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Abstract

Nanotechnology has been broadly used in the agricultural system since last few decades throughout the world, but still facing some challenge to be used as nano-fertilizers, because of its toxicity and hazardous effects on the environment as well as on the human health. Nevertheless, the nanomaterials could serve as a potential tool for the agriculturally important crops. They have shown varied effects on the morphological and physiological changes, uptake and translocation in different parts of plants. Application of various nanoparticles showed dose dependent responses of the different agriculturally cultivated crops and it may vary from plant to plant and species to species. The aim of this review article is to focus effect of nanoparticles on the morphological and physiological changes in plants, their uptake and accumulation in the various biological systems and their consequences on the cellular and genetic toxicity in plants.

Key words

metal oxide nanoparticles, plant growth, seed germination, uptake, translocation

Introduction

Plants are the key components of the biological system and the main source of metabolic pathways and channels occur into the food chain [1]. The nanoparticles synthesized by biological means are advantageous compared to chemical or microbial synthesis because of their nontoxic, rapid and cost-effective method [2]. The nanoparticles synthesized from the plant materials are referred as biogenic or phytosynthesized nanoparticles. The phytosynthesized nanoparticles have distinct assets viz., greater surface area and stability, uniform shape and size compared to physically or chemically synthesized methods (Figure 1). The phytosynthesised nanomaterials are the major concern for the researchers, whose are still trying to optimize the nanomaterials to be used as nano-fertilizers for agriculturally important crop plants in respect to the guarantee of their safe use [3]. Various nanomaterials used in modern agricultural practices have both positive and negative impacts on the cultivated crop plants. Yang and Watts [4] observed the effect of very low concentration of alumina nanoparticles on the carrot, cabbage, corn, cucumber and soybean. They concluded that alumina nanoparticles have shown phytotoxic effect on all the tested plants. Similarly, Lin and Xing [5] also found that the exposure to higher concentrations of aluminium, alumina, multi-walled carbon nanotube, zinc and zinc oxide nanoparticles on root development and seed germination has a phytotoxic effect on the tested plant species. However, the effect of the phytotoxicity of functionalized and non-functionalized single-walled carbon nanotubes on the root growth and development of cabbage, carrot, cucumber, lettuce, onion, and tomato has been investigated by Canas et al. [6]. They concluded that amongst all the various tested crop plants the phytotoxicity vary greatly in between the functionalized and non-functionalized single-walled carbon nanotubes, which may also lead into an adverse effect of the root growth and development.

Apart from this dark shadow, some researchers also highlighted the positive impacts of the nanoparticles on the growth, development and physiological parameters of the plants [7-11] investigated that the foliar or seed treatments of TiO₂ NPs could enhance the growth of spinach. Similarly, Racuciu and Creanga [12] found that application of TMA-OH coated Fe₂O₃ NPs increase the growth of popcorn at lower concentrations. However, Panwar et al. [10] observed the effect of foliar treatments of ZnO NPs in the range of 10-100 ml/l on the seedling germination, growth and biomass production of tomato and stated that the application of 20 mg/l of ZnO NPs showed comparatively better seed germination, growth and biomass production of tomato than other tested treatments. There are some reports of previous researchers, which may enrich our knowledge about the interactions of nanoparticles with plants, but still few reports or no comprehensive report is available, which may directly focus on the effect of nanoparticles on the morphological and physiological changes induced by the nanoparticles on the plants. Thus, the aim of this review article is to focus on the morphological and physiological changes, uptake and translocation in different parts of plants and their consequences on the cellular and genetic toxicity in plants.

Effect of nanoparticles on the morphological and physiological changes in plants

The interaction of nanoparticles with plants had varying effects on the morphological and physiological parameters, but it may be contingent upon the plant species, types and concentrations of nanoparticles [5]. The nanoparticles had the ability to increase the rate and percentage of seed germination, root and shoot biomass of several crop plants [13,14]. The increase in the morphological traits has been directly correlated with the increase in the physiological attributes like photosynthetic activity, N and P metabolism, enhance in enzyme activities [7,9,15,16].

Effect of nanoparticles on the morphological changes in plants

A morphological study conducted on B. monnieri revealed that Ag NPs caused an insignificant decrease the root and shoot length by the desertion of air chamber in root cortex and variation in the shapes, sizes and distribution of xylem elements into the stem (Figure 2) [17]. Song et al. [15] found that application of TiO₂ NPs improved the plant growth at lower concentration on Lemna minor. Similarly, Riahi-Madvar et al. [18] reported that root growth is only influenced by the application of Al₂O₃ NPs at lower concentrations, while, other morphological properties remain unchanged compared to control in wheat. The reason behind elaboration was the selective permeability of seed coats which may challenge the roots with excess in nanoparticles and low rate of transportation of the nanoparticles in the shoot. However, Giordani et al. [19] observed the effect of TiO₂ NPs and Al₂O₃ NPs on tomato seedlings after one week of treatment in the hydroponics cultural system. They concluded that seedlings grown with high concentration of TiO₂ NPs had an abnormal proliferation of root hairs compared to the control or seedlings exposed to Fe₃O₄ NPs and no symptoms of toxicity has been detected in the nanoparticles treated plants.

It is evident from the study of Raliya and Tarafdar [16] that the use of ZnO NPs increases the biomass, shoot length, root length and root area by 27.1%, 31.51%, 66.29%, and 73.52%, respectively over control treatments on cluster bean. However, Sindhura et al. [20] reported an increase in leaf length (22.6% and 17.6%), leaf width (17.7% and 20.69%), number of leaves (51.9% and 53.0%) and plant height (39.8% and 40.21%) compared with control in 30 and 60 days after sowing on groundnut under pot condition, while, in vitro exposure with citrate coated Al₂O₃ NPs and ZnO NPs on mays and cabbage was observed by Pokhrel and Dubey [21]. They concluded that there is a significant change in the meta-xylem count in mays with citrate coated Ag NPs, AgNO₃, and ZnSO₄ treatment, but has no effect with ZnO NPs, and the seed germination and root elongation exposed towards the lower toxicity of nanoparticles in both crops as compared to free ions. The reports of the earlier researchers clearly indicated that the effect of nanoparticles varied for different morphological attributes on plants [16,22-24]. Thus, we summarized some recently published reports for the effects of nanoparticles on the morphology of plants in tabular forms (Table 1).

Table 1. Effect of nanoparticles on the morphological changes in plants.

Types of NPs	Concentration	Morphological changes	References
TiO2 ZnO	10g/kg 5g/kg	The biomass of wheat are reduced by the application of both nanoparticles under field conditions. The TiO2 NPs were adherent to cell walls of plants and retained in the soil for long periods. However, the ZnO NPs dissolved in the soil, and enhance the zinc uptake by plants.	Du et al. (2011)
Fe3O4, TiO2, Carbon	100-5000 μg/ml	Cucumber seed germination was inhibited by all the nanoparticles but less inhibition of seed germination was recorded for carbon nanoparticles compared to other tested nanoparticles.	Mushtaq (2011
Ag	10-100 ppb	It is evident from the results that the various concentrations of Ag NPs have not significantly affected the seed germination of B. monnieri.	Krishnaraj et al. (2012)
ZnO	10-50 mg/l	ZnO NPs caused a concentration dependent inhibition in root length of garlic. The total percentage of abnormal cells increased with the increase of ZnO NPs concentration and the prolongation of treatment time.	Shayamurat et al. (2012)
Ag	40 mg/l	Broken epidermis and root cap were observed in Lolium multiforum.	Yin et al. (2012)
Fe3O4, TiO2	50-500 mg/l	Root morphology showed that initiation in the formation of root hairs on tomato in hydroponic condition.	Giordani et al. (2012)
Ag	10 mg/l	Seedlings treated with different concentrations of PVP coated Ag NPs or AgNO3 for 5 days showed an increase in root length of Eruca sativa.	Vannini et al. (2013)
ZnO	10 mg/l	Foliar spray of ZnO NPs significantly increased the plant biomass, shoot length, root length and root area on cluster bean.	Raliya and Tarafdar (2013)
MWCNT	20-2000 mg/l	Results showed that root and shoot length of red spinach, lettuce, and cucumbers were significantly reduced by the exposure of multi-walled carbon nanotubes only at higher concentrations (1000 mg/l and 2000 mg/l) after 15 days inoculation. Similar toxic effects occurred regarding cell death and electrolyte leakage. Moreover, red spinach and lettuce were most sensitive to MWNTs, followed by rice and cucumber.	Begum et al. (2014)
Ag	10 mg/l	Results showed that the exposure of wheat seedlings to Ag NPs adversely affected the seedling growth and induced morphological modifications in root tip cells.	Vannini et al. (2014)

Effect of nanoparticles on the physiological changes in plants

Use of various nanoparticles had a significant role in the physiology of crop plants. It may directly or indirectly influences the physiological parameters by the alteration in the formation of reactive oxygen species, catalase, peroxidase, superoxide dismutase activities, chlorophyll, phenol and leaf protein contents. Krishnaraj et al. [17] reported that Ag NPs treated B. monnieri plants have higher protein and carbohydrate contents and lower total phenol contents, catalase and peroxidase activity. It is also obvious from the report of Song et al. [15] that the application of TiO₂ NPs at lower concentration (200 mg/ml) increases the chlorophyll, peroxidase catalase, superoxide dismutase activities, and malondialdehyde contents on Lemna minor compared to bulk by the elimination of reactive oxygen species from the plant cells, but at higher concentrations (500 mg/ml), the TiO₂ NPs causes a severe disruption of cell membrane in the culture media.

Similarly, Raliya and Trafadar [16] found that foliar application of ZnO NPs at lower concentration (10 ppm) increased the chlorophyll, phosphorus and total soluble leaf protein concentration on cluster bean. However, Sindhura et al. [20] found increased acidic phosphatase activity, alkaline phosphatase activity and dehydrogenase activity in all the treatments compared to control in 30 and 60 days after sowing on groundnut under pot condition. Moreover, Li et al. [29] observed the various physiological parameters of Fe₂O₃ NPs on watermelon, and proved that a significant amount of Fe₂O₃ NPs has been suspended in a liquid medium, which has been directly taken up and translocated into different parts of the plant. Their experimental results showed that various concentrations of Fe₂O₃ NPs increased the seedling germination and growth attributes and seedling growth, and enhanced physiological parameters. Changes in CAT, SOD and POD activities due to Fe₂O₃ NPs were significantly higher compared to control treatments and the nanoparticle treatment (20 mg/l) had the most obvious effect on the increase of root activity, ferric reductase activity, root apoplastic iron content and plant biomass. They concluded that the suitable concentration (20 mg/l) of Fe₂O₃ NPs could not only increase the seed germination and seedling growth, but also improve the various physiological functions and resistance towards the several environmental stresses on watermelon. We have summarized some recently published reports for the effects of nanoparticles on the physiological changes of plants in tabular forms (Table 2).

Table 2. Effect of nanoparticles on the physiological changes in plants.

Types of NPs	Concentration	Physiological changes	References
TiO2	10-2000 mg/l	Exposure of Lemna minor to TiO2 NPs increased the activities of various enzymes (POD, SOD, and CAT) below concentration of 200 mg/l because of eliminating accumulated reactive oxygen species in plant cells. The	Song et al. (2012)
Al2O3	10-1000 mg/l	The activity of SOD and CAT were increased with the  treatments of Al2O3 NPs at a concentration of 200 and 500 mg/l.	Riahi-Madvar et al. (2012)
ZnO	10 mg/l	Treatment of cluster bean with foliar sprays of ZnO NPs caused a significant increase in chlorophyll content (276.2 %), total soluble leaf protein (27.1%), acid phosphatase (73.5%), alkaline phosphatase (48.7%), and phytase (72.4%) over control.	Raliya and Tarafdar (2013)
Fe2O3	20 mg/l	Increase in root activity, activity of catalase, peroxidase,  superoxide dismutase, chlorophyll, malondialdehyde  contents, ferric reductase activity, the root apoplastic iron content were recorded by the translocation of the significant amount of Fe2O3 NPs suspended in a liquid medium to various tissues of plants.	Li et al. (2013)
SNP ZnO	500-4,000 ppm	Application of various concentrations of both sulfur and zinc oxide nanoparticles in significantly increase the total lipids, proteins, amino acids, thiol and chlorophyll contents compared to untreated control but no significance difference has been observed among the treatments with various concentrations for both nanoparticles.	Patra et al. (2013)
TiO2	200 mg/l	Application of TiO2 NPs had a noticeable effect on chlorophyll a and b and carotenoid contents on Mentha.	Samadi et al. (2014)

Uptake and translocation of nanoparticles in plants

Lopez-Moreno et al. [32] tested the various concentrations of CeO₂ NPs on the growth of cucumber, alfalfa, tomato and corn seedlings and reported that the maximum growth (140%) was recorded at a concentration of 2000 mg/l and minimum growth (50%) at a concentration of 500 mg/l compared to control treatments. A few years later, Lopez-Monero et al. [33] observed the uptake, storage and differential toxicity of CeO₂ NPs in four edible plants through X-ray absorption spectroscopy. They concluded that the differential toxicity could be due to the physical and chemical interaction of nanoparticles with root structures and exudates. Recently, Birbaum et al. [34] exposed CeO₂ NPs as aerosol or suspension on corn leaves and stated that about 50 μg of cerium per gram of leaves was either absorbed or incorporated into maize leaves but there is no evidence of translocation of cerium into the newly developed leaves. These results clearly indicated that the absorption and the translocation ability of CeO₂ NPs are dependent on the plant species. Similarly, Zhu et al. [35] observed the effect of Fe₂O₃ NPs on the uptake, translocation and accumulation on pumpkin seedlings in hydroponic. They concluded that the signal for the uptake of Fe₂O₃ NPs is not only confined to plant parts, but also depend on the growth medium and the uptake of nanoparticles is species dependent process because no uptake has been recorded in lima bean.

Wang et al. [36] didn’t find any indication of Fe₂O₃ NPs uptake on the pumpkin and speculated that if the sizes of the applied nanoparticles are large then it directly affects the penetration of nanoparticles through cell walls and their transport across the plasma membranes. However, Li et al. [29] observed the effect of suspended Fe₂O₃ NPs in liquid medium on watermelon and stated that suspended nanoparticles has been directly taken up and translocated into various plant parts, which may result in the increase in seedling germination and enhanced physiological function to some degrees. The positive effects of nanoparticles increased quickly and then slowed with an increase in the concentration of the treatments.

Kurepa et al. [37] reported that an ultra-small TiO₂ complex with Alizarin red S nano-conjugates were directly up taken and translocated the nanomaterials into the seedlings of A. thaliana. They concluded that root of the experimental plants released mucilaginous substances, which may form a pectin hydrogel capsule around the root and playing a significant role in the inhibition or facilitation of the TiO₂ complexes with Alizarin red S. However, Asli and Neumann [38] reported that TiO₂ NPs is neither up taken nor translocated by the excised maize roots due to their large size.

The experiment conducted on rye-grass confirmed that the adsorption and accumulation of the ZnO NPs to the root surfaces [39]. The cross sectional transverse electron microscopy images of rye-grass root clearly showed the presence of ZnO NPs in the apoplast, cytoplasm and nuclei of the endodermal cells and the vascular system. Later, Lopez-Moreno [32] reported the uptake and accumulation of ZnO NPs on soybean seedlings with the concentration of 500 mg/l. They concluded that high concentrations of nanoparticles increased the probability of agglomerate formations which may restrict the passage of nanoparticles through the cell pore and resulted into the reduce uptake and accumulation of nanoparticles inside the plant tissues.

Doshi et al. [40] observed the Al uptake in red kidney beans when exposed Al NPs and their results showed that the Al concentration in the red kidney beans were not significantly different compared to untreated control treatments. However, Stampoulis et al. [41] investigated the uptake of Ag NPs in zucchini compared to bulk (control) treatments and stated that the silver concentration in shoots was higher, when the plants were exposed Ag NPs compared to bulk and concluded that release of silver ions from Ag NPs is accounted for an increase in the concentration of silver in shoots. Similarly, Haverkamp and Marshall [42] treated Brassica juncea with Ag NPs to find out the real mechanism behind the formation of nanoparticles by plants and stated that there is no accumulation of Ag NPs in any form in the plant tissues. However, Corredor et al. [43] investigated that when carbon-coated Fe₂O₃ NPs were exposed to the leaf petioles of pumpkin plants showed the sign of trace of NPs into the cells located away from the introduced area. Similarly, Gardea-Torresdey et al. [44] reported that the gold and silver ions present in a different valence state in growth media supplemented with agar, reduced and accumulated as Au and Ag NPs inside alfalfa seedlings. Similarly, transformation and accumulation of silver and platinum ions into Ag and Pt NPs in alfalfa and mustard seedlings were also investigated on various plants [45,46] and strongly concluded that the gold, silver and platinum nanoparticles could be accumulated into the seedlings of various tested experimental plants.

Effect of nanoparticles on the cellular and genetic toxicity in plants

Tan et al. [47] studied the toxicity of multi-walled carbon nanotube suspension of rice cells and reported that multi-walled carbon nanotubes at low concentrations cause cell death and at high concentration cause cell mortality. However, Shen et al. [48] reported the concentration and size of single-wall carbon nanotubes cause the toxicity in the rice and Arabidopsis protoplast cells and the breakdown of genetic material in Arabidopsis cell directly correlated with the genetic toxicity of the single walled carbon nanotubes.

Lopez-Moreno et al. [32] investigated the cellular toxicity of CeO₂ and ZnO NPs on soybean seedlings and detected the genetic toxicity of both NPs by RAPD assay. They elaborated that the interaction of genetic material with the zinc ions is the main reason behind the increase in the toxicity level. However, in another study, Ghosh et al. [49] found that TiO₂ NPs were genotoxic and cytotoxic due to the generation of superoxide radicals during lipid peroxidation. However, Babu et al. [50] observed the dose dependent and duration dependent responses in the root meristem of Allium cepa due to decrease in mitotic indices arisen by various types of chromosomal abnormalities against Ag NPs. Kumari et al. [51] found that treatment of A. cepa cells with various concentrations of Ag NPs caused the stickiness and breakage of chromosomes, which may finally lead to the genotoxicity of cells. Similarly, Racuciu and Creanga [52] reported the biocompatible magnetic nanoparticles coated with perchloric acid decreased the level of nucleic acid and postulated that the magnetic nanoparticles induced the chromosomal aberrations in corn cells.

 Conclusions

Nanoparticles have been recently exploited in the agricultural system, but still they are posing some challenges for researchers due to their size, toxicity, reactivity with the environmental factors. It is obvious from various previous studies that all the nanoparticles are not toxic in nature and positively influenced the morphological or physiological traits of the plants. On the contrary, others also proved its toxic effect, but no one could explain the real cause behind the cellular and genetic toxicity in plants. Due to this reason, the application of nanoparticles as nano-biofertilizer is still lagging in agricultural sectors and still away from the development of new and innovative technology. Therefore, more extensive and elaborate studies are needed to explain the mechanism and factors behind this unexplored research area.

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