 3 ppm were more active against Alternaria sp., reduction of Aspergillus niger growth at concentrations Aspergillus niger, Botrytis cinerea, Penicillium expan- between 125–2000 ppm. For Fusarium oxysporum an sum and Rhizopus sp. than the commercially available 69 inhibitory effect was observed at concentrations between ones (size not given). Silver nanoparticles inhibited 25–200 ppm. In all the cases the effect of sulfur nanopar- hyphal growth of fungal phytopathogens Colletotrichum ticles on the fungi exceeded that of sulfur microparticles.59 coccodes, Monilinia sp., and Pyricularia sp. at 2 mM 70 Minimal inhibitory concentrations of orthorhombic and and4mM. Other silver nanoparticles inhibited the 71 monoclinic sulfur nanoparticles against Aspergillus niger growth of Fusarium oxysporum at 8 g/ml. In another were achieved at 37.632 and 2304 g/ml, respectively.60 study, silver nanoparticles inhibited Fusarium oxysporum ∼ 72 Although sulfur nanoparticles are unlikely to release sul- growth at 6 g/well. Silver nanoparticles showed dose- fide ions by spontaneous reduction, their synthesis involves dependent growth inhibition of Phytophthora infestans 73 the use of polysulfides. Therefore some residual sulfide and Phytophthora capsici at 10–30 g/plate. Other sil- ions may be adsorbed onto their surface. They can be ver nanoparticles (concentration not given) showed high released in solution, and their hydrolysis can lead to the activity against Aspergillus terreus and Pseudomonas 74 formation of hydrogen sulfide, a well-known anti-fungal aeruginosa. In a related study, silver nanoparticles exhib- agent. Dose-dependent microbicidal effect (until complete ited dose-dependent growth inhibition against Aspergillus absence of colonies) was presented by hydrogen sulfide spp. and Penicillium spp. between 0.2–2 mg/ml and against 75 on Rhizopus oryzae, Aspergillus niger,andPenicillium Pseudomonas aeruginosa at 100 g/ml. italicum (for two latter species the effect was shown both Antibacterial activity was also demonstrated with other in vitro and on inoculated fruits of Malus domestica, types of silver nanoparticles. For example, antibacterial Actinidia deliciosa, Pyrus bretschneideri Rehd., Citrus effects on Bacillus megaterium, Pseudomonas syringae, sinensis, Citrus reticulata, Lycopersicon esculentum). But Burkholderia glumae, Xanthomonas oryzae and Bacillus thuringiensis (nanoparticle concentration not specified).76 H2S was applied as 150 ml NaHS solution (0.01–2.5 mM) releasing H S by hydrolysis in sealedIP: 192.168.39.211 containers having On: a Sat,Silver 02 Oct nanoparticles 2021 04:35:08 between 0.3–0.75 ppm (20 nm) or 2 Copyright: American Scientificbetween Publishers 0.5–3 ppm (80 nm) exhibited dose-dependent volume of 3 liters.61 Delivered bytoxicity Ingenta toward Nitrosomonas europaea—a bacterium that removes ammonia-derived fertilizers from the soil, oxi- 3.3. Gold Nanoparticles dizing ammonia to nitrite. The toxic effect against Nitro- It was shown that gold nanoparticles (concentration not somonas europaea was attributed to silver ions (they given) were active in vitro against Aspergillus flavus, 77 62 show toxicity between 0.05–1.25 ppm). Dose-dependent Aspergillus niger and Puccinia graminis. Other gold activity against Nitrosomonas europaea was also demon- nanoparticles (concentration not given) were active in vitro strated for other three types of silver nanoparticles against Aspergillus niger and Fusarium oxysporum as between 1–10 mg/liter. After the toxicity test, the bac- 63 well as against E. coli and Staphylococcus aureus. Gold terial cells were found entrapped into the aggregates of nanoparticles displayed activity in vitro against Aspergillus nanoparticles.78 flavus (minimal inhibitory concentration at 0.34 mg/ml) as Silver nanoparticles release ions only by oxidation, the well as against Salmonella typhi, Staphylococcus aureus, anaerobic conditions prevent this process and the nanopar- Vibrio cholerae and HeLa cells. The activity of the ticles did not exhibit toxicity to E. coli even at concentra- 64 nanoparticles was explained by cell damage. tions thousands of times higher than the minimum lethal concentration of silver ions, e.g., up to 158 mg/liter and 3.4. Silver Nanoparticles up to 195 mg/liter for two samples of PEG-thiol-coated Silver nanoparticles caused death of the adult nanoparticles. However, under aerobic conditions the toxi- hematophagous flies Hippobosca maculata between city of nanoparticles to E. coli was exactly equal to that of

5–25 mg/liter and of cattle ticks Rhipicephalus (Boophilus) AgNO3 solutions, having the same concentrations of silver microplus between 5–25 mg/liter.65 In other study it was ions (∼50–300 g/liter).79 also reported that silver nanoparticles had dose-dependent The anti-fungal effect of silver nanoparticles could also activity against the larvae of Rhipicephalus (Boophilus) be due to the release of silver ions. Silver nitrate inhibited microplus between 1.25–20 mg/liter.66 the growth of mycotoxigenic strains of Aspergillus ﬂavus Other silver nanoparticles exhibited dose-dependent OC1 in a dose-dependent way between 70–800 g/ml activity against Hippobosca maculata and Haemaphysalis and of Penicillium vulpinum CM1 between 60–800 g/ml bispinosa between 2–10 mg/liter.67 In one additional study, (for ﬁlter-sterilized silver nitrate solutions) or between silver nanoparticles exhibited strong inhibitory activity 80–800 g/ml (for autoclave-sterilized solutions).80

8704 J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 Pestovsky and Martínez-Antonio The Use of Nanoparticles and Nanoformulations in Agriculture

3.5. Ag2O/Ag Nanoparticles Alternaria alternata, Aspergillus flavus, Fusarium solani These nanoparticles at concentration of 50 mg/liter sup- and Penicillium chrysogenum.87 In another study, cop- pressed the growth of Aspergillus niger, Aspergillus flavus per nanoparticles (characteristics not given) were reported and Aspergillus fumigatus on potato dextrose agar plates.81 to be active against two crop pathogenic Aspergillus species.88 Copper nanoparticles had fungicidal activity against Alternaria alternata, Curvularia lunata, Fusar- 3.6. Ag3O4 Nanoparticles Ag O nanoparticles at concentrations between ium oxysporum and Phoma destructiva if applied as a 3 4 89 10–50 g/well displayed toxicity toward Aspergillus niger paper disc containing 20 g of nanoparticles. Another as well as towards Pseudomonas aeruginosa in agar study using copper nanoparticles (concentration not given) plates. It was hypothesized that the antimicrobial effect has demonstrated activity against three crop pathogenic of the nanoparticles was due to their interaction with fungi Fusarium spp. Copper nanoparticles easily oxidize sulfur-containing membrane proteins.82 in the presence of air, but it was concluded that the anti- fungal effect could not be explained by release of copper ions because copper salt solution (concentration not 3.7. Nickel Nanoparticles given) exhibited at least 2 times smaller activity against Nanoparticles of this metal between 5–10 mg/liter were Fusarium spp. than the nanoparticles did. A peak show- active against larvae of two cattle tick species: Rhipi- ing C C stretching in the control FTIR spectrum of the cephalus Boophilus microplus and Hyalomma ana- cetyltrimethylammonium bromide used was reported, i.e., tolicum anatolicum, as well as against three mosquito either the spectrum was misinterpreted or the stabilizer species: Anopheles subpictus, Culex quinquefasciatus,and used contained impurities.90 Culex gelidus. The pesticidal activity of the nanoparticles was about 2 times higher than that of Ni-hydrazine com- 3.10. Copper Oxide Nanoparticles plexes from which the nanoparticles were synthesized.83 CuO nanoparticles inhibited growth of two crop It should be noted that aggregated uncapped nickel pathogenic fungal strains Pythium between 50–500 mg nanoparticles having median particle diameter (i.e., aggre- [Cu]/liter. Citrate at 300 mg/liter caused partial disso- gate diameter) 34 ± 21 m (volume weighed) or 014 ± lution of CuO nanoparticles at pH 5. Copper ions at 009 m (number weighed) and surface area 6.41 m3/g 500 mg [Cu]/liter (total concentrations of ions and remain- at 10 mg/liter completely dissolved in artificial lysosomal IP: 192.168.39.211 On: Sat,ing 02 nanoparticles) Oct 2021 04:35:08 compete with ferric ions for binding fluid (pH 4.5) for 24 hours, and in cell medium (pH 7.4) Copyright: American Scientificwith siderophores Publishers and ferric reductase or divalent metal they released 1–3% of nickel immediately after dissolu- Delivered bytransporter Ingenta coupled with it.91 tion, and the concentration of dissolved nickel remained stable for at least 24 hours. The same dissolution behav- 3.11. Zinc Oxide Nanoparticles ior was shown for aggregated uncapped almost spherical nickel microparticles having median particle diameter ZnO nanoparticles at 50 g/ml were active against 28 ± 034 m (volume weighed) or 13 ± 051 m (num- Aspergillus flavus, Aspergillus niger, Aspergillus fumigatus Fusarium culmorum Fusarium oxysporum 92 ber weighed) and surface area 1.05 m2/g at 10 mg/liter. But , and . The activity of ZnO nanoparticles at 0.1 M against Fusar- other aggregated uncapped nickel microparticles having ium sp. increased with the size of nanoparticles. ZnO pow- median particle diameter 18±026 m (volume weighed) der had the lowest activity.93 ZnO nanoparticles exhibited or 11 ± 075 m (number weighed) and surface area species- and dose-dependent activity between 4–16 mM 2.15 m2/g at 10 mg/liter released 68% of nickel in artifi- against Aspergillus flavus, Aspergillus nidulans94 (potential cial lysosomal fluid for 24 hours, and their dissolution in plant pathogen),95 Rhizopus stolonifer and Trichoderma cell medium was negligible.84 The above-described nickel harzianum that could be used as a fungicide itself, i.e., microparticles at 100 mg/liter in artificial sweat (pH 6.5) the nanoparticles were not specific to pathogenic fungal released less than 2.2% and less than 1% of nickel, respec- species. Their anti-fungal activity exceeded that of bulk tively, for 24 hours.85 ZnO.94 In other study, ZnO nanoparticles had species- dependent effect against Aspergillus flavus, Aspergillus 3.8. Platinum Nanoparticles niger and the bacterium Pseudomonas aeruginosa with Platinum nanoparticles showed remarkable activity at 2, minimum inhibitory concentrations 2–3 g/ml.96 ZnO − − 4, and 8 g/well against two plant-pathogenic fungi (Col- nanoparticles at 1 · 10 3 and 5 · 10 3 M showed dose- letotrichum acutatum and Cladosporium fulvum) but not dependent anti-fungal effect against Botrytis cinerea,and against Phytophthora capsici, Phytophthora drechsleri and this effect was pronounced in the presence of light.97 How- 86 Didymella bryoniae. ever, the anti-fungal activity of other ZnO nanoparticles between 50–250 ppm against Aspergillus niger and Fusar- 3.9. Copper Nanoparticles ium oxysporum was found to be slightly higher under light Copper nanoparticles between 20–100 mg/liter exhib- conditions compared with that in the dark, and at 500 ppm ited dose-dependent and species-dependent activity against there was no significant difference. The anti-fungal effect

J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 8705 The Use of Nanoparticles and Nanoformulations in Agriculture Pestovsky and Martínez-Antonio of the nanoparticles against Aspergillus niger and Fusar- activity. The activity was also demonstrated on an infected ium oxysporum was dose-dependent and exceeded that of potato (Solanum tuberosum) tuber.103 micronized ZnO (characteristics not given) or of other ZnO nanoparticles applied at the same concentrations. 3.15. Reduced Graphene Oxide Nano Sheets The anti-fungal effect may be, at least partially, due to Reduced graphene oxide nano sheets had dose-dependent the release of zinc ions. For example, the concentra- and species-dependent activity against Aspergillus niger tion of zinc ions in the growth medium at pH 5.5–6 and Fusarium oxysporum at concentrations between exceeded 70 M after 72 hours (concentration of nanopar- 1–500 g/ml, although exhibited the same toxicity against ticles not given). The nanoparticles showed minor toxicity the beneficial fungus Aspergillus oryzae.104 to mice between 0.5–2.0 g/kg body weight or between 100–500 g/ml, and their toxicity to human fibroblast 3.16. Chitosan Nanoparticles cells between 12.5–500 ppm was the same as that of Chitosan nanoparticles exhibited dose-dependent activity micronized particles at the same concentrations, i.e., they against Fusarium graminearum between 100–5000 ppm can be considered as biocompatible.98 ZnO nanoparti- in vitro; at 500 and 1000 ppm they also protected cles between 50–500 mg [Zn]/liter reversibly inhibited the infected spikelets of wheat. Bulk chitosan also had the growth of two crop pathogenic fungal strains of Pythium. same anti-fungal effect. Aggregated nanoparticles were In a growth media containing 300 mg/liter of citrate total detected inside the leaf and spikelet cells of the plants dissolution of ZnO nanoparticles at 100 mg [Zn]/liter was sprayed with the nanoparticles, and their size distri- observed, accompanied by pH increase from 5 to 7.9. The bution did not coincide with this of the nanoparticles 105 authors explained the anti-fungal effect by the competition applied. However, the inhibitory effect of chitosan · −3 of zinc ions released from the nanoparticles with ferric nanoparticles and microparticles at 5 10 gperPetri ions for binding siderophores and ferric reductase or diva- dish on Aspergillus parasiticus growth and spore germination in vitro exceeded that of bulk chitosan. The lent metal transporters.91 Conversely, other ZnO nanopar- dependence of anti-fungal activity on the concentrations ticles between 3–12 M exhibited dose-dependent activity of chitosan and sodium tripolyphosphate taken for syn- against Botrytis cinerea and Penicillium expansum,but thesis was attributed to different size and stability of the same solution after filtration had no effect on fungal 99 the particles as well as to the presence of free phos- growth. IP: 192.168.39.211 On: Sat,phate 02 Oct groups 2021 chelating 04:35:08 Ca2+,Fe2+/Fe3+ and Mg2+ ions Copyright: American Scientificand therefore Publishers making them unavailable for fungal cells.106 Delivered by Ingenta 3.12. ZnO@SiO2 Nanoparticles Chitosan-saponin nanoparticles as well as the only chi- These nanoparticles between 500–4000 ppm inhibited tosan ones cross-linked with sodium tripolyphosphate growth of Aspergillus niger and Fusarium oxysporum. and with CuSO4 had species- and dose-dependent activ- The released zinc ions contributed to this anti-fungal ity against Alternaria alternata, Macrophomina phase- response. However, the nanoparticles were nontoxic to olina and Rhizoctonia solani at concentrations between mice.100 0.001–0.1%.107 A dose-dependent activity of the copper- containing chitosan nanoparticles between 0.08–0.12%

3.13. Fe3O4/ZnO/AgBr Nano Composite against Alternaria solani and Fusarium oxysporum was This nano composite reduced the germination capacity of demonstrated in vitro and on infected Lycopersicon escu- spores of Fusarium graminearum and of Fusarium oxyspo- lentum plants. Treatment with 0.08–0.12% nanoparticles 108 rum almost equally. The anti-fungal activity increased with was beneﬁcial for seeds of healthy plants. The anti- nano composite concentration (from 3.33 to 26.66 ppm) fungal effect cannot be explained by the release of cop- and weight ratio of Fe O to ZnO/AgBr (from 1:2 to 1:10, per ions from the nanoparticles because the effect of 3 4 0.1% CuSO was smaller than that of 0.1% nanoparti- the nano composite with latter ratio had poorer magnetic 4 cles, and because only 0.01% CuSO was used during the separability).101 4 preparation of nanoparticles.107 108 The combined activity of 0.1% chitosan in 0.1% acetic acid107 108 and that 3.14. Titanium Dioxide Nanoparticles of 0.1% saponin107 was also smaller than that of the These nanoparticles caused mortality of Rhipicephalus copper-containing chitosan nanoparticles. The nanopar- Boophilus microplus larvae as well as of adults ticles of low molecular weight chitosan grafted with of Haemaphysalis bispinosa. The insecticidal activity oleoyl and cross-linked with sodium tripolyphosphate increased with the nanoparticle concentration in the inter- inhibited the mycelium growth of Alternaria tenuis- val of 4–20 mg/liter102 The dose-dependent activity sima, Botryosphaeria dothidea, Nigrospora sphaerica and of silver doped hollow anatase nanoparticles between Nigrospora oryzae between 0.5–2 mg/ml in a species- 0.02–0.52 mg/plate against Fusarium solani and Venturia and dose-dependent manner. The anti-fungal activity inaequalis depended on fungal species and on the presence of these nanoparticles was equivalent to that of bulk of light. Silver ions released contributed to the anti-fungal chitosan.109

8706 J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 Pestovsky and Martínez-Antonio The Use of Nanoparticles and Nanoformulations in Agriculture

4. NANOPARTICLES AS PESTICIDE 4.5. Ferrihydrite Nanoparticles · CARRIERS Ferrihydrite (5Fe2O3 9H2O) nanoparticles at 1.6 g/liter 4.1. Silica Nanoparticles decreased the phytotoxic effect of the fungicide (80 g/liter Silica nanoparticles etched with NaOH were used to tiabendazole and 60 g/liter tebuconazole) on Hordeum vul- encapsulate the insecticide abamectin. The nanoparticles gare seeds. The dose dependence (0, 1, 5 g/kg) was nonlin- protected abamectin from photolysis.110 In another appli- ear probably because of catalytic fungicide inactivation.118 cation, nanoporous hollow silica nanoparticles were used Ferrihydrite nanoparticles doped with cobalt enhanced the to encapsulate the pesticide avermectin. The maximum effect of a commercial fungicide consisting of tebucona- avermectin amount released in 30% ethanol was about zole (60 g/liter) and tiabendazole (80 g/liter). This was 42% w/w at pH 10.111 Another encapsulation technique shown for immediate application of nanoparticles with the anti-fungal agents (10 liters of 0.06 g/liter solution for employing CO2 supercritical fluid allowed to lengthen the avermectin releasing time from 1.87 to about 27 days 1000 kg seeds) after the treatment of wheat seeds infected (0.4 mg/ml nanoparticles in 40% ethanol). The nanopar- with the phytopathogenic fungi Alternaria, Fusarium and ticles protected avermectin from decomposition under Bipolaris spp. If nanoparticles were doped with aluminum, UV irradiation.112 For the plant growth-retardant unicona- they enhanced the fungicidal effect immediately and sus- 119 zole encapsulated in the hollow silica nanoparticles, in tained until 7 days of storage. In vitro experiments 30% ethanol, the releasing time extended from 3 to 5 days demonstrated that the effect of the above-described fungi- compared with the nanoparticles prepared without using cide at 0.5% and 1% against Alternaria tenuissima conidia carbon dioxide. The root number, root length, shoot and was enhanced at 0.015 g/liter of ferrihydrite nanoparticles root fresh weight of the Oryza sativa seedlings treated or at 0.015 and at 0.06 g/liter of ferrihydrite nanoparticles 120 with encapsulated uniconazole (0.3 or 1.0 mg/liter) were doped with aluminum. all higher than in the case of the preparation containing non encapsulated uniconazole. Nanoparticles at 0.3 mg/kg 4.6. Calcium Alginate Nanoparticles of uniconazole in soil had a better retardation on liber- Pesticide imidacloprid encapsulated in calcium alginate ating time of the active agent, with a more life-extended nanoparticles was less cytotoxic against Vero cells at 5 effective period than its free form.113 and 10 mg/liter if compared to free imidacloprid, but more effective against leafhoppers after 11–15 days of its appli- 121 4.2. Gold Nanoparticles IP: 192.168.39.211 On: Sat,cation 02 Oct as spray2021 (pesticide04:35:08 concentration 0.145 mg/liter). Copyright: American Scientific Publishers Camellia sinensis leaf treated with 250 mg/liter of gold Delivered by4.7. Ingenta Calcium Alginate-Chitosan Nanoparticles nanoparticles, after its treatment with ferbam, was pene- Calcium alginate-chitosan nanoparticles with the encap- trated by both agents, despite the nonsystemic character sulated insecticide acetamiprid were found to be supe- of ferbam. The presence of smaller nanoparticles caused a rior to commercial formulation in terms of controlled more rapid penetration of ferbam into the plant.114 release of the insecticide in soil.122 Paraquat encapsulation in alginate-chitosan nanoparticles decreased its soil 4.3. Silver Nanoparticles sorption (at 50 M of paraquat and soil pH 3.1 or Silver nanoparticles at 100 mg/liter on ketoconazole 3.4) and is therefore expected to greatly improve its discs (30 g/disc) showed synergistic inhibitory activity bioavailability.123 Likewise, prolonged release of imaza- against Aspergillus flavus, Aspergillus niger, Aspergillus pic and imazapyr from alginate-chitosan nanoparticles was tamarii, Aspergillus versicolor, Macrophomina phaseolina shown. The encapsulated herbicides retained their activ- 115 and Penicillium sp. Silver nanoparticles (concentration ity against Bidens pilosa at 400 g/ha in soil, inhibiting its not given) also showed synergistic activity when combined growth, and had reduced cytotoxicity for Chinese hamster with fluconazole discs (10 g/disc) against Phoma glom- cells at 0.05 and 0.1 mg/ml, also showed reduced geno- 116 erata and Trichoderma sp. toxicity to Allium cepa roots at 0.5 mg/ml and displayed reduced negative effect against soil bacteria at 75 g/liter of 4.4. Zinc Oxide Nanoparticles imazapic and at 25 g/liter of imazapyr124 ZnO nanoparticles with the noncovalently immobilized pesticide thiram displayed dose-dependent activity 4.8. Chitosan Nanoparticles between 0.05–2 g/liter against the pathogenic fungus The encapsulation of Zataria multiflora essential oil in chi- Phytophthora capsici. The formation of reactive oxy- tosan nanoparticles cross-linked with sodium tripolyphos- gen species was directly dependent on the presence of phate increased the activity of this oil against the crop nanoparticles. Synergistic anti-fungal effects between sil- pathogenic fungus Botrytis cinerea, when applied between ver nanoparticles and thiram was also observed. The 188–1500 ppm in vitro and at 1500 ppm on strawber- nanoparticles catalyzed the photodegradation of the pes- ries (Fragaria × ananassa). Blank chitosan nanoparticles ticide, thus removing the excess of thiram after the anti- had some anti-fungal activity between 188–1500 ppm fungal process.117 themselves.125 Chitosan nanoparticles with encapsulated

J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 8707 The Use of Nanoparticles and Nanoformulations in Agriculture Pestovsky and Martínez-Antonio

Schinus molle essential oil between 12.5–200 g/ml increased with the molecular weight of the polyethylene oil and 9.3–150.9 g/ml chitosan decreased viability of glycol used.130 131 Aspergillus parasiticus spores in vitro, but the anti-fungal effect of blank chitosan nanoparticles was comparable.126 4.11. Methoxypolyethyleneglycol-Poly(lactide-co- The prolonged release of paraquat127 or imazapic and glycolide) Nanoparticles imazapyr124 from chitosan nanoparticles was shown. The Methoxypolyethyleneglycol-poly(lactide-co-glycolide) nano- encapsulated paraquat caused limp leaf necrosis in Zea particles were used for simultaneous encapsulation of the mays and Brassica sp. (i.e., not in weeds) at concentration pesticides validamycin and hexaconazole, and their pro- of active principle equivalent to 2 kg/ha in soil.127 longed release at nanoparticle concentration of 10 mg/ml Encapsulated imazapic and imazapyr inhibited Bidens was observed. The nanoparticles displayed higher anti- pilosa growth at a dosage equal to 400 g/ha in soil.124 fungal activity compared with the commercial preparation, The encapsulated herbicides had virtually no toxicity for and the percentage of relative inhibition of the growth of Chinese hamster cells between 0.0048–0.12 mg/ml127 or the fungus Rhizoctonia cerealis increased with the time of 0.05 and 0.1 mg/ml.124 Besides, chitosan nanoparticles exposition to nanoparticles, and contrarily, decreased with with 75 g/liter of encapsulated imazapic and 25 g/liter time of exposition to a commercial preparation.132 of imazapyr displayed a reduced negative effect versus soil bacteria.124 Likewise, 0.38 mg/ml of encapsulated 4.12. Nanoparticles of Poly(citric acid)-Poly(ethylene paraquat127 128 or 0.5 mg/ml of encapsulated imazapic and glycol)-Poly(citric acid) with Encapsulated imazapyr displayed a reduced genotoxicity to Allium cepa Titanium Dioxide Nanoparticles 124 roots and between 0.24–2.29 mg/liter of encapsulated Poly(citric acid)-poly(ethylene glycol)-poly(citric acid) paraquat reduced toxicity to Pseudokirchneriella subcapi- linear-dendritic copolymers were demonstrated to self- tata was shown. Genotoxicity of the nanoparticles added assembly to nanoparticles being able to encapsulate at the time of germination to Allium cepa roots and toxic- the pesticide indoxacarb and anatase nanoparticles, ity of the nanoparticles to Pseudokirchneriella subcapitata simultaneously. These nanoparticles gradually released can be further decreased in the presence of 20 mg/liter of the encapsulated pesticide and prolonged its activity 128 aquatic humic substances, respectively. against Glyphodes pyloalis larvae between 0.04–0.4 ppm compared with free indoxacarb between 0.25–4 ppm. 4.9. Polyethylene Glycol NanoparticlesIP: 192.168.39.211 On: Sat, 02 Oct 2021 04:35:08 Copyright: American ScientificThe encapsulation Publishers in the nanoparticles accelerated the The encapsulation of an organophosphate pesticide,Delivered viz. byphotodegradation Ingenta of the pesticide. TiO2 nanoparticles, acephate in polyethylene glycol nanoparticles prevented if present, enhanced indoxacarb activity against Glyphodes its decomposition. The resulting preparation did not pyloalis larvae and its photodegradation.133 have cytotoxicity and oral toxicity activities. In contrast with bulk acephate, its encapsulated form showed 4.13. Nanoparticles of Polyethylene Glycol Grafted concentration-dependent reduction of acetylcholinesterase onto Alkoxyisophthalate activity in treated Spodoptera litura between 180–300 ppm In the case of the pesticide azadirachtin-A (release condi- of encapsulated acephate, and a high rate of mortality of tions: ∼6 mg pesticide in 25 ml water) the best half-release Spodoptera litura and of tea spider mites (Oligonychus- time was shown for nanoparticles of PEG-1800 compared coffeae) was observed. In field conditions, Bemisia tabaci with PEG-600, PEG-900 and PEG-1500. All the poly- reappeared after 5 days, Spodoptera litura and Lipaphis mers had the decanyl radical.134 Nanoparticles with PEG- erysimi—later on 7th day. The nanoparticles in field con- 2000 and the tetradecyl radical containing encapsulated 129 ditions were applied in the form of spray one time. carbendazim were active against the phytopathogenic fungus Rhizoctonia solani (effective dose for 50% inhibition 4.10. Nanoparticles of Polymers of Ethylene 0.41 mg/liter, fiducial limits 0.3629–0.4660).135 Nanopar- Glycol and Isophthalic Acid Methyl Ester ticles with PEG-600 residue and the hexadecanyl radical The nanoparticles of copolymers of polyethylene gly- improved the period of optimum availability of Mancozeb col and isophthalic acid methyl ester with pyrethroid and had better half-releasing time at ∼250 mg of formu- -cyfluthrin were more effective against adult leaf bee- lation in 300 ml water compared with those having longer tle Callosobruchus maculatus forupto30dayscom- polyethylene glycol chains or octyl radical, and with compared with the usual commercial formulations. The mercial formulations. The effective doses for 50% inhibi- lowest effective concentrations of the nanoparticles for tion of Alternaria solani and Sclerotium rolfsii were 172± 50% mortality of Callosobruchus maculatus (1.89, 1.03, 006 and 160 ± 004 mg of the active ingredient/liter, 2.20, 1.58 mg/liter) was dependent on the polymeric respectively (concentrations tested: 1.562–25 mg/liter).136 matrix composition (containing PEG-600, PEG-1000, Carbofuran encapsulated in nanoparticles of polyethy- PEG-1500, PEG-2000, respectively).130 The half-release lene glycol grafted onto decanyloxyisophthalate showed time of -cyfluthrin and its period of optimum availability more positive effect on Lycopersicon esculentum seedlings

8708 J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 Pestovsky and Martínez-Antonio The Use of Nanoparticles and Nanoformulations in Agriculture infected with the nematode Meloidogyne incognita in pot virus incidences. This virus is transmitted by Bemisia and field conditions, compared with commercial formula- tabaci Gennadius, the infestation of which is prevented tion. The nematicidal effect was dose-dependent between by the mentioned formulation. Glycine max treatment with 5–20 ppm with a maximum at 10 ppm and was higher with this formulation has also given one of the highest seed PEG-900 than with PEG-600 nanoparticles.137 The notable yields.143 advantages of the nanoparticles of polyethylene glycol grafted onto alkoxyisophthalate were their self-assembly 4.15. Poly(epsilon-caprolactone) Nanoparticles and spontaneous carbofuran encapsulation when the solu- The encapsulation of atrazine in poly(epsilon- 137 138 tions of polymer and pesticide were mixed together. caprolactone) nanoparticles enhanced the herbicide effect The coating of Glycine max seeds with nanoparticles that on growth of Brassica sp. treated at the concentration differed from the above-mentioned ones only by the rad- of the active principle equivalent to 2.5 kg/ha in soil, ical (dodecanyl instead of decanyl) and contained encap- while making its soil distribution more uniform and sulated thiram at 2.5 g of the active ingredient per kg decreasing its genotoxicity to Allium cepa roots between of seeds increased their germination percentage and field 0.7–56.7 mg/liter atrazine added at the time of germina- emergence, decreased the seed moisture content and seed tion. The encapsulated herbicide was shown to have no infestation by storage fungi, compared with commercial negative effects against Zea mays seeds.144 fungicide preparation, until 6 months of storage. The effect (except on seed moisture content) increased with 4.16. Solid Lipid Nanoparticles the polyethylene glycol chain length for nanoparticles with In one study the characteristics of nanoparticles with PEG-600, PEG-900, PEG-1500 and PEG-1800.139 encapsulated deltamethrin were determined by the con- The half-releasing time and the period of optimum avail- centrations of their components and the homogenization ability increased with the molecular weight of polyethy- 145–147 conditions. These nanoparticles protected encapsu- lene glycol134 135 138 139 (in the case of nanoparticles with lated deltamethrin against direct and indirect photolysis the decanyl radical and the encapsulated carbofuran the (50 g/ml in 2% acetone).145 146 These nanoparticles were maximum was observed with PEG-1500, ∼6 mg of car- 138 found to release encapsulated deltamethrin for 48 hours at bofuran in 25 ml water) and with the hydrophobicity of 146 the alkyl radical.135 1.4% (w/w), or for 72 hours (starting from a solution of 6 mg/g encapsulated deltamethrin).145 At 60 minutes, IP: 192.168.39.211 On: Sat, 02 Oct 2021 04:35:08 the nanoparticles with 1.89%–2.25% deltamethrin could 4.14. Nanoparticles of Polymers of PolyethyleneCopyright: American Scientific Publishers Delivered bypenetrate Ingenta the whole Capsicum annuum L. leaf (70 m Glycol and Diacids 147 ∼ depth). In another study prolonged releasing of the The release of encapsulated thiamethoxam ( 50 mg for- encapsulated herbicides atrazine and simazine at (909 ± mulation in 50 g dried soil) was improved with increasing 070 · 1012 particles/ml was found. These nanoparticles the chain length of polyethylene glycol blocks of the poly- had low cytotoxicity for mouse fibroblast cells between mer used for preparation of the nanoparticles. The release 15.6–62.5 g/ml herbicides. An enhanced effect on the was also improved by polymers with aromatic hydropho- growth of the target plant Raphanus raphanistrum and no bic segments, particularly with oxyisophthalic acid with adverse effects versus Zea mays plants at the concentration PEG-4000. This was the most stable preparation after 14 of 3 kg/ha of herbicides applied in soil or sprayed onto days of storage.140 In the case of imidacloprid, the best seedlings were observed.148 formulation for maximum releasing was suberic acid and PEG-300, the release continued for 30 days at ∼4mg/ml nanoparticles in water, and the maximum amount released 4.17. Nano-Liposomes reached 88%. In the case of commercial formulations of A simplification of insecticide encapsulation technique, imidacloprid, the maximum release was obtained in just 3 leaving only lecithin and the pesticide, lead to the for- days.141 Although for imidacloprid released from Glycine mation of nano-liposomes. The homogenization conditions max seeds previously coated with the nanoparticles (10 g determined the final characteristics of the nanoformu- nanoparticles per kg seed weight; for release study 10 g lations. The encapsulated etofenprox was shown to be seeds were put in 50 ml water) the best half-release time released for 30 days (concentration not given), and the (9 hours) under agitation conditions was shown for suberic liposome aggregation became slower when the liposomes 149 acid and PEG-1000. Seed germination percentage, seed were coated with chitosan or eudragit EPO. moisture content, length, fresh and dry weight of Glycine max seedlings after 3 and 6 months of seed storage were 4.18. Pesticide Nanoparticles Stabilized with Polymers increased by coating the seeds with the nanoparticles.142 A novel technique of production of nanoparticles, specially The formulation with suberic acid residue and with PEG- for water-insoluble pesticides, consists in a rapid mixing at 1000 at 7.5 g active ingredient per kg of Glycine max seeds 1:1 ratio of pesticide and polymer solutions in the presence had the best activity against stem fly (Melanagromyza of a large amount of water. A multi-inlet vortex mixer sojae Zehntmer) infestation and against yellow mosaic was specially designed for this technique. The possibility

J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 8709 The Use of Nanoparticles and Nanoformulations in Agriculture Pestovsky and Martínez-Antonio of the agricultural use of the nanoparticles consisting of a silica core of the nanoparticles itself. Some dissolution of pesticide and a polymer was not further investigated.150 the nanoparticles was observed, but it was shown not to be the cause of phytotoxicity.154 5. OTHER USES OF NANOPARTICLES IN AGRICULTURE 6.2. Gold Nanoparticles Incubation of roots of Phaseolus vulgaris seedlings with 5.1. Gold Nanoparticles 5 mg/liter of gold nanoparticles caused their penetration The treatment of Allium cepa roots with gold nanoparticles inside the plant cells (except the polyethyleneimine func- increased their mitotic activity. These nanoparticles also tionalized ones). However, no significant phytotoxicity for Gloriosa superba in vitro increased the pollen germination . Phaseolus vulgaris was observed.155 For Raphanus sativus Both effects were observed to increase with the concentra- seeds gold nanoparticles at 24.62 or 49.25 mg/liter were 151 tion of nanoparticles tested; at 10, 100 and 1000 M. also nontoxic.34 Although for Arabidopsis thaliana 150 Moftetra- 5.2. Silver Nanoparticles chloroauric ions in germination medium is a sublethal The treatment with silver nanoparticles, within 3 hours concentration,156 in our opinion, the effects of gold after harvesting, reduced the Asparagus officinalis L. qual- nanoparticles on plants are not only due to gold ions ity deterioration during storage.152 released from them. Gold nanoparticles do easily leach in the presence of a stabilizer of gold ions and a mild 5.3. Titanium Dioxide Nanoparticles oxidant.157 But in the absence of an oxidant the leaching Feeding Bombyx mori larvae with Morus spp. leaves, was not shown. treated with 5 mg/liter of anatase nanoparticles, increased 31.25 nM of gold nanoparticles (core diameter ∼2nm, the mean weight of the cocoons as well as of the cocoon hydrodynamic diameter 6–10 nm, zeta potential +24 ± shell layer. If Bombyx mori larvae were then fed with 5mV,−2 ± 1mV,−17 ± 6 mV for three different sam- leaves treated with 4 mg/liter of the pesticide phoxim, after ples), after their contact with Raphanus sativus seedlings ingestion of nanoparticles, they did not show symptoms of for 5 days, released less than 5 pg gold per mg nanopar- intoxication such as vomiting, cramps, etc.153 ticles to the nutrient solution (pH 5.6, ionic strength 0.003244 M). This was in spite of shaking and stir- IP: 192.168.39.211 On: Sat,ring 02 Oct the 2021 solution 04:35:08 every 2 hours with the intention of 6. PHYTOTOXICITY OF NANOPARTICLESCopyright: American Scientificaerating Publishers it. However, it should be noted that the nanopar- Considering the agricultural applications of nanoparticles,Delivered byticles Ingenta were protected with a thiol monolayer,158 and thi- one should have in mind the possibility of adverse effects ols are strong passivating agents for gold nanoparticles.159 because of their phytotoxicity. Therefore, these nanopar- Additionally, thiols stabilize Au+ ions as well, and ticles must be used carefully to prevent overdosage, and 2-mercaptoethanol did not protect nanoparticles from preliminary experiments in this sense may be required. dissolution.157 Therefore, the concentration of gold ions The main parameters being registered are root and shoot released from non-covalently modified gold nanoparticles, lengths compared with those of untreated plants. e.g., from citrate-capped ones, may be higher, but in our Potential ecotoxicity, a more general problem, should opinion it is still not enough to be the cause of the adverse also be considered. The nanoparticles are expected to physiological effects observed. have negative effects on soils. Their intrinsic anti-fungal and antimicrobial activity may seriously threaten free- 6.3. Silver Nanoparticles living nitrogen-fixing bacteria and disturb natural symbi- Silver nanoparticles (concentration not measured) dis- otic relationships. Some nanoparticles, due to their long played nontoxic or poor phytotoxic effect on Vigna unguic- residence time in cells, may be transferred through food ulata, Vigna mungo, Vigna radiata, Sorghum vulgare webs. It is possible to imagine nanoparticles as miniatur- and Macrotyloma uniflorum. The parameters investigated ized toxic delivery systems, by releasing compounds or were germination time, shoot length, total chlorophyll, reacting against biological molecules at each trophic level chlorophyll a, b and carotene content.160 The treatment without a remarkable loss of toxicity. The nanoparticles of Triticum aestivum seeds with silver nanoparticles at can also interact with natural organic matter affecting their 10 mg/liter caused diminishing of shoot and root length. 16 aggregation state, mobility and bioavailability. Silver uptake by Triticum aestivum at 1 and 10 mg/liter nanoparticles was observed to be dose-dependent. Because 6.1. Silica Nanoparticles the nanoparticles found in roots were smaller than those Although silica nanoparticles penetrated Arabidopsis originally applied, it was concluded that the phytotoxic thaliana roots, it was shown that phytotoxicity observed effect was mediated by silver ions, and even by the com- at 250 and 1000 mg/liter was caused by silanol groups on plete dissolution of nanoparticles followed by secondary the particles surfaces, mainly by changing the pH in the nucleation.161 The formation of silver nanoparticles was growth medium from acidic to alkaline, and not by the indeed shown in Allium cepa var. “Crystal White Wax”

8710 J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 Pestovsky and Martínez-Antonio The Use of Nanoparticles and Nanoformulations in Agriculture bulbs after treatment with 40 mg/liter AgNO3 by foliar were exposed to the nanoparticles via roots. Silver ions spray or after administration of 80 mg/liter AgNO3 dis- exhibited the same phytotoxic or phytostimulatory effects solved in Douglas nutritive solution. The shape of the at these concentrations. In contrast, the exposition of nanoparticles formed was close to spherical or irregu- these plants to PEG alone did not present this stimula- lar, average size was about 500 nm, recorded size var- tory effect. Silver nanoparticles under aerobic conditions ied from ∼300 nm to ∼1000 nm.162 Silver nanoparticles continuously release silver ions, and 10 nm nanoparticles between 0.5–3 mg/liter added to the germination medium exerting higher phytotoxicity for poplars released more caused dose-dependent inhibition of Arabidopsis thaliana silver ions than the 25 nm ones, therefore both effects root elongation and increased roots number. Silver ions were likely mediated by silver ions.172 Lactuca sativa and caused Arabidopsis thaliana root growth inhibition only Cucumis sativus seeds treatments with silver nanoparticles at the highest concentration, 3 mg/liter. The nanoparti- at 100 mg/liter decreased their germination rate and inhib- cles caused more silver accumulation in the leaf compared ited root growth, but the effect was almost undistinguish- 163 with free ions at the same concentration (2 mg/liter). able from this of the solvent alone.28 Silver nanoparticles showed Zea mays seed-germination inhibition at 3.7 and 36.7 mg/liter compared with 500 mg 6.4. Copper Nanoparticles [Ag]/liter for AgNO3. Brassica oleracea seed-germination inhibition was observed between 0.05–73.4 mg/liter of Copper nanoparticles penetrated root cells and inhibited nanoparticles compared with 0.1–200 mg [Ag]/liter for Vigna radiata and Triticum aestivum seedling growths 164 exposed to the nanoparticles between 200–1000 mg/liter AgNO3. Silver nanoparticles at 10 mg/liter inhibited Oryza sativa germination and the growth of germinated via roots. The release of copper ions from the nanopar- 2+ seedlings. The negative effect observed slightly depended ticles was negligible (0.3 mg/liter Cu at 1000 mg/liter on the size of the nanoparticles.165 Between 0.5 and nanoparticles; this concentration was not toxic and even 1 mg/liter, silver nanoparticles caused dose-dependent enhanced plant growth), but the possibility of generation inhibitory effect on the growth of Oryza sativa seedlings. of copper ions inside plant cells, and their possible nega- And oxidative stress was also observed. These nanoparti- tive effect, could not be excluded.173 cles at 1 mg/liter were partially dissolved in the exposure medium used (without plants), releasing 5.815 g/liter of 6.5. Copper Oxide Nanoparticles silver ions after 24 hours.166 IP: 192.168.39.211 On: Sat,Among 02 Oct 21 2021 bacterial 04:35:08 strains isolated from agricultural soil, A proteomic study of Oryza sativaCopyright:irrigated withAmerican sil- Scientific11 showed Publishers no resistance to 1 mg/liter CuO nanoparticles ver nanoparticles at 60 mg/liter revealed the expressionDelivered byin Ingenta vitro,174 among them being Brevibacillus laterosporus, of cellular detoxifying enzymes, as well as the expression having biopesticidal potential against various insects and of modiﬁcation proteins as response to oxidative stress. showing a broad-spectrum antimicrobial activity includ- These nanoparticles also perturbed normal cell metabolic ing this against phytopathogenic bacteria and fungi,175 processes such as the protein synthesis/degradation rate and Pantoea ananatis, an emerging unconventional plant and the apoptosis process. The protein expression patterns pathogen capable of infecting humans.176 But there were were also dependent on the concentration of nanoparticles several strains resistant to higher concentrations. One of 167 applied (30 mg/liter or 60 mg/liter). them could survive even at 25 mg/liter CuO nanoparti- Spherical silver nanoparticles having size of 18.34 nm at cles. It was hypothesized that the toxicity was due to 5 mg/liter caused fragmentation of the cell wall of rice rhi- Cu2+ ions released from the nanoparticles adhered to the zosphere bacteria, penetrated inside the bacterial cells, and cell membrane,174 and the nanoparticles caused membrane transformed bacteria to protoplasts. Some bacterial species damage.174 177 were eliminated completely.168 Ag nanoparticles having a size of 10 nm between 0.12–0.3 mg/liter showed bacteri- 6.6. Zinc Oxide Nanoparticles cidal effect on the beneﬁcial soil bacterium Pseudomonas putida.169 This bacterium can suppress Lycopersicon escu- ZnO nanoparticles inhibited Brassica oleracea seeds ger- lentum foot and root rot caused by Fusarium oxysporum mination at concentrations between 0.01–1000 mg/liter, f. sp. radicislycopersici170 as well as root rot of Lactuca in an increasing dose-dependent way. In contrast, seeds sativa caused by Pythium aphanidermatum and crown and of Zea mays were not affected at any of these concen- root rot of Cucumis sativus caused by Fusarium oxys- trations. On the other hand, the toxicity of ZnSO4,in porum f. sp. Cucurbitacearum.171 Silver nitrate between solution, on these two species far exceeded the effect of 0.2–10 mg/liter caused the same bactericidal effect. In con- ZnO in nanoparticles.164 However, the exposure of seeds trast, bulk Ag (size 44000 nm) between 0.1–10 mg/liter to ZnO nanoparticles at 2000 mg/liter inhibited develop- hadnoeffect.169 ment of roots of Brassica napus, Cucumis sativus, Lactuca Silver nanoparticles having size of 10 nm enhanced sativa, Lolium perenne, Raphanus sativus,andZea mays. poplar (Populus deltoides × nigra) evapotran-spiration at The toxicity of these nanoparticles could not be explained 0.1 mg/liter and inhibited it at 1 mg/liter. The poplars by the zinc ions liberated from nanoparticles because the

J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 8711 The Use of Nanoparticles and Nanoformulations in Agriculture Pestovsky and Martínez-Antonio 154 thaliana Arabidopsis 111 112 110 ide carried Other beneﬁcial Avermectin Avermectin Abamectin on 60 57 IP: 192.168.39.211 On: Sat, 02 Oct 2021 04:35:08 Oryza sativa Copyright:grains American Scientific Publishers Sitophilus oryzae Delivered by Ingenta Aspergillus niger 19 59 113 20 (with Nanofertilizer or Target of encapsulated uniconazole) Fusarium oxysporum Lactuca sativa Lycopersicon esculentum Oryza sativa Aspergillus niger, 1and /g 1 2 /g (after 2 ± 26% 2 ∼ 9mV, 15 nm, /g (after 58.3% 0 2 ∼ ≤ ± 9 /g, pore size 2 cal, stabilized with 31 − 50 nm, mean surface 588 m ∼ 50 nm, 38.04 wt.% S ∼ 10 nm, contain 38.68 wt.% 15 nm, payload ∼ 4and ∼ 3 nm, zeta potential 111 mg/g, surface area ∼ /g (before), 318.62 m 0 2 ≤ 2 /g (before), 237 m ± 2 ± 3 6 20 70 nm, average outside100 diameter nm, pore size 4–5 nm, surface area 20 nm and − respectively encapsulation), payload 4–5 nm, payload 62.5% 291 size 12 nm, surface area 200 m thickness loading 11.31 m ∼ ∼ 567 m surface area hydrodynamic diameter 135 PEG-400, of S; monoclinic: Cylindrical,with stabilized conjugate of SpanTween 80 80, and etching), pore diameter 12with nm, polyvinylpyrrolidone coated 38.68 wt.% and 36.97hydrodynamic wt.% diameters of 20–70 sulfur, nm10–100 and nm, average particle∼ size roughness 5.313 and 3.840respectively nm, Lypophilic and hydrophilic, average particle Functionalized with 3-aminopropyl groups Outside diameter 80–100 nm, average shell 15–20 nm Spherical, average diameter 320 nm, Aggregated, average inner diameter 60–100 nm, shell thickness Uncoated, spherical, 50 nm and 200 nm, Orthorhombic: Spheri The reported uses of nanoparticles in agriculture. 2 Nanoparticle growth plant Pestic type Characteristics stimulating effect Pesticidal effect carried pesticide effects Phytotoxicity Table I. SiO S Stabilized with PEG-400, contain

8712 J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 Pestovsky and Martínez-Antonio The Use of Nanoparticles and Nanoformulations in Agriculture 155 city for Phaseolus vulgaris No phytotoxi- root and 151 Gloriosa pollen 64 Salmonella E. coli 63 , Vibrio , Allium cepa Staphylococcus aureus against Staphylococcus aureus typhi cholerae of against cells and superba germination Antibacterial activity Increase mitotic index Antibacterial activity ide carried Other beneﬁcial 114 , ,

IP: 192.168.39.21162 On: Sat, 02 Oct 2021 04:35:08 Copyright: American Scientific Publishers Delivered by Ingenta Aspergillus niger Puccinia graminis Fusarium oxysporum Aspergillus ﬂavus Aspergillus ﬂavus Aspergillus niger, 27 20 26 24 28 Lactuca sativa thaliana Nanofertilizer or Target of Brassica juncea Cucumis sativus, Arabidopsis Zea mays Lactuca sativa 18, 4 98, 23 mV, 21, ± 66 nm, leaf 2nm, 70 nm, 3 10 1 4 10 1 187 ± 19, 129 ± ± ± ± 20 0 20 nm 03 ± 1 47 34 leaf extract, − 70 ∼ ± juice, spherical leaf extract, 67 29 35 − g/mL, 4 nM) 31 nm, respectively; 01, 24 90, 18 16 mV, respectively; 64, 1 24, 5 1 1 8 14 seed extract, have ± 82, 1346 1 ± ± ± ± 77 ± 29 60 17 00 20 42 ± 19 28 Syzygium cumini Cinnamonum zeylanicum Punica granatum Terminalia arjuna 33 44.3 mV, 62 10 − − 51, 22 − − 90, 19 41, 205 1 74, 70, 215 2 1 ± 21 ± ± ± ± 10 33 83 47 30 22 15 zeta potential 10–20 nm Abelmoschus esculentus hydroxyl, amine and amide groups and triangular, 5–17 nm,and with amide hydroxyl, groups aldehyde spherical, 20–50 nm, average size polyethylene glycol, citrate; primary14, particle 18 size − zeta potential after the experiment broth, triangular with admixture of spherical ones respectively; hydrodynamic size 87 spherical, 24 nm, with hydroxyl groups 1535 respectively respectively; hydrodynamic size afterexperiment the 155 306 − zeta potential Synthesized using Synthesized by the citrate method, near spherical, Synthesized by the citrate method (10 45–75 nm, average size 62 nm, synthesized using Synthesized using Synthesized using Citrate-capped, 30, 50, 69Synthesized nm using Uncoated, coated with branched polyethyleneimine, Ferbam Continued. Nanoparticletype Characteristics stimulating effect growth plant Pesticidal effect carried pesticide Pestic effects Phytotoxicity Table I. SeAu Dodecanethiol functionalized –

J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 8713 The Use of Nanoparticles and Nanoformulations in Agriculture Pestovsky and Martínez-Antonio 34 Raphanus sativus No phytotoxicity for ide carried Other beneﬁcial

IP: 192.168.39.211 On: Sat,, 02 Oct 2021 04:35:08 Copyright: American Scientific Publishers, 70 effect carried pesticide effects Phytotoxicity microplus, Deliveredmicroplus by Ingenta 69 68 sp. sp., sp. 67 65 sp., 66 Boophilus Boophilus Hippobosca maculata larvae Haemaphysalis bispinosa Botrytis cinerea, Curvularia lunata Macrophomina phaseolina, Rhizoctonia solani, Sclerotinia sclerotiorum Monilinia Pyricularia Aspergillus niger, Botrytis cinerea, Penicillium expansum, Rhizopus Rhipicephalus Rhipicephalus Hippobosca maculata Alternaria alternata, Alternaria Colletotrichum coccodes, 34 L. 31 33 32 L. 35 Nanofertilizer or Target of ofﬁcinalis thaliana Borago Triticum aestivum Brassica juncea Raphanus sativus Arabidopsis 2nm extract ± extract extract ;have 400 nm, 74% ∼ leaf extract 220 nm, 17% 15 nm for 5 nm, triangular, ∼ ∼ ± Cryptococcus , 18% Manilkara zapota 7 nm, spherical, 8 ± 35 nm for glucoxylan-capped size 29 nm 10 or 25 nm 47 hydroxyl groups, prepared using Cissus quadrangularis using lateral size 52.4 nm,hydroxyl have groups, prepared using Euphorbia prostrata Acalypha indica supernatant, hydrodynamic size distribution: 13% ∼ laurentii 160 nm, 65% Rhodotorula glutinis hydroxyl and amide groups circular, average size 30–90 nm Irregular shape, 30 nm, Average diameter 25 nm Citrate-capped, 6–42 nm, average Glycoxylan-coated, average size 8, Decahedral, 45 Spherical, mean size 42.46 nm, with Spherical, 70–140 nm, prepared Rod-shaped, 25–80 nm, average 10–50 nm, synthesized using Synthesized using yeast culture Synthesized using cow milk, mostly Continued. Nanoparticletype Characteristics stimulating effect growth plant Pesticidal Pestic Table I. Ag Alginate-capped

8714 J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 Pestovsky and Martínez-Antonio The Use of Nanoparticles and Nanoformulations in Agriculture 74 , Bacillus , , , 76 Xanthomonas oryzae thuringiensis Bacillus megaterium Pseudomonas syringae Burkholderia glumae Pseudomon as aeruginosa Antibacterial activity against Antibacterial activity against , 116 115 , , sp. spp. , , , Trichoderma Aspergillus niger Aspergillus tamarii Aspergillus versicolor Macrophomina phaseolina Penicillium Phoma glomerata Aspergillus ﬂavus ide carried Other beneﬁcial (synergism) IP: 192.168.39.211 On: Sat, 02 Oct(synergism) 2021 04:35:08 Fluconazole Ketoconazole

71 72 Delivered by Ingenta 75 spp. spp., 73 Penicillium Phytophthora capsici Aspergillus terreus Fusarium oxysporum Fusarium oxysporum Phytophthora infestans Aspergillus Nanofertilizer or Target of , , , , Annona ) 27.7 mV, with Psidium guajava Amylomyces Alternaria Tecoma stans , − Calotropis procera Pinus thunbergii , sp. cell free Ficus recemosa , Cymbopogon citratus 14.4– Chrysopogon , cell ﬁltrate, with carboxyl , − culture supernatant Bacillus latex, spherical, 4–25 nm,size average 12.33 nm, haveamino hydroxyl groups and with hydroxyl groups, synthesized using supernatant synthesized using rouxii and commercially available ones, 10–50 nm, circular andsmooth oval edges, with with hydroxyl groups hexagonal, 2–15 nm, withgroups, hydroxyl synthesized using Lactobacillus rhamnosus exopolysaccharide potential 20–60 nm, average sizesynthesized 32.5 using nm, alternata groups and adsorbed nitrate ions cone extract, average sizemostly 5–50 triangular nm, and hexagonal, have hydroxyl and carboxyl groups squamosa zizanioides Delonix regia adsorbed nitrate ions, synthesized using 10 plant extracts ( Mangifera indica Syzigium cumini Ziziphus mauritiana Synthesized using Predominantly spherical, 7–21 nm, Average size 27 nm or 20 nm, Synthesized using peanut shell extract Mostly spherical, triangular, rod and Hydrodynamic size: 26–51 nm, zeta Spherical, appear aggregated, Synthesized using Continued. Nanoparticletype Characteristics stimulating effect growth plant Pesticidal effect carried pesticide Pestic effects Phytotoxicity Table I.

J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 8715 The Use of Nanoparticles and Nanoformulations in Agriculture Pestovsky and Martínez-Antonio 160 172 , 163 nigra Vigna , , 161 × 165 166 167 164 Vigna radiata , 28 sativa mungo Sorghum vulgare Macrotyloma uniﬂorum Zeamays Cucumis sativus, Lactuca Vigna unguiculata Oryza sativa Triticum aestivum Arabidopsis thaliana Oryza sativa Populus deltoides Oryza sativa Brassica oleracea, 152 79 77 78 E. coli against Nitrosomonas europaea against Nitrosomonas europaea against Antibacterial activity Antibacterial activity Antibacterial activity Crop preservative ide carried Other beneﬁcial

IP: 192.168.39.211 On: Sat, 02 Oct 2021 04:35:08 Copyright: American Scientific Publishers Delivered by Ingenta Nanofertilizer or Target of 6 nm, zeta 39.2 mV, in 0 − ± cell ﬁltrate 5 1mV 2 7 nm, average zeta 15–25 nm, containing 0 4 ± ∼ 10 nm, size range 3 nm, coated with 1 ± ∼ ± 0 17 25.13 mV, stable in 5mV;10 8 nm, hydrodynamic − − 0 5 nm, hydrodynamic diameter 13 ± 2 nm, zeta potential 14 nm, coated with adenosine 5 ± 11 50 mV 3 nm, coated with adenosine 0 1 ± ± 13 ± ± 2 − potential buffer, 20 nm, 80 nm polyvinyl alcohol; average size 7 triphosphate disodium; average size 40 triphosphate disodium mean diameter 1.5 ml glycerol per 100 ml Lecanicillium lecanii 5–15.5 nm, coated with PVP also present; 2–14 nm 56 using sucrose without additional stabilizers ∼− amorphous carbon-coated, 25 nm, prone to aggregation diameter 11 potential 2.64 mM NaBH 33.8 nm, zeta potential moderately hard water 7 Spherical, stabilized by 2 mM phosphate Average size 7 4 Polyvinylpyrrolidone-coated, 0.06 mg/L Spherical, 1.6 nm, synthesized using Mean size 13.2 nm, 70% have size Almost spherical, but irregular shapes Citrate-coated, non-spherical, 20, 30–60, 70–120 and 150 nm, prepared Average size 20 nm, zeta potential Spherical, 18.34 nm Stable, PEG-thiol-coated, 10 nm; 29 Continued. type Characteristics stimulating effect Pesticidal effect carried pesticide effects Phytotoxicity Nanoparticle growth plant Pestic Table I.

8716 J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 Pestovsky and Martínez-Antonio The Use of Nanoparticles and Nanoformulations in Agriculture 173 , 37 Triticum aestivum Vicia sativa Phaseolus radiatus 175 and 174 177 174 82 Pseudomonas including beneﬁcial Brevibacillus laterosporus against aeruginosa Pantoea ananatis 20 more strains, Antibacterial activity Antibacterial effects ide carried Other beneﬁcial

IP: 192.168.39.211 On: Sat, 02 Oct 2021 04:35:08 87 Copyright: American Scientific Publishers 86 81

Delivered by Ingenta , 89 , , , , 88 90 sp. 91 sp. sp. Aspergillus ﬂavus, Fusarium solani, Penicillium chrysogenum Curvularia lunata Fusarium oxysporum, Phoma destructiva Aspergillus ﬂavus Aspergillus fumigatus Colletotrichum acutatum Aspergillus niger Alternaria alternata Aspergillus Pythium Aspergillus niger Fusarium Alternaria alternata, Cladosporium fulvum 36 38 20 37 Nanofertilizer or Target of Triticum aestivum Vicia sativa Helianthus annuus Triticum aestivum Lactuca sativa /g 2 surface 53.8 mV, 169 + 179 ) gum, with 1mV – – 2 70 nm (mostly 2 nm, contain > ± ± yedoensis 0 10–17 nm ∼ × /g 2 5nmand 350 nm) to 450 nm, Prunus size 10–50 nm, synthesizedYoshino using cherry tree ( charge 38 small amounts of metallic silver capped with cetyltrimethylammonium bromide 25 m hydrodynamic diameter 46 nm, capped with cetyltrimethyl ammonium bromide agglomerating to particulates < > hydroxyl groups 18.72 nm 20–30 nm, surface area up to Mean size 8 nm, uncapped Capped with Tween 80 Spherical, 3–10 nm, average 3–30 nm, zeta potential Several dozens of nm Mostly round and spherical, 33 nm, Spherical, Continued. 4 O/Ag Spherical, 34 O 2 3 Table I. Ag Ag Cu – CuO 25 nm, surface area up to 25 m Pt Mostly spherical and oval, average Nanoparticle growth plant Pestic type Characteristics stimulating effect Pesticidal effect carried pesticide effects Phytotoxicity

J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 8717 The Use of Nanoparticles and Nanoformulations in Agriculture Pestovsky and Martínez-Antonio , , 94 , 97 96 Listeria , Staphylococcus aureus Serratia marcescens Proteus mirabilis Citrobacter freundii Pseudomonas aeruginosa E. coli monocytogenes Antibacterial activity against Antibacterial activity against Antibacterial activity against ide carried Other beneﬁcial

IP: 192.168.39.211 On: Sat, 02 Oct 2021 04:35:08 , , Copyright: American Scientific Publishers 92 , ,

Delivered by Ingenta, Fusarium , , , 83 Boophilus Hyalomma 93 98 , sp. microplus anatolicum anatolicum Anopheles subpictus Culex quinquefasciatus Culex gelidus oxysporum Aspergillus nidulans Rhizopus stolonifer Trichoderma harzianum (can be a beneficial fungus) Aspergillus niger Aspergillus niger, Aspergillus fumigatus, Fusarium culmorum, Fusarium oxysporum Rhipicephalus Aspergillus niger Fusarium Aspergillus flavus Aspergillus flavus Botrytis cinerea Aspergillus flavus, 42 20 41 Nanofertilizer or Target of Lactuca sativa Vigna radiata 13.6 leaf − ,58nm sp. leaf Aloe -Mn, 188 4 nm, with ionized 44 nm, 0 13 ± ± 0.60 mV, at pH 9 5 − 2 nm, synthesized using 88 ± 5 nm (more active), 20 200 nm, contained nonionic 30–40 nm, zeta potential at 101 ± polygonal, cylindrical and spherical, capped with Tween 80 84 ∼ 2.34–3.80 nm; uncapped, 28 nm broth extract (40 nm)chemically or (25 nm) Aeromonas hydrophila ∼ dispersant and 0.9% NaCl hydroxyl and amino groups, average size 15–20 nm, hydrodynamic radius ∼ pH 3 Parthenium hysterophorus extract, had amino andgroups enolic hydrodynamic radius ∼ carboxyl and hydroxyl groups, stable in water mV; other type: mightnanorods be (diameter 30–40 nm, length 300–400 nm) or nanoprisms with unclear characteristics 70 nm, average aggregate size Capped with natural surfactant, Synthesized using Synthesized from bulk ZnO by ∼ Nearly spherical, with carbonyl, Continued. type Characteristics stimulating effect Pesticidal effect carried pesticide effects Phytotoxicity Nanoparticle growth plant Pestic Table I. PdMn Aluminum hydroxide embedded Cubic-shaped, Ni Spherical, 150 nm, irregular ZnO 27

8718 J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 Pestovsky and Martínez-Antonio The Use of Nanoparticles and Nanoformulations in Agriculture , Zea , , 118 Lactuca sativa 180 , 164 178 mays sativus Lolium perenne Raphanus sativus mays Brassica oleracea, Zea Hordeum vulgare Brassica napus, Cucumis Zea mays 120 spp. on Bipolaris, , 119 capsici tenuissima Fusarium Triticum aestivum seeds Phytophthora Alternaria Alternaria ide carried Other beneﬁcial 117 tiabendazole (synergism) (decrease phytotoxicity) Tebuconazole/ Tebuconasole/tiabendazole IP:Thiram 192.168.39.211 On: Sat, 02 Oct 2021 04:35:08 Copyright: American Scientific Publishers

Delivered by Ingenta, , 100 99 91 sp. Fusarium oxysporum Penicillium expansum Aspergillus niger Pythium Botrytis cinerea 45 Nanofertilizer or Target of Arachis hypogaea 169 179 /g, zeta /g, 2 2 9mV(in 7mV(in 70 nm 5mV > 15 20 2 + + ± 15 nm, contain 7 7 nm, average ± 5nm, 0 13.21 mV < − ± 5 mV, with hydroxyl 0 350 nm) to 450 nm, ∼− 99.5% > > 9 nm, hydrodynamic 4 5 nm, surface area 58 m ± 4 ± diameter 11 zeta potential and carbonyl groups, stableneutral at pH, unstable at0.2–0.4 pH M 3 KCl or in particles, 50–70 nm, agglomerating to particulates (mostly embedded above 4–5 nmspherical shell grape in like nanosilica matrix, 20–40 nm, pore3.1 size nm, surface area 849 m 10–50 nm, average size 20 nm purity doped with cobalt or aluminum surface charge 55 potential adispersant anti-fungal system), deionized water) 17 Generally ﬂattened ellipses, few round Mostly rod-like, 70 17 nm, surface charge 20 Spherical ZnO nanoparticles Maghemite, mostly spherical, Undoped or doped with aluminum Undoped 2–5 nm, synthesized by bacteria, Citrate-capped Continued. · 3 3 O 2 O 2 2 O 2 9H SiO ferrous oxides -Fe Nanoparticle growth plant Pestic type Characteristics stimulating effect Pesticidal effect carried pesticide effects Phytotoxicity Table I. ZnO@ 5Fe Ferric and

J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 8719 The Use of Nanoparticles and Nanoformulations in Agriculture Pestovsky and Martínez-Antonio 28 , 181 178 182 Lactuca sativa L. Zea mays Cucumis sativus Vicia narbonensis Zea mays 153 productivity increase, phoxim antidote Bombyx mori ide carried Other beneficial , 101 Solanum Venturia on effect carried pesticide effects Phytotoxicity Boophilus IP: 192.168.39.211 On: Sat, 02 Oct 2021 04:35:08 tuber; 103 Copyright: American Scientific Publishers102 Delivered by Ingenta Fusarium oxysporum microplus larvae, adult Haemaphysalis bispinosa tuberosum inaequalis Fusarium graminearum Rhipicephalus Fusarium solani 50 47 51 49 48 Nanofertilizer or Target of oleracea Spinacia Spinacea oleracea Triticum aestivum /g, 2 189 /g, purity 2 flower extract 12 nm; g/ml, 330 nM /g ∼ 2 50 nm, < 6 nm, 116 5 :Averagesize 4 ± 51.6 mV 4–6 nm 100 nm O hydrodynamic diameter 208–330 nm, mean 294potential nm, 7.57 zeta mV (129.28 hours), mV (24 hours) 3 AgBr: size not given;around distributed ZnO (oval-like, wurtzite form, size not given). Uncapped in 1 M tetramethylammonium hydroxide, zeta potential − volume fraction 1.5%, saturation magnetization 10 kA/m, contain tetramethylammonium hydroxide rutile; average size 21surface nm, area 50 m ∼ average size 160–220 nm,hydroxyl, with aldehyde and amide groups, synthesized using Calotropis gigantea llulose, average particle size 5–6 nm, surface area 174.8 m < 99.9% stabilized with sodium dodecyl benzene sulfonate 57 Average diameter 98 nm, ferrophase 7 Tetragonal, 80% anatase, 20% Rutile Anatase, average grain size Aggregated, unidentified phase, In 0.5% w/v hydroxypropylmethylce Mixture of rutile and anatase, 18 nm, surface area 23 m Almost spherical, Continued. /ZnO/AgBr Fe (hollow, 4 4 3 2 2 O O O silver-doped) 3 3 2 Nanoparticle growth plant Pestic type Characteristics stimulating effect Pesticidal Table I. Fe Fe TiO TiO Al

8720 J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 Pestovsky and Martínez-Antonio The Use of Nanoparticles and Nanoformulations in Agriculture 186 Daucus Cucumis , Brassica , , 185 sativus oleracea carota Zea mays Lactuca sativa 121 124 ide carried Other beneficial 122 123 Imazapic, imazapyr Paraquat Imidacloprid Leafhoppers Acetamiprid , on 106 126 104 IP: 192.168.39.211 On: Sat, 02 Oct 2021 04:35:08 105 Copyright: American Scientific Publishers Delivered by Ingenta graminearum Triticum aestivum parasiticus parasiticus Aspergillus oryzae (not a pest), Fusarium oxysporum Fusarium Aspergillus Aspergillus Aspergillus niger 53 Nanofertilizer or Target of Glycine max m; 4nm 30 mV, 1 2% 7 6nm < 3mV, 3 1 ± ∼− /g, purity 2 8 ± 2 ± 3 ± 8 8 7nm, 22 0 − 7nmor 8% (imazapyr) ± 9 2 2 ± ± 168 nm, zeta potential 12 nm, polydispersity index m, with hydroxyl and 7 3 ± ± 45.6 mV 5 6mV 8 nm, zeta potential < m. Spherical. Precipitated with ∼+ 1 2 ± ± 1 2 8 99.6%, uncoated or with 2.83 mg of 10–40 nm, average size 15 32.1 mV, encapsulation efficiency 62% 11 (imazapic), 71 encapsulation efficiency 62 246 > phenanthrene per gram of(10.0% nanoparticles monomolecular layer) ormg/g 28.40 (100.0% monomolecular layer) encapsulation efficiency 74.2%, inCaCl 0.01 M specific surface area 103.0 m hydrodynamic diameter 44 diameter 635 0.518, zeta potential diameter 494 ∼ polyvinyl alcohol, aggregated, payload 2.46%, encapsulation efficiency 98.66% polydispersity index 0.390, zeta− potential diameter 180.9 nm, polydispersity0.31, index bimodal size distribution,potential zeta + with 0.35 and 0.5%1–1000 chitosan: size 2% (w/v) NaOH at pH 7. carboxyl groups 150 nm, capped with surfactant AOT and 13 nm, average aggregate size 201.0 nm, Average diameter 7 Average size 377 Spherical, 197–305 nm, hydrodynamic Prepared with 0.2% chitosan: size Spherical, 20–100 nm, hydrodynamic Lateral size ∼ 30–40 nm, hydrodynamic diameter 201.5 nm, Nearly spherical, mean hydrodynamic Continued. 2 oxide nanosheets nate/chitosan tripolyphosphate type Characteristics stimulating effect Pesticidal effect carried pesticide effects Phytotoxicity Nanoparticle growth plant Pestic Table I. CeO Hydroxyapatite Carboxymethylcellulos estabilized, Reduced graphene Calcium alginate Calcium algi- Chitosan/sodium

J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 8721 The Use of Nanoparticles and Nanoformulations in Agriculture Pestovsky and Martínez-Antonio on 125 ) 124 126 Brassica , (not weeds) 127 ananassa Fragaria × parasiticus strawberries ( sp. Aspergillus Bidens pilosa Botrytis cinerea Zea mays ticide carried beneﬁcial 128 essential oil essential oil Schinus molle Paraquat Imazapic, imazapyr Zataria multiﬂora Paraquat 108 , , Solanum effect carried pesticide effects Phytotoxicity on Mill Fragaria Rhizoctonia Rhizoctonia Rhizoctonia 125 on ) , , ,

107 IP: 192.168.39.211 On: Sat, 02 Oct 2021 04:35:08 107 107 Copyright: American Scientific Publishers ananassa Macrophomina phaseolina solani Macrophomina phaseolina solani oxysporum Lycopersicon strawberries ( × Macrophomina phaseolina solani Delivered by Ingenta Alternaria alternata Alternaria alternata, Alternaria solani, Fusarium Alternaria alternata Botrytis cinerea Nanofertilizer or Target of Other Lycopersicon Mill Solanum 5% 5 5mV ± > 6 300 nm, ∼ 3nmor 22.6 mV 31 mV 88 mV 45.33 mV 26 mV (with + 52 + + + + 5 nm, zeta potential ± 7 6 ± 420 nm (dried), 05 nm, zeta potential 7 nm, zeta potential ∼ 5 nm, polydispersity index 1 nm, polydispersity index 2 nm, polydispersity index 2 nm, polydispersity index 00 nm, zeta potential 77% 74 mV 30 1mV 5% (imazapic), 69 1 mV, encapsulation 2 4 10 2 8 1 0 1 ± 0 4 0 13 nm, zeta potential ± ± ± ± ± ± ± ± ± ± ± 9 5 2 03 4 3 ± 1 93 2 6 66 8 9 15 mV (blank), 1.0, zeta potential 0.5, zeta potential 0.33, zeta potential 282 diameter 200.8–990.6 nm, mean hydrodynamic diameter 373 + 233 + 150.1–390.2 nm, mean 192 0.6, zeta potential 96 53 174 diameter 754 hydrodynamic diameter diameter 180.0–487.9 nm, mean hydrodynamic diameter 196 mean hydrodynamic diameter 374 (imazapyr) pesticides), encapsulation efficiency 58 polydispersity index 0.20–0.35, encapsulation efficiency 62 67 efficiency 45.24%, payload 9.05%, no coating Average hydrodynamic diameter Spherical, hydrodynamic diameter Average hydrodynamic diameter Average hydrodynamic diameter Spherical, 200–600 nm, hydrodynamic Average size Average size 478 Polyhedron shaped, hydrodynamic Nanoporous, mean diameter 150 nm, Continued. 4 tripolyphosphate/ CuSO type Characteristics stimulating effect Pesticidal Nanoparticle growth plant Pes Table I. Chitosan/sodium Chitosan-saponin Smooth-rounded, hydrodynamic

8722 J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 Pestovsky and Martínez-Antonio The Use of Nanoparticles and Nanoformulations in Agriculture 130 137 on L. 132 133 135 Lipaphis , 129 136 Solanum Lycopersicon rolfsii erysimi, Spodoptera litura and tea spider mitesRicinus on communis leaves Meloidogyne incognita Rhizoctonia solani Callosobruchus maculatus Rhizoctonia cerealis Alternaria solani, Sclerotium Glyphodes pyloalis Bemisia tabaci 134 131 ide carried Other beneﬁcial 130 hexaconazole -cyﬂuthrin Azadirachtin-A Carbofuran Carbendazim Validamycin, Mancozeb Indoxacarb Nigrospora

, IP: 192.168.39.211 On: Sat, 02 Oct 2021 04:35:08

109 Copyright: American Scientific Publishers Delivered by Ingenta Botryosphaeria dothidea, Nigrospora sphaerica oryzae Alternaria tenuissima, Nanofertilizer or Target of 138 138 encapsulation m in width, 192 2 – kDa, ∼ 4 may be stabilized with 10 stable, encapsulation · 191 4 190 7 nm, covered with polyvinyl 3 m in length, payload at pH 7 ± 3 efficiency 96.82%, payload 9.68% efficiency 23.5% (validamycin), 6.9% (hexaconazole), payload 1.94%, mass ratio 40/1/1 (polymer atplace) the first 12 nm (with anatase),self-assemblies formed tubular gyration 85.1 nm, polymerweight molecular 4 13.00–87.24 nm, encapsulation efficiency 95.5%, payload 19.1% 17.85 nm, and PEG-900: 19.4 nm 30 45%, 37% (with anatase),50%, at 47% pH (with 10 anatase).4–10 Anatase: nm, glycerol 297 nm 38.75 nm, and PEG-1500: 29.6 nm alcohol, Semi-spherical, average size 10 nm, PEG-2000 and tetradecyl: radius of PEG-600 and hexadecanyl: Decanyloxyisophthalate and PEG-600: Stable, almost spherical, mean diameter 269 Decanyl radical and PEG-1800: 2 Continued. weight chitosan grafted with oleoyl and cross-linked with sodium tripolyphosphate glycol and isophthalic acid methyl ester glycol-poly(lactide- co-glycolide) acid)-poly(ethylene glycol)-poly(citric acid) linear- dendritic copolymers/TiO grafted onto alkoxyisophthalate Table I. Low molecular Polyethylene glycol 80–120 nm, irregular shapePolymer of ethylene Methoxypolyethylene Poly(citric Polyethylene Acephate glycol Nanoparticle growth plant Pestic type Characteristics stimulating effect Pesticidal effect carried pesticide effects Phytotoxicity

J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 8723 The Use of Nanoparticles and Nanoformulations in Agriculture Pestovsky and Martínez-Antonio , , 139 , , , Glycine spp., seeds spp. on Bemisia tabaci 144 sp. 143 Zehntmer, Gennadius and yellow mosaic virus on max Aspergillus niger Curvularia lunata Dreschlera halodes Fusarium moniliformae Cladosporium Penicillium Glycine max Alternaria alternata Melanagromy za sojae Brassica 143 140 145 146 141 142 ide carried Other beneficial Deltamethrin Thiram Imidacloprid Imidacloprid Atrazine Deltamethrin Thiamethoxam effect carried pesticide effects Phytotoxicity IP: 192.168.39.211 On: Sat, 02 Oct 2021 04:35:08 Copyright: American Scientific Publishers Delivered by Ingenta 142 seeds Nanofertilizer or Target of Glycine max Glycine max 30 − 2%, 5nm < 1 2 200 nm 50 mV ± ± ∼ 26 mV, 7 5 ∼− 60%, payload − > 230 nm 23– ∼ 140 nm (uncoated), 141 40 mV − ∼ ted), polydispersity + > 1 nm, polydispersity 30 mV (chitosan-coated), 91 ∼+ ± 10% 0 ∼ 0.2, zeta potential 16 nm (blank), 408 > 0 40 mV (lignosulfonate-coated), ± 20% 160 nm (chitosan-coated), 0.2, zeta potential 200 nm (uncoated), 1 ∼ ∼− encapsulation efficiency (uncoated), (lignosulfonate-coa index parentheses: PEG-600 (29.21 nm), PEG-900 (29.46 nm), PEG-1500 (33.60 nm), PEG-1800 (62.60payload nm), 127.5 nm, encapsulation efficiency 78.32%, payload 7.12% 174.9 nm, encapsulation efficiency 81.4%, payload 7.4% Hydrodynamic size ∼ size 371 (with atrazine), polydispersity index ∼ Almost spherical, hydrodynamic size ∼ (chitosan-coated), encapsulation efficiency 95%, payload 12.5% protected with polyvinyl alcohol,for stable 90 days mV (uncoated), encapsulation efficiency 92 (chitosan-coated), zeta potential index 0.633, encapsulation efficiency 86.25%, payload 8.4% Dodecanyl radical, radii of gyration in Suberic acid and PEG-300: micelle size Suberic acid and PEG-1000: micelle size Components: corn oil, lecithin, Tween 80. Oxyisophthalic acid and PEG-4000: micelle 365 Continued. ethylene glycol and diacids caprolactone) Nanoparticle growth plant Pestic type Characteristics stimulating effect Pesticidal Table I. Polymers of Poly(epsilon Solid lipid Components: beeswax, lecithin, Tween 80.

8724 J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 Pestovsky and Martínez-Antonio The Use of Nanoparticles and Nanoformulations in Agriculture 148 raphanistrum Raphanus 147 ide carried Other beneﬁcial 149 150 Etofenprox Bifenthrin Deltamethrin Atrazine, simazine

IP: 192.168.39.211 On: Sat, 02 Oct 2021 04:35:08 Copyright: American Scientific Publishers Delivered by Ingenta Nanofertilizer or Target of 5 0 2 0 ± 1nm 5 35 nm, ± 4 1 0 5mV 120 nm, ± 37 ± 7nm 0 5 ∼ − 2 8nm 2 ± 3mV 0 1 ± 0 0 ± 3 nm (blank), ± 0.2, average zeta 3 4nm 5 7% (uncoated), 02% (atrazine), 2 < 1 0 0 ± 28 ± 3 ± ± 300 nm (blank), + 5 ∼ 8% 7% 12% (uncoated), 29% (chitosan-coated) 15 mV, encapsulation 01 nm, after 120 days 5% (chitosan-coated), payload 05% (simazine) 4 mV (uncoated), 40 90% 0 0 008, zeta potential − 3 1 0 0 > 0 1 nm (with herbicides), ± ± 7 nm (uncoated), 254 ± ± ± ± 3 ± 1 8 43 ± ± 3% 07% 16% 3% 53 280 nm (with herbicides), 7 180 (eudragit EPO), encapsulation efficiency 93.2%, etofenprox to lecithin ratio 1:3 mV (chitosan-coated), 44 (eudragit EPO), zeta potential − (chitosan-coated), 206 polydispersity index 0.1, aggregated, payload and polybutylacrylate: radius mV (uncoated), (chitosan-coated), encapsulation efficiency 97 82 23 20 (uncoated), 143 (chitosan-coated), polydispersity index 0 after 120 days 255 ∼ polydispersity index potential hydrodynamic diameter 272 Hydrodynamic size 129 polyvinyl alcohol. Deformed spherical, average size 111 178 97 efficiency 89 With block copolymer of polyacrylic acid Components: corn oil, lecithin, Tween 80. Components: glycerol tripalmytate, Continued. polymers Nanoparticle growth plant Pestic type Characteristics stimulating effect Pesticidal effect carried pesticide effects Phytotoxicity Table I. Nano-liposomes 155 Pesticide with

J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 8725 The Use of Nanoparticles and Nanoformulations in Agriculture Pestovsky and Martínez-Antonio supernatant or an equimolar zinc solution was non-toxic in NaCl solutions, if pH is less than 3 or more than 8. 178 for these roots. For TiO2 nanoparticles with solution characteristics: dis- ZnO nanoparticles, prepared at 7 and 10 mg [Zn]/liter, solution area 40 m2 in 100 ml, pH 1.5, 0.001 or 0.01 M generally were flattened ellipses with only few round par- NaCl, and particle characteristics: size 28.3 nm, surface ticles, and agglomerated in water to form polydisperse area 55.7 m2/g, 86% anatase, 14% rutile, the concentration particulates in a broad size range from 5 nm to 450 nm of titanium ions in the solution rapidly reaches 5.5 M, (although mostly distributed around 350 nm169 and having but then it decreases very rapidly to less than 1 M.184 surface charge of 557 ± 25mV179). These nanoparticles showed bacteriostatic effect on the beneficial bacterium 6.9. Alumina Nanoparticles Pseudomonas putida in vitro. As comparison, zinc nitrate Al2O3 nanoparticles at 2000 mg/liter inhibited Zea mays at 1 and 10 mg [Zn]/liter caused the same effect. Inter- root elongation but did not affect the root elongation of estingly, the same ZnO nanoparticles at 1 and 5 mg Brassica napus, Cucumis sativus, Lactuca sativa, Lolium [Zn]/liter, bulk ZnO (size less than 1000 nm) between perenne and Raphanus sativus plants grown from treated 0.01–10 mg [Zn]/liter and zinc nitrate at 0.05 and 0.1 mg seeds.178 However, root growth of Zea mays, Cucumis [Zn]/liter, showed beneficial effect on Pseudomonas putida sativus, Brassica oleracea and Daucus carota seedlings 169 instead. exposed to other alumina nanoparticles at 2 mg/ml was inhibited. When the surface of the nanoparticles was 6.7. Iron Oxide Nanoparticles covered with noncovalently immobilized phenanthrene, The treatment of Zea mays seedlings with ferrofluid (fer- it was found to significantly reduce their phytotoxicity to ric and ferrous oxides, concentration not given) caused Cucumis sativus. Accordingly, an equivalent concentration detrimental effects on their growth.180 On the contrary, of 0.28 mg/ml of phenanthrene alone was found to be another type of ferrofluid, consisting of nanoparticles, had nontoxic.185 This work did not discuss the increased sol- a stimulating effect on the growth of Zea mays plantlets ubility of nanoscale alumina and did not characterize the at 0.01 and 0.05 ml/liter, while having an inhibitory concentration of aqueous aluminum species, although the 181 40 effect at higher concentrations (0.1–0.25 ml/liter). Fe3O4 phytotoxicity effect had been well documented. nanoparticles produced an inhibitory effect on the germination index and root elongation of Cucumis sativus 6.10. Cerium Dioxide Nanoparticles and Lactuca sativa, but the rootIP: weight 192.168.39.211 was increased, On: Sat,CeO 02 Octnanoparticles 2021 04:35:08 at 2000 mg/liter had toxic effect only therefore the development of thickerCopyright: roots was American favored. Scientific2 Publishers Delivered byon IngentaLactuca sativa from seven plant species investigated It should be noted that the used solvent (1 M tetramethy- (Brassica napus, Brassica oleracea, Cucumis sativus, Lac- lammonium chloride) alone had the same effect, i.e., the 28 tuca sativa, Lycopersicon esculentum, Raphanus sativus, effect could be merely due to the solvent. Triticum aestivum).186 6.8. Titanium Dioxide Nanoparticles 7. CONCLUSION Treatment with TiO2 nanoparticles lead to DNA fragmentation in the roots of Vicia narbonensis L. The levels Nanoparticles have great potential to improve the agri- of various oxidative stress markers increased in a dose- cultural productivity. In most of literature sources inor- dependent way between 0.2%–4% of nanoparticles.182 ganic nanoparticles are mainly considered. Their wider However, for Avena sativa L. cv. Zlaták a nutrient solu- use compared with the organic ones could be due to tion containing dissolved titanium (in the form of tita- their biological activity (unlike organic nanoparticles, in nium ascorbate) at 2 and 18 ppm displayed strict inhibitory most of cases inorganic nanoparticles are not inert car- effect on plant growth only if ammonium acetate was used riers, and this can lead to synergistic effects, especially as the nitrogen source. However, if calcium nitrate was in the case of pesticidal uses; in many cases they can be used instead of ammonium acetate, titanium had benefi- used directly, i.e., without immobilized active substances). cial effect at 2 ppm but a detrimental effect at 18 ppm. Inorganic nanoparticles also have low degradability. Addi- The following mechanism of action of titanium ions was tionally, inorganic nanoparticles also can be manipulated proposed: the titanium ions bind to biomolecules and dis- just because of their commercial availability (one can pur- place the Mg2+ and Fe2+ ions (and possibly some other chase nanoparticles and immobilize on them the substance cations) which activates detoxification mechanisms; these of interest, although polymeric nanoparticles are usually include increased uptake of the displaced elements, the produced at the time of encapsulation, and moreover, the increased synthesis of chlorophylls, and the increased releasing of the active substance usually begins immedi- activity of nitrate reductase. Nitrate reduction, in turn, ately upon their preparation leading to preparation storage requires increased synthesis of organic nitrogen acceptors. difficulty). On the other hand, the absence of biologi- Therefore, the possible beneficial effect of titanium might cal activity of organic nanoparticles used as carriers in be explained by the hormesis effect.183 Moreover, the tita- some cases can be advantageous; for instance, polymeric nium dioxide nanoparticles can release titanium ions even nanoparticles usually do not require stabilizers that can

8726 J. Nanosci. Nanotechnol. 17, 8699–8730, 2017 Pestovsky and Martínez-Antonio The Use of Nanoparticles and Nanoformulations in Agriculture possess toxicity; several agents can be easily encapsulated .massey.ac.nz/∼flrc/workshops/13/Manuscripts/Paper_Bishop_2_ simultaneously; inorganic nanoparticles can also be encap- 2013.pdf. sulated inside the polymers for a better retardation effect; 8. W.H.DeJongandP.J.A.Borm,Int. J. Nanomed. 3, 133 (2008). 9. P. A. Revell, Nanotechnol. Perceptions 2, 283 (2006). if biopolymers (e.g., alginate) are used, the resulting par- 10. R. J. B. Peters, H. Bouwmeester, S. Gottardo, V. Amenta, M. Arena, ticles are more eco-friendly than the inorganic ones. P. Brandhoff, H. J. P. Marvin, A. Mech, F. B. Moniz, L. Q. Pesudo, However, whatever the chemical nature of nanoparti- H. Rauscher, R. Schoonjans, A. K. Undas, M. V. Vettori, S. Weigel, cles is, one should remember potential adverse effects, and K. Aschberger, Trends Food Sci. 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Received: 18 May 2017. Accepted: 3 July 2017.

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