Arbuscular mycorrhizae alleviate negative effects of zinc oxide nanoparticle and zinc accumulation in maize plants – A soil microcosm experiment
Introduction
Rapid development in nanotechnology has led to a wide range of applications of engineered nanoparticles (NPs), small compounds between 1 and 100 nm in size (Roco, 2011). These compounds enter natural ecosystems through direct application, accidental release, contaminated soil/sediments, or atmospheric fallouts (Rico et al., 2011). As such, their environmental behavior and fate, toxicity, and potential risk to ecosystems has attracted recent attention (Klaine et al., 2008, Navarro et al., 2008, Rico et al., 2011). NPs may accumulate and/or increase concentrations of the component metal in edible parts of plants, have adverse effects on agronomic traits, yield, and productivity of crops, induce variations in the nutritional value, and transfer within trophic levels (Rico et al., 2011, Gardea-Torresdey et al., 2014).
Zinc oxide (ZnO) NPs are widely used in applications including cosmetics, personal care products, paints, electronic devices, catalysts, and anti-microbial agents (Ma et al., 2013). In appropriate amounts, Zn derivates are an essential element for the human body, and some forms such as zinc acetate, chloride, citrate, gluconate, lactate, oxide, carbonate and sulphate are considered Generally Recognized as Safe (GRAS) and authorized for the fortification of foods (FDA, 2011, ODS, 2011). Therefore, several studies have examined the utilization of Zn in food fortification (Akhtar et al., 2008, Tripathi and Platel, 2010, Bautista-Gallego et al., 2013). However, when present in excess, ZnO NPs can cause toxicity in plants (Lin and Xing, 2007, Lin and Xing, 2008, López-Moreno et al., 2010, Kumari et al., 2011) and soil microorganims (Dinesh et al., 2012), reduce soil quality (Du et al., 2011, Priester et al., 2012), and reduce plant biomass and yields (De La Rosa et al., 2011, Yoon et al., 2014). ZnO NPs can also cause Zn accumulation in plants, especially in edible parts of food crops (Kim et al., 2011, Priester et al., 2012), and then subsequently enter human bodies and pose a significant health risk.
Arbuscular mycorrhizal (AM) fungi (AMF) are a group of ubiquitous soil fungi in terrestrial ecosystems that form symbiotic associations with more than 90% of surveyed higher plants (Smith and Read, 2008). In addition to their well-known contribution to plant nutrient acquisition and growth, AMF can mediate the effects of heavy metals on their host plants, allowing some plants to grow in soils with excess toxic metals (González-Guerrero et al., 2009, Meier et al., 2012). In copper-contaminated soil, AMF can assist plants in transforming copper into metallic NPs found in and near roots (Manceau et al., 2008). Feng et al. (2013) were the first to show that some metal oxide nanoparticles, iron oxide FeO NPs and silver Ag NPs, differently influenced AMF and the consequent effects of AMF on plant growth, indicating a potential interaction between AMF and metal or metal oxide NPs. ZnO NPs-induced toxicity is partly related to Zn solubility (Franklin et al., 2007, Rousk et al., 2012), but AMF can exert protective effects on plants against excessive Zn accumulation under high soil Zn conditions (Cavagnaro et al., 2010, Watts-Williams et al., 2013). Thus, AMF may play a potential role in alleviating ZnO NPs-induced toxicity to plants growing in ZnO NPs-polluted soil. However, to our knowledge, no study has yet been conducted to investigate this potential role of AMF.
Maize is one of the most common food crops grown in the world, and can be easily colonized by AMF (Wang et al., 2006). Here, using maize as a plant model, we conducted a soil microcosm experiment to identify (1) whether ZnO NPs produce adverse effects on maize growth, nutrient acquisition, and physiological responses, particularly when the ZnO NPs reach typical pollution levels; (2) whether AM inoculation can alleviate ZnO NPs-induced toxicity, and (3) the possible detoxification mechanisms employed by AMF.
Section snippets
Soil and AM fungal inocula
We collected soil from an experimental field (0–15 cm depth) at the Henan University of Science and Technology. After being sifted through a 2 mm sieve, the soil was autoclaved at 121 °C for 2 h, and air-dried. The soil is classified as Aquic Ustochrepts (US soil taxonomy) and soil texture is loamy, with a pH (1:2.5 soil/water) of 8.2, 2.08% organic matter, 1.03 g/kg total N, 1.82 g/kg total P, 19.2 g/kg total K, 65.2 mg/kg alkali-hydrolyzable N, 9.02 mg/kg Olsen P, 278.64 mg/kg 1 M NH4OAc
Root colonization rate
As expected, maize plants in the NM controls were not colonized. In all AM plants, root colonization rates were above 40% at all ZnO NPs doses, but sometimes lower in Gv-plants than in Gc-plants (Fig. 1). As ZnO NPs dose increased, root colonization rates in both Gv and Gc treatments showed a decreasing trend, and significantly decreased at concentrations of 800 mg/kg and above, but did not change significantly between the zero dose and the 400 mg/kg dose. The two-way ANOVA results show that AM
Discussion
The results of phytotoxicity by ZnO NPs have been widely studied, and in high concentrations they may cause inhibition of seed germination and root growth (Lin and Xing, 2007, De La Rosa et al., 2011), cytogenetic toxicity and genotoxicity (Kumari et al., 2011), and reduction of plant biomass and yields (Lin and Xing, 2008, Du et al., 2011, Yoon et al., 2014). However, most studies examining plant–NPs interactions use hydroponic systems, or only examine NPs' effects on plant germination.
Conclusions
Our soil microcosm experiment illustrated that high concentrations of Zn exceeding a toxic threshold accumulated in both shoots and roots of ZnO NPs-treated maize plants, and thus could pose environmental risks. For the first time, we demonstrate the toxicity of ZnO NPs to AM symbiosis, and show that AMF help to alleviate ZnO NPs-induced phytotoxicity in plants by decreasing ZnO NPs bioavailability and Zn accumulation, decreasing Zn partitioning to shoots, decreasing ROS production, and by
Acknowledgments
This work was sponsored by the National Natural Science Foundation of China (41471395, 41171369), the Innovation Team Foundation of Henan University of Science and Technology (2015TTD002), Program for Science & Technology Innovation Talents in Universities of Henan Province (2012HASTIT014), and the Foundation for University Key Youth Teachers of Henan Province (2012GGJS-079).
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Fayuan Wang and Xueqin Liu are the co-first authors.