Effects of Copper Nanoparticles (CuO NPs) on Crop Plants: a Mini ...

Effects of Copper Nanoparticles (CuO NPs) on Crop Plants: a Mini Review

V. D. Rajput, T. Minkina, S. Suskova, S. Mandzhieva, V. Tsitsuashvili, V. Chapligin & A. Fedorenko BioNanoScience ISSN 2191-1630 BioNanoSci. DOI 10.1007/s12668-017-0466-3

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Author's personal copy BioNanoSci. https://doi.org/10.1007/s12668-017-0466-3

Effects of Copper Nanoparticles (CuO NPs) on Crop Plants: a Mini Review V. D. Rajput 1 & T. Minkina 1 & S. Suskova 1 & S. Mandzhieva 1 & V. Tsitsuashvili 1 & V. Chapligin 1 & A. Fedorenko 1

# Springer Science+Business Media, LLC, part of Springer Nature 2017

Abstract Nanoparticles (NPs) received great attention due to their unique properties and beneficiary applications in various sectors. The rapid growth of NPs production and its abundant uses create additional risks on an anthropogenically modified ecosystem, and consequently on human beings. The main aim of this review article is to explore the possible threats imposed by CuO NPs on cultivated crop plants. We searched PubMed, Google Scholar, and Web of Science portals for the literature review to get latest updated information and developments in the field of toxicity of CuO NPs on cultivated plants. This review article clearly denoted the toxic effects of CuO NPs on cultivated crop plants by inhibiting seed germination, decreases in the shoot and root lengths, reduction in photosynthesis and respiration rate, and morphological as well enzymatic changes. The information is significant to researchers and policymakers to define limits and future prospectives. Keywords Nanoparticles . Plant . Soil . Toxicity . CuO

1 Introduction Increasing production and application of nanoparticles (NPs) in agriculture, absorption on crop plants may contaminate edible materials and consequently impose a threat to human health. Crop plants are essential and play a critical role to provide food materials. In recent years, significant research has been focused on studying the effects of NPs on various * V. D. Rajput [email protected]; [email protected]

1

Academy of Biology and Biotechnology, Southern Federal University, Rostov, Russia

crop plants. Nanoparticles have been applied in the increased number of commercial applications such as electronics, optics, textiles, medicine, catalysts, water treatment, and environmental remediation [1–5]. Based on the core material, NPs can be broadly divided into inorganic and organic. Inorganic NPs are divided into metals [silver (Ag), aluminum (Al), tin (Sn), gold (Au), cobalt (Co), copper (Cu), iron (Fe), molybdenum (Mo), nickel (Ni), indium (In), lanthanum (La), cerium (Ce), selenium (Se), stannum (Sn), titanium (Ti), zirconium (Zr), zinc (Zn)] and metal oxides (Al2O3, CeO2, CuO, Cu2O, In2O3, La2O3, MgO, NiO, SiO2, TiO2, SnO2, ZnO, ZrO2). Metalbased copper oxide (CuO), zinc oxide (ZnO), silver (Ag), titanium dioxide (TiO2), and iron oxide (Fe3O4) are widely used and monitored for their toxic effects on activity, abundance, and diversity of flora and fauna [6, 7]. The Nano-era began in the early 2000s, and global nanotechnology market in environmental applications reached $23.4 billion in 2014 and expected to reach about $25.7 billion by 2015 and $41.8 billion by 2020 [8]. Whereas, global nanocomposite market, in value terms, should reach $5.3 billion by 2021 from $1.6 billion in 2016 [9]. Once released to the environment, nanowastes accumulate in ecosystems and threats to living organisms. The mechanism of NPs uptake by plant roots is not clearly understood. Studies have shown that depending on the size, NPs may enter in plant cell through carrier proteins, ion channels, via fluid phase endocytosis, plasmodesmata transport, or entry may be facilitated through natural organic matter or root exudates and formation of new pores [10]. Under controlled conditions, strong plant growth inhibition was observed for radish (Raphanus sativus), perennial ryegrass (Lolium perenne), and annual ryegrass (Lolium rigidum) by Atha et al. [11]. In crop plants, negative effects were reported including inhibition of seed germination, root and shoot growth, oxidative stress, and biochemical variations. Physicochemical and toxicological activities of NPs

Author's personal copy BioNanoSci.

vary from larger particles of the same nanomaterials [12]. Such variations might be due to the ability of particles that can cross the plant cell membrane. One of the biggest challenges for the definition of risk associated with a nanomaterial release event is the uncertainty regarding how the properties of nanomaterials change once they interact with the environment as well as how the weather conditions affect nanomaterials [13, 14]. Therefore, there is a demand to assess the risks associated with NPs on the ecosystem. Due to increasing interest in NPs influence, a specific attention is addressed to metal and metal oxide NPs, in particular to CuO. This article presents a comprehensive literature review of CuO NPs toxicity on crop plants.

2 Copper Nanoparticles (CuO NPs) Copper is widely distributed in plant tissues and is essential micronutrient for growth and involved in many physiological processes [15, 16]. It is widely used in agricultural industries, cosmetics, coatings, environmental remediation, fungicides, food industry, chemical industry, fuel additives, textile industries, medical industry, paints, plastics, wastewater treatment, and electronics [17]. Copper as an element converts toxic above a threshold level, which depends on the type of crop plants [18]. It is reported that on average 1 kg of dry plant tissue contains approximately 10 mg of Cu [19]. On the one side, it has reshaped current science by being utilized in different industries, but on the other hand, exerted toxic effects on the living systems. Copper is available in two oxidation states Cu1+ and Cu2+. This allows Cu to function as a reducing or oxidizing agent in biochemical reactions. But at the same time, this property makes Cu also potentially toxic as Cu ions which may catalyze the production of free radicals [20, 21], induce oxidative stress [22], and convert as genotoxic substances [23]. Copper NPs appear as a brownish-black powder and reduced when exposed to hydrogen or carbon monoxide which is harmful to humans and dangerous to aquatic life. It is necessary to develop more reliable, eco-friendly, nontoxic techniques to the synthesis of NPs. Various techniques are using for NPs synthesis viz. laser ablation, chemical reduction, milling, and sputtering. This technique, e.g., chemical reduction method, in which various hazardous chemicals are used later, creates additional risks on human health and environment, while other approaches are expensive, and need high energy. However, biogenic synthesis method to produce NPs is eco-friendly and free of chemical contaminants [24]. The biological synthesis of Cu NPs utilizes the plant extracts, enzymes, and microorganisms [25, 26]. The studies included in this review have mostly used commercially available CuO NPs (Sigma Aldrich, Merck etc).

3 Effects of CuO NPs on Crop Plants There are several reports about the toxicity of CuO NPs on plant morphology, germination and quality of produces, and transpiration and translocation in plant tissues (Fig. 1). Recent studies of CuO NPs toxicity showed negative impact on seed germination and plant growth on various crop plants, i.e., lettuce (Lactuca sativa), alfalfa (Medicago sativa), wheat (Triticum aestivum), mungbean (Vigna radiate), kidneybean (Phaseolus vulgaris), maize (Zea mays), cucumber (Cucumis sativus), cilantro (Coriandrum sativum), rice (Oryza sativa), spinach (Spinacia oleracea), onion (Allium cepa), mustard (Brassica juncea), tomato (Solanum lycopersicum), soybean (Glycine max), carrot (Daucus carota), sweet potato (Ipomoea batatas), barley (Hordeum vulgare), cotton-chickpea (Cicer arietinum), radish (Raphanus sativus), and zucchini (Cucurbita pepo). [27–57]. After accumulation, NPs start to affect plant growth by lowering the germination rate, decreasing biomass, reducing the length of roots and shoots, altering the process of photosynthesis and transpiration rate, and enhancing chromatin condensation and lipid peroxidation (Table 1). It was noted that the accumulation and uptake of NPs depend on the concentrations and exposure timing [58]. A recent study conducted by Jain et al. [59] observed differences in NPs phytotoxicity due to differences in size and surface anatomy of seeds and plant species. 3.1 Effects of CuO NPs on Seed Germination Seed germination is the beginning of a physiological process. Seed coat act as a protector for the embryo [60]. Once the seed coat is ruptured, the radicle is the first tissue to direct contact with metals [61]. Zafar et al. [44] investigated that the CuO NPs affected mustard seed germination and seedling growth. The most dominant form of Cu is Cu oxide near the root zone. A hydroponic study conducted by Peng et al. [37] on rice concluded that CuO NPs can be taken by root, transported, biotransformed, and moved into the epidermis, exodermis, cortex, and finally reached to stele; however, it is difficult to pass through the Casparian strip. Studies also available which shows absorbed NPs by roots are not translocated to the shoots may be localized in the epidermis and exodermis, or mechanism is not well understood [62]. An experiment conducted by Zuverza-Mena et al. [36] on nano-CuO, micro-CuO, and ionic Cu reduced more than 50% seed germination of cilantro (Coriandrum sativum) seeds and affected nutritional quality at 80 mg kg−1 in spiked soil. Whereas, the germination rate of rice was slightly affected (7%) at 1000 mg L−1 of CuO NPs compared with control [36]. Shaw and Hossain [38] reported significant inhibition in seed germination below 0.5 mM nano-CuO treatment. Our hydroponic experiment showed that CuO NPs (10,000 mg L−1) inhibited the germination rate and


Fig. 1 Schematic presentation of effect of CuO NPs on plants

retarded the root and shoot length of spring barley (Hordeum sativum distichum) [63]. 3.2 Effects of CuO on Plant Growth and Morphology The toxicity of NPs depends on plant species, growth conditions, exposure time, concentration, type, and size of NPs. It is well noted that the Cu ions in small concentrations are able to stimulate the plant growth and play the role as microelement [58, 60]. Another study shows that excess CuO NPs reduced the uptake of other nutrients such as B, Mo, Mn, Mg, Zn, and Fe [46]. Table (1) showed the effects of CuO NPs on various crop plants. Xiong et al. [64] demonstrated that the most of the CuO NPs were deposited as micrometric aggregates either on the leaf surface or in the stomata and also deformed stomatal aperture similarly as abiotic stress [65], and CuO NPs aggregation could block stomata. The study conducted on irrigation water containing Cu NPs by Singh and Kumar [40] showed reductions in the root and shoot lengths of Spinach (Spinacia oleracea). The foliar application of CuO NPs accumulated in plant leaves and translocated one part to another [66]. Deng et al. [41] revealed that the CuO NPs reduced the growth of onion root tip and showed that root treated with 80 mg L−1 CuO NPs inhibited growth and stopped growth completely after 72 h exposure. The nano and micro CuO reduced the shoot length in cilantro (Coriandrum sativum) grown in soil with the high content of organic matter [36]. Hong et al. [28] also demonstrated similar results in hydroponically grown alfalfa (Medicago sativa). Nair and Chung, [43] found CuO NPs

suppressed shoot-growth, reduced total chlorophyll and carotenoid contents, and shortened primary and lateral roots of Indian mustard (Brassica juncea L). The accumulation of CuO NPs exhibited a disturbed ultrastructure in leaves especially in the photosynthetic apparatus via lowering the number of thylakoids per granum, plastoglobules, and starch content as well as stomatal aperture [39, 66]. Our pot experiments on barley also showed similar findings; accumulations of Cu in roots were observed by transmission electron microscopy (TEM) (Fig. 2) (unpublished data). It is reported that the exposure to Cu NPs reduced 90% biomass of zucchini (Cucurbita pepo) [55], retarded seedling growth of mungbean (Phaseolus radiatus), and wheat (Triticum aestivum) [30]. Copper NPs changed root morphology of wheat grown in sandy soil [49]. Adverse effects on tuber biomass of sweet potato (Ipomoea batatas) were observed in the highest concentration of Cu2+ [48]. However, the green synthesis of CuO NPs may be beneficiary for the agriculture and medical uses [25, 26].

4 Conclusions and Future Perspectives The toxicity of Cu NPs has been reported widely in various plant species but at the same time, many positive reports are also available. Therefore, the environmental fate of CuO NPs must be determined carefully, and criteria for sustainable applications must be defined. Increasing number of results discussing toxicity of CuO NPs requires to be considered

Author's personal copy BioNanoSci. Table 1

Effects of CuO NPs on cultivated plants

Crops

Concentration (mg L−1)

Dimensions/size (nm)

Toxic effects

Ref.

Lettuce

100–300

–

[27, 28]

Alfalfa

0–20

10–100

Wheat

200

< 50

Mungbean

00–500

–

Maize Cucumber

2–100 100–600

– –

Affected seed germination, vigor index, and fresh weight. Reduced more than 49% root lengths Reduced the size of the plants, altered nutrient elements and enzymatic activity Decreased more than 13% shoot and 59% roots length compare to untreated plants, and brown necrotic lesions appeared on the root Affected chlorophyll production, nutrient availability, decreased root and lateral root growth, and increased proline content Chlorotic symptoms appeared on the root Inhibited seed germination (23.3%)

[28] [29, 30]

[31]

[33] [35]

Cilantro

0–80

–

Affected germination rate and shoot elongation

[36]

Rice Spinach

0–1000 1000

< 50 < 50

[39] [40]

Onion

0–80

40

Mustard

0–1500

< 50

Tomato

0–500

20–40

Decreased the number of thylakoids per granum Elevated concentration affected plants, reduced the root and shoot length, total weight, and chlorophyll contents Reduced/stopped root growth at high concentration, deformed the surface of root cap and meristematic zone Observed thinner and brittle root with brown necrotic lesions. Affected ROS enzyme system, antioxidants, proline, lipid peroxidation Reduced total chlorophyll content

Soybean

50–500

–

Carrot

1–1000

25–55

Sweet potato Barley

100–1000 –

25–55 < 50

Cotton

1000

30

Zucchini

0–1000

50

along with the search of the new application as the research has demonstrated the hazardous effect of NPs on germination, Fig. 2 Cross section of the root of barley. a Control. b Exposure to CuO NPs (1000 mg L−1). EP epidermis, ED endoderm, CC central cylinder of the root. Dark arrow indicate the accumulation of CuO in an intercellular compartment (unpublished data)

Affected shoot growth, weight, and chlorophyll content as well as root length and its fresh weight Reduced the shoots biomass and restricted the Cu accumulation in the taproot periderm Affected tuber biomass Induced the release of ROS, damaged cell membrane, decreased shoot and root lengths, and reduced the enzymatic activities Affected root length, aggregates observed on outer epidermis of root Reduced 90% biomass

[41] [42, 43]

[45] [46] [47] [48] [49]

[50, 51] [55]

accumulation, and on growth. Past and future research must be placed in the context of current risk assessments associated


with CuO NPs, their use, distribution, and release in an environment. Funding information This work was supported by the Russian Science Foundation (no. 16-14-10217). Compliance with Ethical Standards Conflict of Interest The authors declare that they have no conflict of interest.

References 1.

2. 3.

4.

5.

6.

7.

8.

9.

10.

11.

12.

13.

Keller, A. A., & Lazareva, A. (2014). Predicted releases of engineered nanomaterials: From global to regional to local. Environmental Science & Technology Letters, 1, 65–70. Salata, O. V. (2004). Applications of nanoparticles in biology and medicine. Journal of Nanobiotechnology, 2, 3. Servin, A. D., De la Torre-Roche, R., Castillo-Michel, H., Pagano, L., Hawthorne, J., Musante, C., Pignatello, J., Uchimiya, M., & White, J. C. (2016). Exposure of agricultural crops to nanoparticle CeO2 in biochar-amended soil. Plant Physiology and Biochemistry, 110, 147–157. Weir, A., Westerhoff, P., Fabricius, L., Hristovski, K., & von Goetz, N. (2012). Titanium dioxide nanoparticles in food and personal care products. Environmental Science & Technology, 46, 2242–2250. Yadav, T., Mungray, A. A., & Mungray, A. K. (2014). Fabricated nanoparticles: current status and potential phytotoxic threats. Reviews of Environmental Contamination and Toxicology, 230, 83–110. Josko, I., Oleszczuk, P., & Futa, B. (2014). The effect of inorganic nanoparticles (ZnO, Cr2O3, CuO and Ni) and their bulk counterparts on enzyme activities in different soils. Geoderma, 232, 528–537. Rajput, V. D., Tatiana, M., Svetlana, S., Viktoriia, T., Saglara, M., Andrey, G., Dina, N., & Natalya, G. (2017). Effect of nanoparticles on crops and soil microbial communities. Journal of Soils and Sediments, 1–9. https://doi.org/10.1007/s11368-017-1793-2 . BBC. (2015) Nanotechnology in environmental applications: the global market. Nano, 39C. https://www.bccresearch.com/marketresearch/nanotechnology. Accessed 15 May 2017. BBC. (2017). Global markets for nanocomposites, nanoparticles, nanoclays, and nanotubes. Nano, 21G. https://www.bccresearch.com/ market-research/nanotechnology. Accessed 15 May 2017. Rico, C. M., Majumdar, S., Duarte-Gardea, M., Peralta-Videa, J. R., & Gardea-Torresdey, J. L. (2011). Interaction of nanoparticles with edible plants and their possible implications in the food chain. Journal of Agricultural and Food Chemistry, 59, 3485–3498. Atha, D. H., Wang, H., Petersen, E. J., Cleveland, D., Holbrook, R. D., Jaruga, P., Dizdaroglu, M., Xing, B., & Nelson, B. C. (2012). Copper oxide nanoparticle mediated DNA damage in terrestrial plant models. Environmental Science & Technology, 46, 1819–1827. Powers, K. W., Brown, S. C., Krishna, V. B., Wasdo, S. C., Moudgil, B. M., & Roberts, S. M. (2006). Research strategies for safety evaluation of nanomaterials. Part VI characterization of nanoscale particles for toxicological evaluation. Toxicological Sciences, 90, 296–303. Royal Society and Royal Academy of Engineering. (2004). Nanoscience and nanotechnologies: opportunities and uncertainties. Royal Society Policy Document 19/04. London: Royal Society. https://royalsociety.org/~/media/Royal_Society_ Content/policy/publications/2004/9693.pdf. Accessed 07 Mar 2017.

14.

Handy, R. D., & Shaw, B. J. (2007). Toxic effects of nanoparticles and nanomaterials: implications for public health, risk assessment and the public perception of nanotechnology. Health Risk & Society, 9, 125–144. 15. Chibber, S., Ansari, S. A., & Satar, R. (2013). New vision to CuO, ZnO, and TiO2 nanoparticles: their outcome and effects. Journal of Nanoparticle Research, 15, 1–13. 16. Sommer, A. L. (1931). Copper as an essential for plant growth. Plant Physiology, 6, 339–345. 17. Rafique, M., Shaikh, A. J., Rasheed, R., Tahir, M. B., Bakhat, H. F., Rafique, M. S., & Rabbani, F. (2017). A review on synthesis, characterization and applications of copper nanoparticles using green method. Nano, 12, 04. 18. An, Y. J. (2006). Assessment of comparative toxicities of lead and copper using plant assay. Chemosphere, 62, 1359–1365. 19. Baker, D. E., & Senef, J. P. (1995). Copper. In B. J. Alloy (Ed.), Heavy metals in soils (pp. 179–205). London: Blackie Academic and Professional. 20. Hänsch, R., & Mendel, R. R. (2009). Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Current Opinion in Plant Biology, 12, 259–266. 21. Ivask, A., Bondarenko, O., Jepihhina, N., & Kahru, A. (2010). Profiling of the reactive oxygen species related ecotoxicity of CuO, ZnO, TiO2, silver and fullerene nanoparticles using a set of recombinant luminescent Escherichia coli strains: differentiating the impact of particles and solubilised metals. Analytical and Bioanalytical Chemistry, 398, 701–716. 22. Valko, M., Morris, H., & Cronin, M. T. (2005). Metals, toxicity and oxidative stress. Current Medicinal Chemistry, 12, 1161–1208. 23. Ahamed, M., Siddiqui, M. A., Akhtar, M. J., Ahmad, I., Pant, A. B., & Alhadlaq, H. A. (2010). Genotoxic potential of copper oxide nanoparticles in human lung epithelial cells. Biochemical and Biophysical Research Communications, 396, 578–583. 24. Sharma, D., Kanchi, S., & Bisetty, K. (2015). Biogenic synthesis of nanoparticles: a review. Arabian Journal of Chemistry. https://doi. org/10.1016/j.arabjc.2015.11.002. 25. Kumar, P. P. N. V., Shameem, K. P., Kalyani, R. L., & Pammi, S. V. N. (2015). Green synthesis of copper oxide nanoparticles using aloe vera leaf extract and its antibacterial activity against fish bacterial pathogens. BioNanoScience, 5, 135–139. 26. Kasana, R. C., Panwar, N. R., Kaul, R. K., & Kumar, P. (2017). Biosynthesis and effects of copper nanoparticles on plants. Environmental Chemistry Letters, 15, 233–240. 27. Shams, M., Yildirim, E., Agar, G., Ercisli, S., Dursun, A., Ekinci, M., & Kul, R. (2018). Nitric oxide alleviates copper toxicity in germinating seed and seedling growth of Lactuca sativa L. Notulae Botanicae Horti Agrobotanici, 46(1), 167–172. 28. Hong, J., Rico, C. M., Zhao, L., Adeleye, A. S., Keller, A. A., Peralta-Videa, J. R., & Gardea-Torresdey, J. L. (2015). Toxic effects of copper-based nanoparticles or compounds to lettuce (Lactuca sativa) and alfalfa (Medicago sativa). Environmental Science: Processes & Impacts, 17, 177–185. 29. Dimkpa, C. O., McLean, J. E., Latta, D. E., Manangón, E., Britt, D. W., & Johnson, W. P. (2012). CuO and ZnO nanoparticles: phytotoxicity, metal speciation, and induction of oxidative stress in sandgrown wheat. Journal of Nanoparticle Research, 14, 1125. 30. Lee, W. M., An, Y. J., Yoon, H., & Kweon, H. S. (2008). Toxicity and bioavailability of copper nanoparticles to the terrestrial plants mungbean (Phaseolus radiatus) and wheat (Triticum aestivum): plant agar test for water-insoluble nanoparticles. Environmental Toxicology and Chemistry, 27, 1915–1921. 31. Nair, P. M. G., & Chung, M. (2014). Copper oxide nanoparticle toxicity in mungbean (Vigna radiata L.) seedlings: physiological and molecular level responses of in vitro grown plants. Acta Physiologiae Plantarum, 36, 2947–2958.

Author's personal copy BioNanoSci. 32.

33.

34.

35.

36.

37.

38. 39.

40.

41.

42.

43.

44.

45.

46.

47.

48.

49.

Apodaca, S. A., Tana, W., Dominguezb, O. E., Hernandez-Viezcasc, J. A., Peralta-Videaa, J. R., & Gardea-Torresdey, J. L. (2017). Physiological and biochemical effects of nanoparticulate copper, bulk copper, copper chloride, and kinetin in kidney bean (Phaseolus vulgaris) plants. Sci Total Environ, 599-600, 2085–2094. Wang, Z., Xie, X., Zhao, J., Liu, X., Feng, W., White, J. C., & Xing, B. (2012). Xylem- and phloem-based transport of CuO nanoparticles in maize (Zea mays L.) Environmental Science & Technology, 46, 4434– 4441. Kim, S., Sin, H., Lee, S., & Lee, I. (2013). Influence of metal oxide particles on soil enzyme activity and bioaccumulation of two plants. Journal of Microbiology and Biotechnology, 23(9), 1279–1286. Moon, Y. S., Park, E. S., Kim TO, Lee, H. S., & Lee, S. E. (2014). SELDI-TOF MS-based discovery of a biomarker in Cucumis sativus seeds exposed to CuO nanoparticles. Envrionmental Toxicology and Pharmacology, 38, 922–931. Zuverza-Mena, N., Medina-Velo, I. A., Barrios, A. C., Tan, W., Peralta-Videa, J. R., & Gardea-Torresdey, J. L. (2015). Copper nanoparticles/compounds impact agronomic and physiological parameters in cilantro (Coriandrum sativum). Environmental Science: Processes & Impacts, 17, 1783–1793. Peng, C., Duan, D., Xu, C., Chen, Y., Sun, L., Zhang, H., Yuan, X., Zheng, L., Yang, Y., Yang, J., Zhen, X., Chen, Y., & Shi, J. (2015). Translocation and biotransformation of CuO nanoparticles in rice (Oryza sativa L.) plants. Environmental Pollution, 197, 99–107. Shaw, A. K., & Hossain, Z. (2013). Impact of nano-CuO stress on rice (Oryza sativa L.) seedlings. Chemosphere, 93, 906–915. Costa, D. M. V. J., & Sharma, P. K. (2016). Effect of copper oxide nanoparticles on growth, morphology, photosynthesis, and antioxidant response in Oryza sativa. Photosynthetica, 54, 110. Singh, D., & Kumar, A. (2016). Impact of irrigation using water containing CuO and ZnO nanoparticles on Spinach oleracea grown in soil media. Bulletin of Environmental Contamination and Toxicology, 97, 548–553. Deng, F., Wang, S., & Xin, H. (2016). Toxicity of CuO nanoparticles to structure and metabolic activity of Allium cepa root tips. Bulletin of Environmental Contamination and Toxicology, 97, 702–708. Rao, S., & Shekhawat, G. S. (2016). Phytotoxicity and oxidative stress perspective of two selected nanoparticles in Brassica juncea. 3. Biotech, 6, 244. Nair, P. M. G., & Chung, I. M. (2015). Study on the correlation between copper oxide nanoparticles induced growth suppression and enhanced lignification in indian mustard (Brassica juncea L.) Ecotoxicology and Environmental Safety, 113, 302–313. Zafar, H., Ali, A., & Zia, M. (2017). CuO nanoparticles inhibited root growth from Brassica nigra seedlings but induced root from stem and leaf explants. Applied Biochemistry and Biotechnology, 181, 365–378. Singh, A., Singh, N. B., Hussain, I., & Singh, H. (2017). Effect of biologically synthesized copper oxide nanoparticles on metabolism and antioxidant activity to the crop plants Solanum lycopersicum and Brassica oleracea var. botrytis. Journal of Biotechnology, 262, 11–27. Nair, P. G., & Chung, I. (2014). A mechanistic study on the toxic effect of copper oxide nanoparticles in soybean (Glycine max L.) root development and lignification of root cells. Biological Trace Element Research, 162, 342–352. Ebbs, S. D., Bradfield, S. J., Kumar, P., White, J. C., Musante, C., & Ma, X. (2016). Accumulation of zinc, copper, or cerium in carrot (Daucus carota) exposed to metal oxide nanoparticles and metal ions. Environmental Science Nano, 3, 114–126. Bradfield, S. J., Kumar, P., White, J. C., & Ebbs, S. D. (2017). Zinc, copper, or cerium accumulation from metal oxide nanoparticles or ions in sweet potato: yield effects and projected dietary intake from consumption. Plant Physiology and Biochemistry, 110, 128–137. Shaw, A. K., Ghosh, S., Kalaji, H. M., Bosa, K., Brestic, M., Zivcak, M., & Hossain, Z. (2014). Nano-CuO stress induced modulation of

50.

51.

52.

53.

54.

55.

56.

57.

58.

59.

60.

61.

62.

63.

64.

antioxidative defense and photosynthetic performance of syrian barley (Hordeum vulgare L.) Environmental and Experimental Botany, 102, 37–47. Nhan, L. V., Yukui, R., Weidong, C., Jianying, S., Shutong, L., Trung, N. Q., & Liming, L. (2016). Toxicity and bio-effects of CuO nanoparticles on transgenic Ipt-cotton. Journal of Plant Interactions, 11, 108–116. Le Van, N., Ma, C. X., Shang, J. Y., Rui, Y. K., Liu, S. T., & Xing, B. S. (2016). Effects of CuO nanoparticles on insecticidal activity and phytotoxicity in conventional and transgenic cotton. Chemosphere, 144, 661–670. Adhikari, T., Kundu, S., Biswas, A. K., Tarafdar, J. C., & Rao, A. S. (2012). Effect of copper oxide nanoparticle on seed germination of selected crops. Journal of Agricultural Science and Technology, 2, 815–823. SG, W., Huang, L., Head, J., Chen, D. R., Kong, I. C., & Tang, Y. J. (2012). Phytotoxicity of metal oxide nanoparticles is related to both dissolved metals ions and adsorption of particles on seed surfaces. Journal of Petroleum & Environmental Biotechnology, 3, 126. Rajput, V.D., Tstitsuashvili, V.S., Sushkova, S.N., & Nevidomskaya, D.G. (2017) Effects of ZnO and CuO nanoparticles on soil, plant and microbial community. International Scientific Conference XX Dokoutchaev Youth Readings, Saint Petersburg, Russia, UDC 631.416.8 (9). http://www.dokuchaevskie.ru/information/2017g. Accessed 05 May 2017. Stampoulis, D., Sinha, S. K., & White, J. C. (2009). Assaydependent phytotoxicity of nanoparticles to plants. Environmental Science & Technology, 43, 9473–9479. Harir, S. M., Asma, G. O., Kadhim, M. I., & Nabeel, K. I. (2017). Influence of silver and copper nanoparticles on physiological characteristics of Phaseolus vulgaris L. in vitro and in vivo. International Journal of Current Microbiology & Applied Sciences, 6(1), 834–843. Singh, A., Singh, N. B., Hussain, I., Singh, H., & Yadav, V. (2017). Synthesis and characterization of copper oxide nanoparticles and its impact on germination of Vigna radiata (L.) R. Wilczek. Tropical Plant Biology, 4(2), 246–253. Karlsson, H. L., Gustafsson, J., Cronholm, P., & Möller, L. (2009). Size-dependent toxicity of metal oxide particles—a comparison between nano- and micrometer size. Toxicology Letters, 188, 112–118. Jain, N., Bhargava, A., Pareek, V., Akhtar, M. S., & Panwar, J. (2017). Does seed size and surface anatomy play role in combating phytotoxicity of nanoparticles? Ecotoxicology. https://doi.org/10. 1007/s10646-017-1758-7. Wierzbicka, M., & Obidzinska, J. (1998). The uptake of lead on seed imbibition and germination in different plant species. Plant Science, 137, 155–171. Kranner, I., & Colville, L. (2011). Metals and seeds: biochemical and molecular implications and their significance for seed germination. Environmental and Experimental Botany, 72, 93–105. Miralles, P., Church, T. L., & Harris, A. T. (2012). Toxicity, uptake, and translocation of engineered nanomaterials in vascular plants. Environmental Science & Technology, 46, 9224–9239. Rajput, V.D., Minkina, T., Mandzhieva, S., Duply, N., Fedorenko, A., Sushkova, S., Tsitsuashvili, V. (2017). Influence of copper oxide nanoparticle on seed germination and seedling growth. International scientific conference on Bmodern technologies in the study of biodiversity and planting of plants, Rostov, Russia, 115-116. http:// conference2017.bg.sfedu.ru/index.php?option=com_content&view= article&id=12&Itemid=129. Accessed 26 Oct 2017. Xiong, T. T., Dumat, C., Dappe, V., Vezin, H., Schreck, E., Shahid, M., Pierart, A., & Sobanska, S. (2017). Copper oxide nanoparticle foliar uptake, phytotoxicity, and consequences for sustainable urban agriculture. Environmental Science & Technology Letters. https:// doi.org/10.1021/acs.est.6b05546.

Author's personal copy BioNanoSci. 65.

Rajput, V. D., Chen, Y., & Ayup, M. (2015). Effects of high salinity on physiological and anatomical indices in the early stages of Populus euphratica growth. Russian Journal of Plant Physiology, 62, 229–236.

66.

Olchowik, J., Bzdyk, R. M., Studnicki, M., Bederska-Błaszczyk, M., Urban, A., & Aleksandrowicz-Trzcińska, M. (2017). The effect of silver and copper nanoparticles on the condition of english oak (Quercus robur L.) seedlings in a container nursery experiment. Forests, 8, 310.