Abstract

The present investigation was to determine the effect of nano-TiO2 (2 to 6 nm) and waste water on early seedling growth of maize. The suspensions of nano-TiO2 either in deionized water or autoclaved waste water were applied at 100 mg/L, 50 mg/L and 25 mg/L under in vitro conditions. Analyses of waste water showed that it was not suitable for irrigation purposes as it had a higher content of heavy metals (Fe, Mn, Zn, Cd, Cr and Cu) which were above permissible levels for irrigation. The higher concentration of nano-TiO2 (100 mg/L) and waste water significantly inhibited seed germination, seedling growth and caused accumulation of phenolics in maize plants (p < 0.05). The application of nano-TiO2 at 25 mg/L significantly increased shoot fresh weight, shoot dry weight, root fresh weight, root dry weight, root area, chlorophyll a, chlorophyll b and carotenoids content (p < 0.05). The adverse effects of waste water on growth attributes of maize were significantly ameliorated by nano-TiO2 at 25 mg/L (p < 0.05). The treatment of waste water with nano-TiO2 (25 mg/L) is recommended before its utilization for agriculture purposes.

INTRODUCTION

Titanium dioxide (TiO2) nanoparticles have diverse industrial applications compared with other nanoparticles (Jovanovic et al. 2011a). They are a component of various products, for example cosmetics, sunscreens, electronics, biomedicine and biomedical products (Handy et al. 2008a; Melquiades et al. 2008; Navarro et al. 2008; Jovanovic et al. 2011b). TiO2 nanoparticles are used as an additive in paints and building materials (Chen & Poon 2009). It is also used in plastics, ink and paper products, and as a food additive (Ortlieb 2010). It is used to decontaminate water, soil and air (Aarthi & Madras 2007).

Presence of TiO2 has been reported in different environmental matrices, namely water, soils, bacteria, algae, fungi, plankton, fish and some plant species (Handy et al. 2008a, 2008b; Navarro et al. 2008; Frazier et al. 2014). Chen et al. (2012) have reported that TiO2 nanoparticles induce oxidative stress and cause lipid peroxidation and inhibition of cell growth. According to Frazier et al. (2014), root lengths, biomass and germination rates of Nicotiana tabacum seedlings was significantly inhibited after exposure to TiO2 nanoparticles (0.1, 1, 2.5, and 5%) for 3 weeks. Higher concentration of TiO2 also decreased seed germination and seedling growth of onion and vice versa at lower concentration (Raskar & Laware 2013). Seed germination of Triticum aestivum and the radicle and plumule length of seedlings were affected significantly in the presence of TiO2 nanoparticles (Mahmoodzadeh & Aghili 2014). Chen et al. (2012) recorded that cell growth and photosynthetic efficiency of Chlamydomonas reinhardtii were inhibited by TiO2 exposure at high concentration but other cell constituents such as chlorophyll a remained constant. Several studies have revealed non-toxic effects of nano-TiO2 on plant growth at lower concentrations (Zheng et al. 2005; Seeger et al. 2009; Larue et al. 2012).

Waste water is defined as marginal quality water originating in urban and suburban areas. This water is used for irrigation purposes in those areas where water is scanty for agriculture. This marginal quality water is used for irrigation of more than 20 million hectares of land all over the world and nearly 10% of the world's population consume food crops irrigated with this marginal water (WHO 2006; Hamilton et al. 2007). Marginal water contains many domestic and industrial influents which pose serious risk to food crops if used untreated (Srinivasan & Reddy 2009). Although waste water contains organic matter and various types of nutrients beneficial for crop plants, it is also a source of different types of heavy metals, which have negative impacts on food crops (Mojid et al. 2016). Therefore, proper treatment of waste water is recommended prior to its utilization for agricultural purposes.

There are various physical, chemical and biological approaches for the treatment of waste water. Among such practices use of nanotechnology for waste water treatment has increased in recent years. Nanotechnology has potential advantages: for example, nanoparticles are economical and highly effective in removing and recovering the pollutant (Tyagi et al. 2012). Despite the use of nanotechnology in various fields, the environmental and ethical concerns associated with the application of nanoparticles need to be addressed (Zhuang & Gentry 2011).

Advanced oxidation process with UV irradiation and photocatalyst TiO2 are gaining growing acceptance as an effective waste water treatment method (Barakat 2014). The aim of the present investigation was to determine the effects of waste water treated with nano-TiO2 on seedling growth of maize.

MATERIALS AND METHODS

Municipal waste water was obtained from Bannu city KP Pakistan and analyzed for heavy metals (Ni, Cr, Cu, Cd, Mn, Fe and Zn) using atomic absorption spectrophotometer (Varian FAAS-240) as described by Lajunen (1992). Digestion of waste water was carried in HNO3 (Gregg 1989).

The TiO2 nanoparticles were obtained from the Nano Sciences and Catalysis Division, National Centre for Physics, Quaid-i-Azam University, Islamabad, Pakistan. The diameter range of the nanoparticles was 2–6 nm with mean value of 4 nm.

The TiO2 nanoparticles were dispersed in autoclaved deionized water or autoclaved waste water under ultra-sonication. The solutions of nanoparticles were placed in sunlight for a whole day (8 h) in glass flasks. Seeds of Zea mays (maize) were obtained from the National Agriculture Research Centre, Islamabad, surface sterilized with 10% chlorox solution and washed three times with autoclaved distilled water. Seeds were transferred onto the filter papers in petri dishes. The filter papers were moistened with 5 ml suspension of nano-TiO2 in autoclaved deionized water or autoclaved waste water and incubated at 25–27 °C in the dark for 5 days. After seed germination the growth chamber was set at day/night photoperiod (16/8 h), day/night temperature (24/20 2 ± 2), and day/night relative humidity (75/80%).

The treatments were: untreated control; 100 mg/L nano-TiO2 suspension in autoclaved deionized water; 50 mg/L nano-TiO2 suspension in autoclaved deionized water; 25 mg/L nano-TiO2 suspension in autoclaved deionized water; only waste water; 100 mg/L nano-TiO2 suspension in autoclaved waste water; 50 mg/L nano-TiO2 suspension in autoclaved waste water; and 25 mg/L nano-TiO2 suspension in autoclaved waste water.

The seed germination (%) was calculated as:  
formula
(1)
The plants were harvested 14 days after initiation of the experiment and analyzed for morphological and physiological growth attributes. The shoot and root weight was determined by using an electronic balance. Root length and root area were determined using the Root Law Software Program (Washington State Research Foundation, USA).

Estimation of photosynthetic pigments was carried out by the method as given by Arnon (1949).

The method of Wolfe et al. (2003) was used for the extraction and quantification of total soluble phenolics content in leaves of maize. The frozen leaf tissue (0.5 g) was extracted in methanol (10 ml). A total of 0.5 ml filtrate of this phenolics extract was added to 1.5 ml freshly prepared Folin-Ciocalteu reagent. The mixture was kept in the dark for 5 minutes and 1.5 ml sodium carbonate solution (7%) was added. The optical density (OD) of the reaction mixture was noted at 760 nm after incubation of samples for 90 minutes at room temperature. The OD readings were compared with a standard curve for gallic acid. The total soluble phenolics content was expressed as μg gallic acid eq./gram leaf tissue.

The data were analyzed statistically by analysis of variance and mean values were compared by Duncan's multiple range test (Duncan 1955).

RESULTS

The results of heavy metal composition of waste water are summarized in Table 1. The concentration of heavy metals such as Fe, Mn, Zn, Cr, Cd and Cu were higher than permissible limits as set by FAO (1985) for irrigation purposes.

Table 1

Heavy metal composition of municipal waste water

Heavy metals Concentration (mg/L) FAO (1985) (mg/L) National Environment Quality Standards (NEQS) (mg/L) 
Fe 10.07 
Mn 1.27 0.2 1.5 
Zn 3.78 Nil 
Ni 2.78 
Cd 0.52 0.01 0.1 
Cr 1.06 0.1 
Cu 0.9 0.1 
Heavy metals Concentration (mg/L) FAO (1985) (mg/L) National Environment Quality Standards (NEQS) (mg/L) 
Fe 10.07 
Mn 1.27 0.2 1.5 
Zn 3.78 Nil 
Ni 2.78 
Cd 0.52 0.01 0.1 
Cr 1.06 0.1 
Cu 0.9 0.1 

Results presented in Figure 1 show that application of nano-TiO2 at 100 mg/L and 50 mg/L significantly reduced seed germination (%) as compared to untreated control (p < 0.05). The inhibitory effect of nano-TiO2 at 100 mg/L on seed germination was more pronounced than at 50 mg/L. The application of nano-TiO2 at 25 mg/L did not affect seed germination and caused 100% seed germination. The waste water showed significant reduction in seed germination % as compared to untreated control (p < 0.05). The treatments with nano-TiO2 at 100 mg/L, 50 mg/L and waste water also showed significantly lower seed germination than the untreated control. The application of nano-TiO2 at 25 mg/L significantly ameliorated the adverse effect of waste water on seed germination and resulted in 100% seed germination.

Figure 1

Effect of nano-TiO2 and waste water on seed germination (%). Least significant difference (LSD): 3.997. Mean values sharing common letters are statistically similar.

Figure 1

Effect of nano-TiO2 and waste water on seed germination (%). Least significant difference (LSD): 3.997. Mean values sharing common letters are statistically similar.

Results presented in Figure 2(a) and 2(b) show that application of nano-TiO2 at 100 mg/L significantly reduced shoot fresh weight and shoot dry weight compared with the untreated control (p < 0.05). The effect of lower concentration of nano-TiO2 (25 mg/L) significantly increased (37%) shoot dry weight compared with the untreated control. The application of nano-TiO2 at 100 mg/L under the waste water treatment significantly decreased shoot dry weight compared with the control. The application of nano-TiO2 at 50 mg/L and 25 mg/L significantly increased the shoot dry weight under waste water treatment. The beneficial effect of nano-TiO2 on shoot dry weight under waste water treatment was significantly more pronounced (58%) at 25 mg/L than at 50 mg/L (p < 0.05).

Figure 2

Effect of nano-TiO2 and waste water on (a) shoot fresh weight LSD: 0.131, (b) shoot dry weight LSD: 0.010, (c) root fresh weight LSD: 0.169, and (d) root dry weight LSD: 0.025. Mean values sharing common letters are statistically similar.

Figure 2

Effect of nano-TiO2 and waste water on (a) shoot fresh weight LSD: 0.131, (b) shoot dry weight LSD: 0.010, (c) root fresh weight LSD: 0.169, and (d) root dry weight LSD: 0.025. Mean values sharing common letters are statistically similar.

Results presented in Figure 2(c) and 2(d) show that application of nano-TiO2 at 25 mg/L both under normal water or waste water treatment significantly increased root fresh weight and root dry weight compared with the untreated control (p < 0.05). The nano-TiO2 at 100 mg/L and 50 mg/L had no effect on root weight. The waste water had no significant effect on root fresh weight and root dry weight.

The application of nano-TiO2 at all the three concentrations (100 mg/L, 50 mg/L and 25 mg/L) did not significantly affect root length compared with the control. The irrigation with waste water had no significant effect on root length. Moreover, application of nano-TiO2 at 100 mg/L and 50 mg/L under waste water treatment did not significantly affect root length compared with the control. The application of nano-TiO2 at 25 mg/L under waste water treatment significantly improved (57%) root length compared with the untreated control (Figure 3(a)).

Figure 3

Effect of nano-TiO2 and waste water on (a) root length LSD: 54.578 and (b) root area LSD: 2.832. Mean values sharing common letters are statistically similar.

Figure 3

Effect of nano-TiO2 and waste water on (a) root length LSD: 54.578 and (b) root area LSD: 2.832. Mean values sharing common letters are statistically similar.

Results showed that application of nano-TiO2 at 25 mg/L under normal water treatment significantly increased (55%) root area compared with the control (Figure 3(b)). The application of waste water significantly decreased (54%) root area compared with the untreated control (p < 0.05). The reduction in root area by waste water was significantly ameliorated by application of nano-TiO2 at 25 mg/L.

Higher concentration of nano-TiO2 (100 mg/L) exhibited significant reduction in chlorophyll a and chlorophyll b contents of maize leaves compared with the untreated control (p < 0.05). The application of nano-TiO2 at 25 mg/L showed a significant increase in chlorophyll a and chlorophyll b content over the control (Figure 4(a) and 4(b)). The treatment with waste water showed significant reduction in chlorophyll a and chlorophyll b compared with the control. The application of nano-TiO2 at 25 mg/L significantly ameliorated the adverse effects of waste water treatment on photosynthetic pigments.

Figure 4

Effect of nano-TiO2 and waste water on (a) chlorophyll a LSD: 4.197, (b) chlorophyll b LSD: 2.006, (c) carotenoids LSD: 5.063, and (d) total soluble phenolics content LSD: 12.987. Mean values sharing common letters are statistically similar.

Figure 4

Effect of nano-TiO2 and waste water on (a) chlorophyll a LSD: 4.197, (b) chlorophyll b LSD: 2.006, (c) carotenoids LSD: 5.063, and (d) total soluble phenolics content LSD: 12.987. Mean values sharing common letters are statistically similar.

The application of nano-TiO2 at 25 mg/L stimulated the carotenoids content of maize leaves over control (Figure 4(c)). Waste water treatment did not affect carotenoids content. The effect of nano-TiO2 under waste water treatment was also non-significant.

The application of nano-TiO2 at 100 mg/L and 50 mg/L significantly increased total soluble phenolics content in maize leaves compared with the untreated control (p < 0.05). The nano-TiO2 at 25 mg/L did not significantly affect total soluble phenolics content. The effect of nano-TiO2 at 100 mg/L and 50 mg/L on leaf total soluble phenolics content was also stimulatory under waste water treatment. However, the application of nano-TiO2 at 25 mg/L under waste water treatment did not significantly affect total soluble phenolics content compared with the untreated control (Figure 4(d)).

DISCUSSION

It was observed that higher concentration (100 mg/L) of nano-TiO2 inhibited seed germination and seedling growth of maize. In contrast the lower concentration of nano-TiO2 (25 mg/L) stimulated growth attributes of maize. The effect of waste water on seedling growth was inhibitory. It was found that nano-TiO2 ameliorated the adverse effects of waste water on seed germination and early seedling growth of maize.

Various nanoparticles such as TiO2 and fullerene have been investigated for their nano-toxicity. However, information recorded so far has been inconclusive in terms of attributing phytotoxicity to the nanoparticles (Lin & Xing 2007). Ghosh et al. (2010) have reported adverse effects of TiO2 nanoparticles on growth of Nicotiana tabacum. They observed induction of DNA injuries at high concentration of TiO2 nanoparticles. Application of TiO2 on Allium cepa revealed an increased malondialdehyde (MDA) level which is a common biomarker portraying membrane lipid peroxidation (Goel & Sheoran 2003; Ghosh et al. 2010). Such higher MDA production is a signal of stress and inhibits the physiological pathways involved in seed germination (Jiang et al. 2013).

The capability of a material to generate an electron lone pair upon exposure to UV radiation is called its photocatalytic activity (PCA). The subsequent free radicals are powerful oxidizers of hydrocarbons. The PCA in TiO2 has been implicated in sanitation, sterilization and remediation. Exposure of TiO2 to ultraviolet radiation leads to the creation of powerful oxidizing agents which can decompose a variety of bacteria, organic and inorganic materials (Zakaria et al. 2014). The beneficial effects of nano-TiO2 on growth attributes of maize under waste water might be due to the fact that these nanoparticles are powerful oxidizing agents and have neutralized the toxic effects of various types of heavy metals present in the waste water. The higher concentrations of nano-TiO2 exhibited toxic effects whereas the lower concentration was beneficial. Higher concentration of TiO2 decreased seed germination and seedling growth of onion and vice versa at lower concentration (Raskar & Laware 2013).

During the present investigation the higher concentration of nano-TiO2 inhibited photosynthetic pigments. Chen et al. (2012) recorded that cell growth and photosynthetic efficiency of Chlamydomonas reinhardtii was inhibited by TiO2 exposure at high concentration but other cell constituents such as chlorophyll a remained constant. Toxicity of nano-particles generally occurs because of either chemical composition (e.g. release of (toxic) ions) or stimuli caused by the surface, size and/or shape of the particle in action (Brunner et al. 2006). The effect of waste water on photosynthetic pigments was inhibitory. This might be because waste water contains large amounts of toxic chemicals such as heavy metals as were found during the study. These heavy metals adversely affect physiological processes of plants (Khan et al. 2015). The beneficial effects of a lower concentration of nano-TiO2 under waste water treatment on chlorophyll a and chlorophyll b might be due to self-cleaning properties of TiO2 (Zakaria et al. 2014).

The application of a higher concentration of nano-TiO2 and waste water caused accumulation of soluble phenolics in leaves of maize. The accumulation of soluble phenolics under metal stress is a common phenomenon and indicates stress tolerance of plants to a particular metal stress (Diaz et al. 2001). Phenolic compounds function as antioxidants due to their capacity to scavenge free radicals (Fauconneau et al. 1997). TiO2 produces lipid peroxidation products and reactive species that induce injury of epithelial cells and DNA damage in the cell lines (Falck et al. 2009; Trouiller et al. 2009). Chen et al. (2012) have reported that TiO2 nanoparticles induce oxidative stress and cause lipid peroxidation and inhibition of cell growth. The phenolic compounds make chelates with heavy metals and thus their antioxidant activities are increased (Jung et al. 2003). When exposed to heavy metals, plants accumulate phenolic compounds (Winkel-Shirley 2002). The accumulation of phenolics in plants is usually related to the production of lower plant biomass (Latif et al. 2016).

CONCLUSION

The waste water treatment with nano-TiO2 at 25 mg/L exhibited beneficial effects on growth attributes of maize. In contrast, the higher concentration of nano-TiO2 was phytotoxic. This indicated that nano-TiO2 (25 mg/L) has no toxic effects on growth of maize and can be recommended for future application to maize under waste water irrigation.

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