Effect of metal and metal oxide nanoparticles on growth and physiology of globally important food crops: A critical review

Accepted Manuscript Title: Effect of metal and metal oxide nanoparticles on growth and physiology of globally important food crops: a critical review Author: Muhammad Rizwan Shafaqat Ali Muhammad Farooq Qayyum Yong Sik Ok Muhammad Adrees Muhammad Ibrahim Muhammad Zia-ur-Rehman Mujahid Farid Farhat Abbas PII: DOI: Reference:

S0304-3894(16)30499-X http://dx.doi.org/doi:10.1016/j.jhazmat.2016.05.061 HAZMAT 17750

To appear in:

Journal of Hazardous Materials

Received date: Revised date: Accepted date:

29-8-2015 12-5-2016 19-5-2016

Please cite this article as: Muhammad Rizwan, Shafaqat Ali, Muhammad Farooq Qayyum, Yong Sik Ok, Muhammad Adrees, Muhammad Ibrahim, Muhammad Zia-urRehman, Mujahid Farid, Farhat Abbas, Effect of metal and metal oxide nanoparticles on growth and physiology of globally important food crops: a critical review, Journal of Hazardous Materials http://dx.doi.org/10.1016/j.jhazmat.2016.05.061 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Effect of metal and metal oxide nanoparticles on growth and physiology of globally important food crops: a critical review Muhammad Rizwana, Shafaqat Alia, Muhammad Farooq Qayyumb*, Yong Sik Okc, Muhammad Adreesa, Muhammad Ibrahima, Muhammad Zia-ur-Rehmand, Mujahid Faride, Farhat Abbasa a

Department of Environmental Sciences and Engineering, Government College University Allama Iqbal Road 38000

Faisalabad, Pakistan b

Department of Soil Sciences, Faculty of Agricultural Sciences and Technology. Bahauddin Zakariya University

Multan, Pakistan c

Korea Biochar Research Centre and Department of Biological Environment, Kangwon National University,

Chuncheon 200-701, Korea d e

Institute of Soil and Environmental Sciences, University of Agriculture, Faisalabad 38040 (Pakistan)

Department of Environmental Sciences, University of Gujrat, Hafiz Hayat Campus, Gujrat, Pakistan.

*

Corresponding Author: Muhammad Farooq Qayyum

E-Mail: [email protected]

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Highlights:    

Metal and metal oxide nanoparticles (NPs) are widely used worldwide. NPs has both positive and negative effects of crop plants NPs toxicity decreased growth, biomass and yield of food crops This review discussed the NPs effects and toxicity mechanisms in food crops

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Abstract The concentrations of engineered metal and metal oxide nanoparticles (NPs) have increased in the environment due to increasing demand of NPs based products. This is causing a major concern for sustainable agriculture. This review presents the effects of NPs on agricultural crops at biochemical, physiological and molecular levels. Numerous studies showed that metal and metal oxide NPs affected the growth, yield and quality of important agricultural crops. The NPs altered mineral nutrition, photosynthesis and caused oxidative stress and induced genotoxicity in crops. The activities of antioxidant enzymes increased at low NPs toxicity while decreased at higher NPs toxicity in crops. Due to exposure of crop plants to NPs, the concentration of NPs increased in different plant parts including fruits and grains which could transfer to the food chain and pose a threat to human health. In conclusion, most of the NPs have both positive and negative effects on crops at physiological, morphological, biochemical and molecular levels. The effects of NPs on crop plants vary greatly with plant species, growth stages, growth conditions, method, dose, and duration of NPs exposure along with other factors. Further research orientation is also discussed in this review article. Key words: crop plants, genotoxicity, metals toxicity, plant biochemistry

Contents 1. Introduction ............................................................................................................................................... 5 2. Sources of nanoparticles in soil ................................................................................................................ 6 3. Uptake and translocation in plants ............................................................................................................ 6 4. Effects of NPs on plants ............................................................................................................................ 9 4.1. Effect on seed germination ................................................................................................................ 9 4.2. Effect on plant growth and morphology .......................................................................................... 12 4.3. Effect on grain yield and quality ...................................................................................................... 14 5. Mechanisms of nanoparticle toxicity in plants........................................................................................ 15 5.1. Indirect changes in the growth medium ........................................................................................... 15 5.2. Genotoxicity..................................................................................................................................... 16 5.3. Alteration in mineral uptake and assimilation ................................................................................. 18 5.4. Enhancement in ROS generation and reduction in antioxidant enzymes ........................................ 19 5.5. Reduction in photosynthesis and gas exchange parameters ............................................................. 21 6. Conclusion and perspectives ................................................................................................................... 21 3

Acknowledgements……………………………………………………………………………………………………………………………….20 References ................................................................................................................................................... 22

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1. Introduction Nanotechnology has been widely used in food, biomedical, and agricultural sectors worldwide [1, 2]. Although nanoparticles (NPs) naturally exist in the environment, the application of nanotechnology has resulted in a significant increase in the production of engineered nanoparticles (ENPs). It is estimated that over 800 products are currently available in the market [2-5]. Engineered NPs have a characteristic dimension of ≤ 100 nm and different properties from non-nanoscale particles with the same chemical composition [6]. The NPs may enter into soils through the application of pesticides, paints as well as direct release from industries [7-9]. Due to their static nature and interaction with soil and air, plants are exposed to the NPs that are released into the environment. Direct exposure of plants to metal and metal oxide NPs also should not be ignored. In the past few years, both beneficial and negative effects of NPs on crop growth have been reported. These effects were dependent on the type, source and size of the NPs, the plant species, and the exposure duration of NPs to crops [10-14]. For example, silver (Ag) NPs increased ascorbate and chlorophyll in the leaves of asparagus (Asparagus officinalis L.) and iron (Fe) NPs increased soybean (Glycine max L.) biomass [10, 14]. Similarly, application of silica NPs increased the seed germination, root and shoot length, photosynthesis and dry weight of maize seedlings grown under field conditions [106]. In addition, titanium dioxide (TiO2) NPs decreased the hydrogen per oxide (H2O2), malondialdehyde (MDA) and electrolyte leakage in chickpea (Cicer arietinum L.) as compared to the control plants [171]. On the other hand, several reports indicated that metal NPs adversely affected growth and physiology of important crops such as wheat (Triticum aestivum L.), rice (Oryza sativa L.), maize (Zea mays L.), and soybean [15-19]. In addition, metal and metal oxide NPs were more toxic to crops than bulk metal particles [20]. It has been widely reported that crops exposed to NPs could uptake and translocate NPs to different parts of the crops [21-23]. The NPs reduced seed germination of many crop plants [24-26]. The toxic effects of NPs in many plant species can be observed by reduced plant growth, biomass, and fruit/grain yield [19, 23, 27]. An excess of NPs caused physiological disorders in crops (reduction in photosynthesis and gas exchange attributes), oxidative stress and reduction in the activities of antioxidant enzymes (cytotoxicity and genotoxicity) [18, 28-31]. Several studies reported that NPs decreased mitotic index and impaired stages of cell divisions in root tips of many plants and altered the expression of genes related to root growth [32-35]. Nanoparticles are not only directly toxic to plants, but also cause 5

indirect toxicities by altering the growth medium, damaging the roots, altering soil bacterial communities, and causing uptake of co-contaminants by plants [36-38]. Thus, NPs could increase or decrease crop growth and yield and they can be transferred into the food chain with unknown consequences to humans and animals [18, 24-31]. Over the last decade, both positive and toxic effects of metal and metal oxide NPs on growth, yield, and physiology of agricultural crops have been widely reported in the literature [24, 25, 38-40]. Therefore, here, we reviewed the effects of metal and metal oxide NPs on seed germination, plant growth and morphology, mineral uptake, photosynthesis, oxidative stress, and antioxidant enzymes and genetic levels of important food crops. This review is mainly focused on ENPs as the production of ENPs is continuously increasing due to commercial use of ENPs products [41-47]. Based on the literature, we highlighted the existing findings and future research priorities regarding NPs to avoid their negative effects on food crops. The NPs discussed in each section are arranged in alphabetical order for better understanding of the manuscript.

2. Sources of nanoparticles in soil Nanoparticle production is rapidly increasing due to the growing market of NP-based products that have resulted in the appearance of NPs in different places such as soil, water and air [41]. Oceans and soils are among the main sinks of NPs in the environment (e.g. via sludge application to soil). It has been estimated that 63-91% ENPs have ended up in landfills worldwide, which could subsequently be released into the soils, water, and atmosphere [41-43]. Nanoparticles could also enter into soils through the intentional use of NP-based agrochemicals and their release from industries [7, 43-45]. Nanoparticles are entering the soils due to the use of NPs for remediation purposes, the accidental release from the manufacturing units, irrigation with wastewater, and atmospheric fallouts [11, 46-47]. Thus, entry of NPs into the soils and water might be of great concern due to food chain contamination through agricultural crops grown in these contaminated soils and irrigated with contaminated water.

3. Uptake and translocation in plants Internalization of metal and metal oxide NPs into edible and reproductive parts of crops is of particular concern because most of the NPs are toxic to living organisms. It has been reported 6

that plant agar test might be a good protocol for testing the uptake and phytotoxicity in plants [51, 100]. Several studies have reported that plants can take up metal and metal oxide NPs either through the soils or foliar contact [21, 48-49]. Nanoparticles can pass through the plants by adhering to the root surfaces and entering the epidermis and cortex via an apoplastic pathway [21, 22, 48, 5052]. However, uptake and translocation of NPs in plants may vary with plant species, cultivars, and growth conditions [27, 53-55]. Crop plants exposed to metal and metal oxide NPs accumulated NPs in their roots and translocated to aerial parts, the amount which depended on plants, exposure concentration, size, type, and agglomeration of NPs [22, 23, 51, 56-60]. Cifuentes et al. [61] reported that magnetic carbon coated NPs penetrated through roots in four crops including pea (Pisum sativum L.), sunflower (Helianthus annuus L.), tomato (Solanum lycopersicum L.), and wheat (Triticum aestivum) moved towards the vascular cylinder and reached the aerial parts through transpiration in the xylem vessels. Similar results were reported in rice with Ag NPs [39]. In groundnut (Arachis hypogaea L.), foliar application of CaO NPs (10 to 1000 ppm; the size of 69.9 nm) showed the entry of Ca into leaves, stem, and roots through phloem compared to bulk sources of sprayed Ca (CaO and CaNO3) [66]. Foliar applied NPs can enter through leaves and have the ability to move in different parts of crops [66-68]. Hong et al. [67] and Larue et al. [68] observed internalization of foliar applied CeO2 NPs and TiO2 in cucumber (Cucumis sativus L.) and lettuce (Lactuca sativa L.) leaves, respectively, and both NPs were observed in different parts of the crops. Antisari et al. [19] studied the uptake of metal oxides (cerium oxide (CeO2), iron oxide (Fe3O4), tin dioxide (SnO2), TiO2 and metallic (silver (Ag), cobalt (Co), nickel (Ni) NPs in tomato. The authors reported that metals from NPs mainly accumulated in the tomato roots and plants treated with Ag, Co, and Ni NPs showed higher concentration of the elements in both shoots and roots as compared to the control. Similar results were reported in tomato seedlings exposed to CeO2 NPs [64]. On the other hand, roots accumulated metals from NPs, but metals were not translocated to aerial parts in many plants [65, 14]. For example, Rico et al. [14] reported that cerium (Ce) accumulation increased in wheat roots with increasing CeO2 NPs concentration in soils, but did not change across treatments in leaves, hull, and grains, indicating a lack of Ce translocation to the aerial parts of wheat. Similarly, Wang et al. [20] reported that Fe3O4 NPs were not 7

translocated to shoots in rye grass and pumpkin (Cucurbita maxima L.). Similarly, in cucumber grown hydroponically, most of the CeO2 NPs remained as NPs and small amounts were biotransformed to CePO4 in roots and to cerium carboxylates in shoots [73]. In addition, Cui et al. [29] reported that a part of CeO2 NPs were transformed from Ce(IV) to Ce(III) in the lettuce roots. Ma et al. 2015 [72] found that a fraction of Ce was changed to Ce(III)–carboxyl complexes. More recently, Peng et al. [74] reported that copper oxide nanoparticles (CuO NPs) entered the stele through lateral roots in rice and translocated to leaves; the Cu (II) was mainly combined with cysteine, citrate, and phosphate ligands and was even reduced to Cu (I). For maize, Wang et al. [75] reported that CuO NPs (100 mg L-1, size: 20−40 nm) were translocated from roots to shoots via xylem and re-translocated from shoots to roots via phloem; CuO NPs, during this translocation, could be reduced from Cu (II) to Cu (I). Excess Cu is toxic to plants and caused reduction in growth and yield of rapeseed (Brassica napus L.) and wheat [76-78]. Ma et al. [36] observed that lanthanum oxide nanoparticles (La2O3 NPs) were transformed into needle-like LaPO4 nano-clusters in the intercellular regions of cucumber roots. The La was combined with phosphate or carboxylic group in aerial parts of the cucumber. Transformation is a critical factor which affects the fate and toxicity of NPs in living organisms. After absorption by roots, plants can transform NPs into other forms [29, 69-72]. For example, Parsons et al. [69] observed Ni NPs in roots and shoots of mesquite (Prosopis sp.) treated with uncoated nickel hydroxide nanoparticles (Ni(OH)2 NPs), whereas leaves had a Ni(II)-organic acid type complex. Du et al. [21] revealed that most of the TiO2 NPs were found adhering to wheat root tip cell wall of periderm cells while roots treated with zinc oxide (ZnO) NPs were free of particles [21]. It has been reported that rapeseed and wheat roots accumulated higher concentration of TiO2 NPs with 14 nm size than the same NPs with the size of 25 nm. Root to shoot translocation increased with decreasing the size of NPs and rapeseed accumulated more Ti than wheat [58]. The authors argued that this difference might be due to the agglomeration status of NPs during plant exposure as 14 nm TiO2 NPs were agglomerated but 25 nm TiO2 NPs were not in the exposure suspension. Larue et al. [58] reported that TiO2 NPs with a diameter of greater than 140 nm were not accumulated in wheat roots and NPs with a diameter greater than 36 nm accumulated in wheat roots, but were not translocated to the shoots. Hernandez-Viezcas et al. [71] observed O-bound Zn, in a form resembling Zn-citrate, in soybean grains treated with ZnO NPs (500 mg kg-1 of 8

soil, size: 10 nm) which could be an important Zn complex. Wang et al. [65] observed zero upward translocation of ZnO NPs from roots to shoots in cowpea (Vigna unguiculata L.) grown in either solution or soil culture. Lin and Xing [62] reported that ZnO NPs adhered to the root surface of rye grass (Lolium perenne L.) and were found in the apoplast and protoplast of the root endodermis and stele. In summary, the supply and growth of major agricultural crops exposed to NPs are affected. The findings above show that NPs are taken up by the plants either through root or foliar exposure, depending upon the type and size of NPs, the exposure medium, and the crop species. NPs are translocated to different parts of the crops and this accumulation of NPs into important food crops has relevance to the food chain. However, plant/NP interaction mechanisms are still poorly understood and more detailed studies are needed to explore these mechanisms, especially at molecular levels. Detailed studies are needed to quantify the NPs adsorption and uptake in different crops under varying growth conditions. Moreover, real soil based studies with relevant environmental exposure conditions are lacking.

4. Effects of NPs on plants

Due to the extensive use of metal and metal oxide NPs and their possible entry into the food chain through plants, the growth and yield of important crops may be compromised. Thus, there is urgent need to review the available literature on the potential toxicity of NPs in crops. In spite of some studies reporting the beneficial effects of NPs on agricultural crops, toxic effects on crops are widely reported, which may well exceed the possible advantages of NP application in agricultural crops. Toxic effects of NPs in plants include the decrease in seed germination, growth inhibition, and reduction in yield and quality (Figure 1). In the following sub-sections, the both positive and toxic effects of NPs on growth, yield, and physiology of important food crops are reported (Table 1).

4.1. Effect on seed germination Seed germination is the first step which determines the success of crop growth in soils contaminated with metal and metal oxide NPs. In recent, toxic effects of metal NPs on seed germination of food crops have been widely reported [24, 25, 79-80]. In general, toxicity of NPs 9

reduced the seed germination rate and dispersed the germination events of many crop species [24, 26, 81]. Some work has focused on the effects of Ag NPs on seed germination of rice, barley (Hordeum vulgare L.), turnip (Brassica rapa L.) and faba bean (Vicia faba L.) [24, 39, 95]. Results showed that Ag NPs decreased germination of turnip and faba bean in dose-dependent manner. For barley, Ag NPs decreased seed germination by 10-20% as compared to the control. Rice seed germination decreased with increasing dose and size of Ag NPs. Similarly, metal oxide NPs (CuO, NiO, TiO2, iron oxide (Fe2O3) and Co3O4) reduced the seed germination of lettuce, radish (Raphanus sativus L.) and cucumber by adsorbing on seed surfaces and releasing free metal ions near the seeds [81]. The authors reported that toxic effects of NPs on seed germination vary with crops (i.e., lettuce > cucumber > radish) and seed size. However, Yasur and Rani [92] reported that Ag NPs (upto 4000 mg L-1) did not affect the seed germination of castor bean, (Ricinus communis L.). In the literature, few studies are available related to seed germination of crop plants in soils [95]. For example, inhibition of seed germination was less pronounced in rye grass, barley, and flax (Linum usitatissimum L.) exposed to zero-valent iron NPs (0–5000 mg L-1) or Ag NPs (0–100 mg L-1) in soils compared to water. Moreover, seed germination varied in different soils i.e., less pronounced in clayey soil compared to sandy soil [95]. The seed germination of sorghum (Sorghum bicolor L.) increased by the reduction of surface area attributes which led to greater soil aggregation and sorption of dissolved silver ion as well as Ag NPs [96]. Similarly, Gruyer et al. [97] reported that seed germination of radish and lettuce was less inhibited in soil applied Ag NPs, as compared to water applied NPs in a dosedependent manner. Copper oxide nanoparticle (CuO NPs) significantly reduced seed germination of cucumber and a lowered the germination rate to 23.3% at 600 mg L-1 [25]. In addition, seed germination of rice was significantly reduced under CuO NPs stress in a dose dependent manner [83]. López-Moreno et al. [84] studied the effect of cerium oxide (CeO2) NPs at a concentration of 0 to 4000 mg L-1 on seeds of tomato, cucumber, maize, and alfalfa (Medicago sativa L.). Results showed that 2000 mg L-1 CeO2 NPs reduced the seed germination of maize, tomato, and cucumber by 30, 30, and 20% as compared to the control respectively while seed germination of alfalfa was not significantly decreased. In tomato, application of SiO2 NPs (8 g L-1, size: 12 nm) increased seed germination, mean germination time, seed germination index, and seed vigor index [94]. Several studies reported that NP-mediated inhibition in seed germination might be 10

due to partial dissolution of NPs and release of toxic metal ions or surface modifications in exposure solution or plant tissues [36, 85]. Metal and metal oxide NPs both decreased and increased the seed germination of several food crops [86-87]. For example, a few studies have focused on the effect of TiO2 NPs on seed germination of wheat, maize, rapeseed, radish, tomato, onion (Allium cepa L.), parsley (Petroselinum crispum L.), and fennel (Foeniculum vulgare L.) [60, 87-91, 142]. The authors reported that there was 100% seed germination of tomato and onion with 100 mg L-1 of TiO2 NPs and for radish, 100% germination was observed with 400 mg L-1 [87]. Seed germination of parsley was increased by 92% with 30 mg mL-1 and application of 40 mg L1

TiO2 NPs improved mean germination time of fennel by 31.8% in comparison to the untreated

control [90]. Similarly, TiO2 NPs (10, 50, and 100 ppm of aqueous TiO2 suspension, size 14 and 25 nm) did not affect seed germination of wheat and rapeseed [58]. Authors suggested that no effect of TiO2 NPs on wheat seed germination might be due to the inertness of NPs. However, authors reported that higher concentration of NPs were toxic to plants and reduced the seed germination. For example, TiO2 NPs increased the seed germination of wheat plants at concentration between 2 to 10 ppm and decreased seed germination at higher concentrations (100 and 500 ppm) [88]. From these studies, it can be concluded that lower concentration of TiO2 NPs may serve as a seed-priming agent for food crops. However, positive effects of TiO2 NPs on seed germination depend on size, concentration, duration of exposure, growth conditions, and plant species. Thus, further studies are needed to evaluate the effectiveness of TiO2 NPs application in agricultural crops. More recently, Zhang et al. [40] have found that ZnO NPs did not affect the seed germination of maize and cucumber. Boonyanitipong et al. [93] observed that ZnO and TiO2 NPs (100 to 1000 ppm and seed soaking for 1 to 3 day) did not affect the seed germination of rice. On the other hand, the frequency of seed germination decreased in maize, chinese cabbage (Brassica pekinensis L.), and garden cress (Lepidium sativum L.) with increasing ZnO NPs concentration [26, 79, 82]. In conclusion, metal and metal oxide NPs reduced or improved seed germination of many plants; plant response varied significantly among NPs and was partially correlated to dose and the size of the NPs. Although NPs positively or negatively affected seed germination of tested plants, the mechanisms behind the germination are still poorly understood, especially in soil. 11

4.2. Effect on plant growth and morphology Plant morphological parameters such as leaf area, shoot and root lengths, as well as shoot and root weights are indicators of plant health. In literature, negative effects of metal based. NPs like ZnO, Fe2O3, aluminum dioxide (Al2O3), CuO, on shoot/ root growth and elongation have been reported in many crop species such as rice, wheat, maize, tomato, and barley. Studies found that toxicity might be due to enhanced release of metal ions from NPs [15-17]. It is worth mentioning that Ag NPs inhibited the root growth and biomass of many crops such as wheat, rice, sorghum, and tomato [15, 34, 91, 96, 103-104]. Ag NPs (1000 ppm, size: 25 nm, 12 days) damaged the root cell walls and vacuoles of rice, which might be due to the penetrations of large sized NPs through small pores of cell walls [103]. Similar results were also observed in rice seedlings exposed to Ag NPs [102]. Rice seedling exposed to Ag NPs, (0, 0.2, 0.5, and 1 mg L-1 for one week) showed significant reductions in root elongation as well as shoot and root fresh weights [105]. In wheat, Ag NPs reduced the growth in a dose dependent manner in different cultures [15, 34]. Thuesombat et al. [39] observed Ag NPs-mediated dose and size-dependent decrease in shoot and root fresh and dry weight of rice. It has been reported that lower Ag NPs treatments, up to 30 mg L-1, accelerated the rice root growth while higher concentration, at 60 mg L-1, reduced the root growth and caused root death. Shoot growth was more susceptible to NPs stress [102]. Dimkpa et al. [15] reported that wheat seedlings exposed to CuO NPs for 14 days reduced the shoot and root lengths by 13% and 59%, respectively, and exhibited the necrotic spots on roots and the roots were thinner and more brittle than the control. The authors suggested that Cu released from CuO NPs caused phytotoxicity but the Zn released from ZnO NPs did not play a significant role for the changes in plant growth [15]. Similarly, 72 h exposure to CuO NPs, 5 mg L-1 suspension, severely inhibited the elongation and biomass of rice roots [35]. CuO NPs (20 ppm for 15 days) reduced the root length by 49.5% and 47.6% in both lettuce and alfalfa respectively and roots were brown in color as compared to the control plants [98]. Adhikari et al. [99] reported that root growth of soybean and chickpea was prevented above 500 ppm CuO NPs (< 50 nm). Zhang et al. [116] reported the no significant effect of CeO2 NPs (10 mg L-1 for 10 days size: 400-700 nm) on radish growth. Similarly, Shaw et al. [18] observed a gradual decrease in shoot length as well as shoot weight of barley exposed to increasing CuO NPs concentrations (0.5, 1.0, and 1.5 mM suspensions with size < 50nm) in both 10 and 20 days. In addition, soil 12

application of Fe3O4 NPs increased the tomato root growth while SnO2 NP exposure decreased it [19]. Plant height and shoot and root biomass of cotton seedlings linearly decreased with increasing CeO2 and SiO2 NPs in growth media [22, 55]. Previous studies have reported both the positive and no effects of CeO2 NPs on crop growth and development [64, 115-116]. In tomato, CeO2 NPs (0.1–10 mg L-1) slightly improved the plant height and biomass [75]. Moreover, CeO2 NPs (10 mg L-1) affected the second-generation seedlings of tomato, which were smaller and weaker with lower biomass and water transpiration as compared to control second-generation seedlings [115]. On the other hand, SiO2 NPs application (5–20 kg ha-1) in sandy loam soil increased shoot and root length, stem height, and leaf area of twenty-day-old maize seedlings [106]. Positive effects of Si nutrition on plant growth have been widely reported, especially under stressful conditions in different growth mediums [78, 107-108]. Toxic effects of NPs on plant growth depend on the size, type, concentration, and duration of NPs application in the growth medium [39, 60, 100-101]. For example, Mahmoodzadeh et al. [19] reported that lower concentration of TiO2 NPs (10 and 100 ppm, size ~ 20 nm) significantly increased the fresh weight of wheat shoots and roots while higher TiO2 NPs concentration (> 100 ppm) decreased fresh weights in a dose-dependent manner. In other instance, TiO2 NPs (1,000– 5,000 mg L−1) did not significantly change the biomass of tomato [60]. Several studies reported the toxic effects of ZnO NPs on the growth of many crops grown in different environmental conditions [109-112]. ZnO NPs (500 and 750 mg kg-1 of soil in pot) reduced the root and shoot biomass of alfalfa by 80% and 25%, respectively [12]. Kouhi et al. [112] studied the anatomical and ultrastructural modifications of the roots and leaves of rapeseed treated with ZnO NPs (100 mg L-1, size: for 2 months). Results showed that ZnO NPs decreased the diameter of root tip as well as the size of epidermal and pericycle cells. The NPs also decreased the size of mitochondria, plastoglobuli, and the number of chloroplasts in the leaves while increasing the size of starch grains and the number of plastoglobuli. All these modifications were recorded compared to control and all these modifications resulted in decreased crop growth and biomass. Pavani et al. [111] reported that ZnO NPs increased the shoot and root lengths and fresh and dry weights of chickpea. Kim et al. [110] observed that CuO and ZnO NPs (1,000 ppm for 5 days) reduced the biomass of cucumber by 75% and 35% 13

respectively. ZnO NPs (50 or 500 mg kg-1 of soil) reduced the root and shoot length, root surface area, and volume of soybean as compared to control [113]. Foliar application of ZnO- and FeO NPs (20 and 50 ppm respectively) enhanced the growth of mung bean (Vigna radiate L.) [117]. In addition, ZnO NPs (100 to 1000 mg L−1) reduced the root length and number of roots of rice plants.TiO2 NPs, at similar concentration, had no effect on root length [93]. Studies related to toxicity of NPs in crop plants under field conditions are rare [21, 114]. It has been reported that TiO2 and ZnO NPs decreased wheat growth [21] whereas application of zero valent Cu, Co, and Fe increased the growth of soybean under field conditions [114]. Although, NPs have both positive and negative effects on plant growth and morphology, the response varied with dose applied, plant species, experimental conditions and exposure duration. Furthermore, most of the studies were performed under controlled conditions with short-term exposure to NPs and long-term studies are still lacking in this regard.

4.3. Effect on grain yield and quality Nanoparticle toxicity reduced the grain/fruit yield and nutritional quality of many food crops. The effects of CeO2 NPs on yield and quality of crops vary with plants and cultivars [14, 23, 118]. For example, application of CeO2 NPs, 500 ppm in soil, increased yield, spike length, the number of spikelets spike-1 and the number of grains spike-1 of wheat. Rico et al. [14] reported that grain yield of wheat increased by 36.6% with 500 ppm of CeO2 NPs applied in the soil. In another study, however, authors observed opposite results in barley with the application of the same NPs under similar conditions. Barley seedlings exposed to 500 ppm CeO2 NPs did not form seeds [23]. In rice grains, CeO2 NPs decreased Fe, sulfur (S), prolamin, glutelin, lauric and valeric acids, and starch content [120]. CeO2 NPs (800 mg kg-1) reduced cucumber yield by 31.6% [122]. In addition, Zhao et al. [123] reported that CeO2 and ZnO NPs (400 and 800 mg kg1

of soil) altered the quality of carbohydrates, proteins and mineral nutrients of cucumbers. More

recently, Zhao et al. [124] reported that maize yield was reduced by 38% and 49% with CeO2and ZnO NPs, respectively, and these NPs also altered the quality of corn by altering the mineral elements in cobs and kernels. Similar results were observed in soybean plants exposed to CeO2and ZnO NPs applied in soil [118]. In addition, CeO2 NPs decreased the Mo concentration in cucumber fruits and altered non-reducing sugars, phenolic content, and fractionation of proteins

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[123]. TiO2 NPs reduced K and P in cucumber fruits [27]. In tomato fruits, Ag NPs increased the potassium (K) content while reducing magnesium (Mg), phosphorus (P), and S content [19]. In summary, grain/fruit yield and quality were significantly affected when plants were exposed to different types of NPs in alternative time and dose-dependent manners. However, these studies are limited and there is a need to fully understand whether the decrease in fruit/grain yield and quality are indicators of NPs toxicities in plants. In general, data regarding the toxic effects of NPs on grain yield, development and quality are not adequate; more detailed studies are needed regarding the effects of NPs on grain/fruit development and quality of many crop plants. In these studies, specific endpoints should be included related to grain yield parameters, number, and mass of fruits/grains, as well as for nutritional content such as carbohydrates, proteins, amino acid, and metal. Long-term experimental conditions could adequately assess the grain/fruit quality and nutritional status and molecular level study may also be instructive.

5. Mechanisms of nanoparticle toxicity in plants In above section, we reported that NPs caused toxicities in crops and as a result decreased the crop growth, biomass, grain yield, and quality. This reduction in growth and yield might be due to different NP-mediated toxicity mechanisms at the soil and plant levels. A good understanding of these toxicity mechanisms is crucial for reduction of the toxic effects of NPs on crops. To date, the mechanisms of NPs-mediated toxicity in plants have been extensively studied [30, 35, 55, 102, 122]. At the soil level, these toxicity mechanisms may include physical damage to roots due to adsorption of NPs on the root surface and alteration of bacterial communities in the soil, which indirectly affect crop growth. On the plant level, these mechanisms may include genotoxicity, alteration in mineral nutrient uptake by plants, ROS generation, which reduces photosynthesis, and gas exchange and may result in decreased plant growth and biomass. In the following sub-sections, these mechanisms are described in detail with the support of published reports.

5.1. Indirect changes in the growth medium Crop growth is not only affected by the direct toxicity of NPs but may also be affected by indirect changes in the growth media, which is probably another factor in the toxicity of NPs to crops [35, 38, 125]. Soil health is indicated by the activities of soil microbes. NPs could alter soil 15

bacterial communities in planted soils as compared to unplanted soils which impact crop growth and yield [37]. It has been widely reported that ENPs affected soil microbial activities and diversity which ultimately affected crop growth and biomass (Reviewed by Simonin and Richaume [165]. Furthermore, CeO2 and TiO2 NPs disrupted bacteria legume symbiosis in soybean and pea plants, which may compromise crop yield [126-128]. However, detailed research is needed to understand the impacts of NP-symbiosis with bacteria. Dimkpa et al. [38] reported that Pseudomonas chlororaphis O6 (PcO6) increased the production of siderophore by 17% under ZnO NPs exposure, as compared to without NPs exposure. PcO6 decreased uptake of Zn and Fe by 58 and 18% respectively in bean plants suggesting that soil bacteria could reduce the uptake of essential nutrients by plants under NP exposure. Ma et al. [36] proposed that organic acids, extruded from root cells, induced the dissolution of La2O3 NPs at the root surface of cucumber plants, which might play an important role in NPs phytotoxicity. Certain NPs could cover root surface and as a result, water movement is reduced leading to water stress in plants. For example, TiO2 NPs decreased water transport capacity of the primary root cell walls of maize by depositing at the root surface and as a result decreased leaf transpiration [125]. Wang et al. [35] observed the aggregation of CuO NPs on the root surface of rice plants, which caused physical damage to roots. In addition, different dispersion agents have been used for the dispersion and stabilization of NPs. These dispersion agents may also cause toxicities in plants depending upon their properties and nature of the experiment [169-170].

5.2. Genotoxicity The interaction of plant cells with metal and metal oxide NPs caused genotoxicity in plants by the modification of plant gene expression [28, 31, 129-130]. Recently, studies on genotoxicity caused by NPs in important food crops have been widely reported [30, 32, 102, 131-133]. Rajeshwari et al. [135] observed a gradual decline in the mitotic index in onion root tips treated with Al2O3 NPs. Abou-Zeid and Moustafa [134] observed cytological changes caused by Ag NPs in root tips of germinated seeds, of wheat and barley. Authors reported that Ag NPs seed pretreatment caused chromosomal aberrations, chromosomes aneuploidy, binucleate cells, deletion chromosomes, deformed nuclei, micronuclei, chromosome fragments, and sticky chromosomes at metaphase and anaphase. In addition, the mitotic index significantly increased in the tested plants compared to the control. Patlolla et al. [129] reported that Ag NPs 16

significantly increased the number of chromosomal aberrations and decreased the mitotic index in root tips of faba bean. Similarly, Ag and ZnO NPs (22, 75, and 100 ppm and below 100 nm size) impaired stages of cell division, disturbed metaphase, caused multiple chromosomal breaks and cell disintegration in root tips of onion [32-36]. Ag NPs (10 mg L-1 seed priming for 4 h, size of 10 nm) altered expression of several proteins involved in primary metabolisms and cell defense in shoots and roots of wheat plants [34]. Mirzajani et al. [102] studied the effect of AgNPs suspension on rice from a proteomic point of view using gel-base combined Nano LC/FTICR MSMS. The authors identified the 28 NPs responsive (decrease/increase in abundance) proteins, which are mainly involved in transcription and protein degradation, cell wall and DNA/RNA/protein direct damage, and cell division. Nair and Chung [105] observed Ag NPs mediated differential transcription of genes related to oxidative stress tolerance in shoots and roots of rice seedlings, which showed induction of oxidative stress tolerance mechanisms in rice plants. Ag NPs altered the transcription of antioxidant and aquaporin genes in A. thaliana [105, 143]. Syu et al. [144] reported that in A thaliana, Ag NPs activated the gene expression involved in cellular events, including cell proliferation, metabolism, and hormone signaling pathways The CuO NPs altered the expression of genes associated with root growth of rice plants and damaged the DNA in radish and rye grass [28, 35]. In addition, Nagaonkar et al. [132] observed a gradual decline in mitotic index and an increase in abnormality index in root tips of onion treated with CuO NPs (40 to 100 mg L-1). Nair and Chung [104] observed that CuO NPs (100500 mg L-1) caused a significant inhibition of CAT and APX genes in roots of Indian mustard (Brassica juncea L.) while the expression of these genes was not changed in shoots. Similarly, different concentration of CuO NPs up-regulated the CuZn-SOD gene in roots of chickpea but did not change the APX gene in shoots and roots [136]. The expression levels of PAL, C4H, and CAD genes were significantly up-regulated in soybean roots exposed to CuO NPs (100, 200, and 400 mg L-1) for 14 days [137]. Similarly, CuO NP stress caused a significant induction of genes related to oxidative stress responses, sulfur assimilation, glutathione, and proline biosynthesis [137]. Tumburu et al. [145] reported that exposure to 12 d of either TiO2 or CeO2 NPs altered the regulation of 204 and 142 genes in A thaliana, respectively. In maize, TiO2-NP (0.2, 1.0, 2.0, and

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4.0%) treatments for 24 h followed by germination for 72 h led to a significant increase in chromosomal aberrations and a decrease in mitotic activity in root tip meristem [141]. The ZnO NPs induced several kinds of root apical meristem mitotic aberrations, chromosome stickiness, bridges, and breakages, in a concentration- and time-dependent manner in garlic [138]. Similar results were observed in onion root tips treated with ZnO NPs [139-140]. In A thaliana, a model plant, zerovalent iron NPs caused a significant increase in levels of the H+ATPase isoform, responsible for stomatal opening, AHA2, as compared to control plants [142]. The above studies showed in-depth molecular mechanisms underlying plant responses to metal and metal oxide NPs. However, genotoxicity studies of metal and metal oxide NPs in crop plants are limited. In addition, most of the studies were conducted in vitro and in vivo might be helpful to understand the mechanisms behind the genotoxic effects of NPs in crop plants.

5.3. Alteration in mineral uptake and assimilation Absorption of adequate amounts of essential mineral elements, mainly during the early growth stages, is required for normal crop growth and development. Several studies revealed that metal and metal oxide NPs affect mineral nutritional status of many crop plants [19, 38, 55, 98, 146]. For example, foliar application of Ag NPs (0-1000 ppm; size: 35 nm) decreased mineral elements (boron (B), Zn, Ca, P, potassium (K), Fe, Cu, Mn, Na and Mg) in different parts of tomato seedlings, which showed nutrient deficiency symptoms [149]. In transgenic cotton, CeO2 and SiO2 NPs altered the most nutrient elements (Fe, Cu, Mg, Zn, and Na) in shoots and roots [22, 55, 150]. Whereas Corral-Diaz et al. [150] reported that CeO2 NPs (0-500 mg kg-1 of soil for 40 days) did not affect mineral elements in different parts of radish, except Ni, which reduced with increasing NPs in the soil. In a study involving bean, CuO NPs (100, 250, and 500 mg kg-1 sand, size: 50 nm) decreased the shoot concentration of Fe, Zn, and calcium (Ca) while increased sodium (Na) [147]. Similarly, CuO NPs decreased manganese (Mn), P, Ca, and Mg in lettuce [148]. On the other hand, CuO NPs (5, 10, and 20 mg L-1, size: 10–100 nm) increased Cu, P, and S by 100%, 50%, and 20% respectively in alfalfa shoots and decreased P and Fe in lettuce shoots [98]. SnO2 NPs decreased K, Ca, Mg and S content in leaves and stems of tomato [19]. It has been widely reported that toxic metal ions decreased the mineral uptake by plants [166-167]. The reduction in

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mineral uptake by plants due to NPs might be due to release of soluble metals from NPs [15-17, 168]. The above studies showed that mineral uptake and accumulation in plants reduced when exposed to metal and metal oxide NPs. There is a need to examine how NPs reduce mineral uptake by roots including adsorption, absorption, and transport from the root surface to the xylem and translocation from the roots to the shoots or grains.

5.4. Enhancement in ROS generation and reduction in antioxidant enzymes Metal and metal oxide NPs caused oxidative stress in plants by producing reactive oxygen species (ROS). When dissolved, metal and metal oxide NPs may release ions and could interact with different groups of proteins and trigger formation of ROS [18, 20, 59, 151-152]. It has been reported that metal and metal oxide NPs caused more oxidative stress in a dose-dependent manner in many plants than bulk metal particles [20, 29, 135]. The Ag NPs increased electrolyte leakage twofold in wheat seedlings as compared to control [59]. In rice roots, CeO2 NPs (125 mg L−1 for 10 days) enhanced lipid peroxidation and electrolyte leakage, but did not affect the H2O2 content, while H2O2 generation was increased in roots at 500 mg L−1 NPs [120-121]. Similarly, in maize leaves, CeO2 NPs (400 or 800 mg kg−1 up to 15 days) treatments increased accumulation of H2O2 in different parts of the leaves, such as the phloem, xylem, bundle sheath cells, and epidermal cells [48]. In addition, CuO NPs (1.5 mM) increased foliar H2O2 (∼2–8-fold over control) and MDA (∼1.8-fold) concentrations in barley [18]. Similar CuO NP-mediated increases in H2O2 and MDA levels were observed in leaves of rice and chickpea seedlings [83, 136]. Similarly, CuO and ZnO NPs caused oxidative stress in wheat, which was evidenced by increased lipid peroxidation and oxidized glutathione in roots [15]. In tomato, NiO NPs (2.0 g L-1, size: ≤ 50 nm) caused a significant (122%) increase in intracellular ROS production in roots as compared to control [126]. To scavenge ROS, plants have evolved an antioxidant defense system as the first line of defense against ROS generation, which combines enzymatic and non-enzymatic antioxidants [22, 48, 119, 124, 153]. Under mild NP stress, the activities of key antioxidant enzymes increased in many crop plants [126]. However, under higher stress, the activities of antioxidant enzymes decreased, which might be due to oxidative burst in plants [152]. For example, the activities of superoxide dismutase (SOD), ascorbate peroxidase (APX), and catalases (CAT) increased in 19

wheat seedlings exposed to 200 mg L-1 Al2O3 NPs for 5 days, and at higher NPs concentration, the activities of antioxidant enzymes remained the same or decreased as compared to the control [155]. In addition, Ag NPs inhibited the activities of CAT and SOD in wheat leaves and roots [59]. CeO2 NPs, 500 ppm for 48 days, decreased the activities of CAT, dehydroascorbate reductase (DHAR), and glutathione reductase (GR) in barley leaves as compared to the control [23]. In cilantro (Coriandrum sativum L.) plants, CeO2 NPs (125 mg kg-1 of soil for 30 days) increased CAT activities in shoots and APX in roots [156]. Similarly, CeO2 NPs (≥500 mg L-1 in agar medium for 5 days) altered the activity of SOD in lettuce roots [29]. In barley, CuO NP, (1.0 and 1.5 mM for 20 days) enhanced the activities of APX, SOD and GR and decreased DHAR and monodehydroascorbate reductase (MDAR) activities in shoots [18]. Similarly, Nair and Chung [154] reported that CuO NPs (500 mg L-1) significantly increased the SOD activity in roots and shoots of Indian mustard, while the same NP concentration caused a significant decrease in APX activity in both shoots and roots. CuO and ZnO NPs (100 ppm) caused a significant increase in SOD, POD and CAT activities in roots of cucumber [110]. Faisal et al. [126] reported that NiO NPs (2.0 g L-1, size: ≤ 50 nm) increased CAT, GR and SOD activities, 6.8, 3.7, and 1.7 fold higher, respectively, in tomato roots as compared to control. In faba bean, TiO2 NPs did not change the antioxidant enzymes activities in shoots while in roots, GR activity decreased at 50 mg L-1 of NPs and APX activity decreased with 5 and 25 mg L-1 [30]. The NPs also induced the significant changes in soil enzyme activities such as protease, catalase, peroxidase, dehydrogenase, β-glucosidase, and acid phosphatase [21, 157]. The above studies showed that NPs caused oxidative stress as indicated by the production of ROS under NPs stress. Under mild stress, the plant defense system was affective to scavenge ROS production but at higher stress, plants failed to combat ROS generation due to severe oxidative bursts. Moreover, NPs-mediated increase or decrease in antioxidant enzymes activities might be due to differences in plants, kind and size of NPs, exposure duration, and experimental conditions. From the above studies, it might be concluded that plants could tolerate lower concentration of NPs by enhancing the activities of antioxidants that scavenge ROS and as a result, achieve equilibrium between ROS formation and detoxification. However, higher NP concentrations are highly toxic and cause an oxidative burst in plants and as a result, reduction in antioxidant enzyme activities was observed in plants.

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5.5. Reduction in photosynthesis and gas exchange parameters Oxidative stress in plants may interfere with the biochemical reactions and reduce photosynthesis and gas exchange possibly because of higher ROS production [158-159]. The effect of metal and metal oxide NPs on photosynthesis and gas exchange in food crops has been widely reported [18, 102, 134, 152, 159]. Seed priming with Ag NPs reduced the photosynthetic pigments and quenched chlorophyll fluorescence in wheat, soybean, and barley [59, 122, 134, 161]. Moreover, Ag NPs also reduced the photosynthetic pigments in shoots of rice plants [102]. Application of CeO2 NPs (400 or 800 mg kg−1) at 10, 15, and 20 days post germination did not affect the net photosynthetic rate, transpiration rate, and stomatal conductance of maize leaves [48]. Similar results were observed in radish and cucumber plants exposed to CeO2 NPs grown in soil under controlled conditions [122, 150]. Excess metal and metal oxide NPs caused a significant decrease in total chlorophyll content in many crop plants such as Indian mustard, pea, and soybean [137, 152, 162-164]. In crop plants, the toxic effects of metal and metal oxide NPs on photosynthetic pigments also depend upon the duration of the applied stress [18]. For example, Shaw et al. [18] reported that no apparent change in chlorophyll contents in barley leaves were observed under CuO NPs stress (0.5, 1.0, and 1.5 mM suspensions with size < 50 nm) on the 10th day of growth, but the chlorophyll contents suddenly decreased on the 20th day of growth, irrespective of concentrations, as compared to control. Application of ZnO NPs at 800 mg kg-1 of soil reduced the maize leaf net photosynthesis by 12% and stomatal conductance by 15% as compared to control [124]. This showed that the plants could tolerate NPs toxicity up-to certain period of time and prolonged exposure to NPs could cause toxicities which might be due to negative effects of NPs on plant defense system such as antioxidant enzymes.

6. Conclusion and perspectives The above studies showed that metal and metal oxide NPs have both positive and negative effects on growth, yield, and quality of important agricultural crops. The inclusion of NPs in the growth media increased the concentration of NPs in different parts of plants. Few studies showed that NPs increased the seed germination, growth and biomass of plants. On the other hand, the findings from several studies showed that accumulation of NPs in plants reduced the seed germination, growth, and yield of crops. This reduction in growth and yield might be due to 21

different mechanisms occurring at both growth-medium and plant levels. At the growth medium level, NPs might physically damage the roots due to aggregation on the root surface, altered soil bacterial communities, and increased the concentration of co-contaminants in plants due to their interactions in the growth media. At the plant level, toxicity mechanisms include alteration in mineral nutrient uptake, genotoxicity, production of ROS, which decreased antioxidant enzyme activities, and decreased photosynthesis and gas exchange. In conclusion, NPs caused toxicity in plants at the physiological, morphological, bio-chemical, and molecular level the toxic effects of NPs on crop plants vary greatly with plant species, growth stages, method, and duration of exposure, along with other factors. The above studies further suggest that NPs could be transferred into the food chain through grains/fruits of crops. Future critical research efforts are needed to understand the NPs mechanisms in plants and soil including the following 

Although a large number of studies are related to the effects of metal and metal oxide NPs on crops of agricultural importance, there is still a need for more investigation of the effect of NPs to better understand the mechanisms of NPs positive and toxic effects under various conditions.



Moreover, studies related to the effect of NPs and other contaminants on plant growth and physiology of plants are rare. Our environment does not isolate factors so the effect of co-contamination, including NPs, in different growth media on the growth of plants will be helpful to understand the interactions.



In addition, at the soil level, detailed studies are needed to examine the interaction of NPs with mineral nutrients in the soil (both solution and solid phases) and interaction with soil organic matter. Furthermore, there is urgent need to study the effects of NPs on soil chemical characteristics such as soil and soil solution pH and cation exchange capacity of soil (CEC). Such studies may help to obtain deeper insight into the toxic effects of NPs on crop plants and more adequately address the associated safety concerns in the food chain.



More in depth studies are needed to evaluate the NPs speciation in the soil and soil solution and in the different parts of the plants to identify the NPs toxicity mechanisms in plants and soil.

Acknowledgements 22

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37

Decrease in grain yield and quality

•

• Alterations in metabolic pathways

Decrease in • • •

Increase in

Shoot length, leaf area Biomass Photosynthesis and gas exchange attributes

• • •

ROS generation Antioxidant enzymes Damage to lipids •

Alteration in • • •

Root length Root biomass Mineral nutrient uptake

Increase in NPs concentration in grain, shoot and roots

NPs in soil

Alteration in root tip morphology and cell division

Effect on seed germination

Agrichemicals, accidental release, leakage from landfills, commercial products, NPs use for remediation purposes, atmospheric fallout

Figure 1. Possible sources of nanoparticles (NPs) in the soil and their effects on growth and physiology of plants. ROS = reactive oxygen species.

38

Table 1: Effects of NPs on plant morphology and physiology Plant species Wheat

NPs size/range and concentration used Ag, size < 10 nm; Conc. 1 and 10 mg L-1

CuO, ZnO; size < 50 and < 100 nm, respectively; 500 mg kg-1 for each

Growth media and exposed duration Seeds germinated on filter papers moistened with 5 mL of test solutions for 5 days in dark In sand matrix; 14 days

Effects

References

NPs decreased the shoot and root length and fresh biomass. Higher treatment altered the expression of several proteins mainly involved in primary metabolism and cell defense in plants NPs reduced the root and shoot length and biomass. NPs decreased the chlorophyll contents and increased the POD and CAT activities in roots as compared to control

[34]

[15]

CuO; size 25-80 nm Conc. 5.0, 10, 100, and 200 mg kg-1

Agar culture media; 48 h

The plant uptake and adsorption of CuO increased with increasing exposure concentrations

[51]

CuO; size < 100 nm Conc. 0 to 1000 mg L-1

Agar culture media; 2 days

Seedling growth significantly decreased with increasing NPs concentration in the medium. The 2-d median

[100]

effective concentrations of NPs were 570 mg L-1. Fe2O3, size 20 to 30 nm Conc. 0, 100, 500, 1000, 5000 and 10000 ppm TiO2, ZnO; size < 100 nm; Conc. 10 and 5 g kg-1, respectively

Rice

TiO2, ZnO; size 14 to 655 nm; Conc. 100 mg L-1 Ag; size < 25 nm; Conc. 1000 mg L-1 Ag; size < 100 nm; Conc: 0, 30, 60 µg mL-

25 seeds were placed on paper in petri dishes with 3 ml of each NPs conc. and germinated seeds were noted daily for 8 days Plants were grown for 5 months in lysimeter

100 ppm NPs increased the seed germination as compared to the control while NPs reduced the seed germination with higher treatments

[89]

NPs decreased the growth and yield of plants

[21]

15-day-old seedlings transferred to vials containing NPs suspension 12 days of treatment to 3 weeks old seedlings 7, 14, and 21 days of treatments in phytotrons to

NPs with diameter of > 140 nm could not entered in the wheat roots. NPs did not affect the seedling growth, photosynthesis and transpiration of wheat plants NPs damaged the root cell walls and vacuoles of plants

[57]

30 µg NPs mL-1 of solution improved the plant growth while higher concentration reduced the shoot and root

[103] [102]

39

1

7 day-old-plant

Ag; size < 20 nm; Conc. 0, 0.2, 0.5 and 1 µg mL-1

Germinated seedlings were placed onto Whatman #1 paper bridges in test tubes containing 4 mL of 1/4 strength Hoagland’s medium for one week Seeds were placed in petri dishes with 5 ml of each NPs concentration for 10 days

CeO2, size < 8 nm; Conc. 0, 62.5, 125, 250 and 500 mg L-1

CuO; size < 50 nm; Conc. 0.5, 1.0, 1.5 mM CuO; size = 40 nm; Conc. 100 mg L-1

TiO2, ZnO; size < 100 nm; Conc. 100, 500, 1000 mg L-1 for each

Maize

Cotton pads soaked with dissolved CuO-NPs in plastic trays Twenty-one-day-old uniform seedlings were exposed to CuO for 14 days in hydroponics Soaking for 1, 2 and 3 days in dark and then germinated for 7 days after treatments

growth and damaged the root cell morphology and structural features NPs significantly reduced the root elongation, shoot and root fresh weights, total chlorophyll and carotenoids contents. ROS production increased in plants in a dose dependent manner

[105]

62.5 mg CeO2 L-1 decreased H2O2 generation as compared to the control while higher NPs concentrations increased the H2O2 generation. 125 mg CeO2 L-1 enhanced the lipid peroxidation and electrolyte leakage as compared to the lower NPs concentration and control NPs exposure decreased the seed germination and seedling growth. NPs caused the severe oxidative burst in plants.

[121]

NPs moved into the root epidermis, exodermis, and cortex, and they ultimately reached the endodermis and transported from roots to leaves and Cu-citrate complexes were observed in the root cells ZnO NPs reduced the root length and number of roots, whereas TiO2 NPs has no effect on root length

[74]

[75]

[83]

[93]

CuO; size = 20-40 nm; Conc. 100 µg mL-1

Fifteen-day-old seedlings were exposed to CuO for 15 days in hydroponics

Seed germination was not affected but NPs inhibited the growth of maize seedlings

Nanosilica, size = 20-40 nm; Conc. 0, 5, 10, 15, and 20 kg ha-1

Field trial with different treatments for 20 and 40 days

NPs increased the seed germination, root length, shoot length and leaf area of maize seedlings. Photosynthetic pigments and plant dry biomass increased with NPs as compared to the control

[106]

ZnO; size < 10 nm;

10 seeds were germinated

NPs reduced the root length and altered the root anatomy

[101] 40

Conc. 0-1000 µg mL-1

Chickpea

Soybean

in each petri dishes containing 5 ml of test chemical for 7 days ZnO; size < 30±10 nm; 10 seed per petri dish Conc. 0, 10, 100 containing filter paper and1000 µg mL-1 soaked with 5 ml of test medium for 5 days in dark ZnO; size < 30±10 nm; Seed were sown in sandy Conc. 0, 100, 200, loam soil for 30 days -1 400,800 mg kg TiO2; size < 100 nm; Seed were soaked with NPs Conc. 0.2, 1.0, 2.0, and for 24 h and then allowed 4.0% to germinate in petri dishes for 72 h CuO; size < 50 nm; 15 seeds per dish Conc. 0, 800, 1000, containing filter paper 1500, 2000 µg mL-1 soaked with 5 mL of test solution for 5 days in dark CuO; size < 50 nm; Plants were grown in Conc. 0, 50, 100, 200, culture vessels placed 400 and 500 µg mL-1 growth chamber for 10 days TiO2; size < 100 nm; Plants were grown in Conc. 5 mg L-1 growth chamber for 21 days and NPs sprayed twice on the 12th and 16th days CuO; size < 50 nm; Plants were grown in Conc. 0, 50, 100, 200, Murashige and Skoog 400, and 500 µg mL-1 medium in growth chamber for 14 days ZnO; size < 50 nm; Conc. 0, 50, or 500 mg kg-1

Plants were grown in a standard soil microcosm study for a period of 8–9 weeks in greenhouse

NPs reduced the root length by 17% as compared to control while Zn concentration significantly increased in roots

[40]

Zinc concentration increased with increasing NPs in soil.

[52]

NPs delayed seed germination and root length reduced only with higher treatment. Root mitotic index reduced and chromosomal aberrations increased in plants

[141]

Seed germination was not checked but root growth was inhibited above 500 ppm and root necrosis was occurred

[99]

NPs decreased the shoot and root growth and increased ROS generation and caused cytotoxicity in root cells

[104]

NPs decreased H2O2, MDA and electrolyte leakage index as compared to the control but the response varied between studied genotypes

[171]

Exposure to 500 mg L-1 of NPs significantly reduced the shoot growth, weight, and total chlorophyll content. However, the root length and fresh weights were significantly reduced at all concentrations while H2O2 contents increased Roots and shoots lengths, surface area and volume decreased under NPs treatments compared to control. Plants with higher treatment did not form seeds

[17]

[113]

41

Tomato

Barley

Rapeseed

Indian mustard

Cotton

Ag; size 10-15 nm; Conc. 0, 50, 100, 1000, 2500, 5000 µg mL-1 Ag; size 35 nm; Conc. 0, 250, 500, 750, and 1000 µg mL-1

Six weeks-old-seedlings in hydroponics under greenhouse conditions for 5 weeks Plants were grown in silt loam soil and at four leaf stage, NPs were sprayed on weekly basis for 14 weeks CeO2; size 231±16 nm; NPs were mixed Conc. 0, 125, 250, and thoroughly in the potting 500 mg kg-1 of soil soil before transplanting 9day-old seedlings CuO; size < 50 nm; water soaked seeds were Conc. 0.5, 1 and 1.5 allowed to germinate on mM suspension of similar cotton pads soaked CuO with respective CuO-NPs suspension for 20 days ZnO; size < 50 nm; Seeds were allowed to Conc. 0, 5, 10, 25, 50, germinate in petri dishes 75, 100, 125, 250, and containing respective NPs 500 µg mL-1 suspension for 6 days ZnO; size < 50 nm; Hydroponic conditions for Conc. 0, 100 µg mL-1 2 months CuO; purity of 99.9%; surface area of 29 m2 g1 ; Conc. 0, 20, 50, 100, 200, 400 and 500 mg L-1

Half strength semi solid Murashige and Skoog medium in growth chamber for 14 days

ZnO; size <100 nm; Conc. 0, 200, 500, 1000, 1500 µg mL-1 SiO2; size <30 nm; Conc. 0, 10, 100, 500, and 2000 mg L-1

Hydroponic conditions and 13-day-old plants were exposed to NPs for 96 h Hydroponic conditions and 21-day-old plants were exposed to NPs for 30 days

Mature plants was demonstrated by reduced root elongation, lower chlorophyll contents, higher superoxide dismutase activity and less fruit productivity

[60]

The amount of mineral elements, potassium and iron, decreased in leaf and deficiency symptoms appeared on leaves

[149]

NPs increased the plant height, chlorophyll contents, dry biomass and yield components. NPs also increased oxidative stress and K leakage from plants

[23]

Shoot and root length and biomass decreased by NPs exposure in dose dependent manner. H2O2 and MDA contents increased in plants especially at higher treatments. NPs also increased the antioxidant enzymes activities as compared to the control NPs exposure decreased the shoot and root length and dry masses of plants

[18]

NPs decreased the plant growth and biomass and negatively affected root and leaf anatomy and ultrastructure NPs decreased the shoot and root length, leaf size and root system architecture was changed. Photosynthetic pigments decreased while oxidative stress increased upon NPs exposure

[112]

NPs decreased the shoot and root length and biomass. ROS generation and activities of antioxidant enzymes increased by NPs exposure NPs decreased the plant height and shoot and root biomass in a dose dependent manner.

[152]

[63]

[154]

[22]

42

Cucumber

CeO2; Conc. 0, 100, 500, 2000 mg L-1

Hydroponic conditions and 21-day-old plants were exposed to NPs for 52 days

ZnO; size <50 nm; Conc. 0, 2000 mg L-1

Plants were grown in loamy sand soil for 8 weeks Pot exp. in soil and 5-dayold plants were exposed to NPs for 4 weeks

CuO and ZnO; size < 50 nm; Conc. 0, 10, 50, 100, 500, and 1,000 mg L-1 CuO; size < 100 nm; Conc. 0, 100, 200, 400, and 600 mg L-1

Alfalfa

ZnO; size = 10 nm; Conc. 0, 250, 500, 750 mg kg-1 CuO; size = 10 – 100 nm; Conc. 0, 5, 10, 20 mg L-1

Onion

Sorghum

ZnO; size = 20 nm; Conc. 0, 10, 20, 30, 40 mg L-1

CuO; size = 17-93 nm; Conc. 10, 20, 40,60, 80 and 100mg L-1 Ag; size = 5 - 25 nm; Conc. 0, 5, 10, 20, and

Seeds were soaked in water and then with NPs for 6 h placed in petri dishes containing suspension solution for 7 days Plants were grown in soil amended with NPs for 30 days NPs were exposed for 15 days to 10 day-old hydroponically grown plants Seed were sown in petri plats containing filter paper soaked with NPs. Plants were harvested after 10 days of treatments Solid meristematic root tips were directly placed in NPs suspensions for 1, 2, 3 hrs 2 day-old seedlings were placed in agar media

NPs decreased the plant height and shoot and root biomass decreased in a dose dependent manner. Contents of most nutrient elements (Fe, Ca, Mg, Zn and Na) in roots decreased with NPs exposure Soil enzymes activities decreased due to NPs. Shoot and root length and biomass decreased and Zn concentration increased in plants upon NPs exposure Plant biomass significantly decreased to 75% and 35% than that of control with highest concentration of CuO and ZnO NPs, respectively. Both NPs significantly increased antioxidant enzymes activities in plants NPs decreased the seed germination and root elongation in a dose dependent manner. 34 proteins were differentially expressed in cucumber seeds after exposure to CuO NPs as compared to control NPs decreased the shoot and root length and biomass. NPs also decreased the leaf area and leaf protein contents. The CAT activities in root increased while not affected in stem and leaf upon NPs exposure NPs decreased the root length while increased the Cu, P, and S concentrations in shoots. The CAT activity decreased in both shoots and roots while APX activity increased in roots upon NPs exposure Seed germination increased at lower NPs concentrations but decreased at higher concentrations. Overall shoot and root length and biomass were decreased upon NPs exposure. In root tips, mitotic index decreased and chromosomal abnormalities increased especially with higher NPs concentrations Mitotic index decreased and chromosomal abnormalities increased with increasing NPs concentrations and treatment duration NPs inhibited the plant growth in agar media but the plant growth was not affected in soil media. Properties of NPs

[55]

[157]

[110]

[25]

[12]

[98]

[139]

[132]

[96]

43

40 µg mL-1 in agar and 0, 100, 300, 500, 1000, and 2000 mg kg-1 in artificial soil

containing treatments for 2 days. Seeds were sown in soil and were analyzed after 5 days

changed in soil but not in agar media.

44