Arbuscular mycorrhizae alleviate negative effects of zinc oxide nanoparticle and zinc accumulation in maize plants – A soil microcosm experiment

Highlights

• Interactions between ZnO NPs and arbuscular mycorrhizal symbiosis are first studied.

• High doses of ZnO NPs show toxicity to arbuscular mycorrhizal symbiosis.

• Arbuscular mycorrhizal fungi alleviate ZnO NPs-induced phytotoxicity in maize.

• AM symbiosis reduces the accumulation of ZnO NPs-derived Zn in maize plants.

• AM symbiosis reduces potential risk of ZnO NPs to agricultural ecosystems.

Abstract

ZnO nanoparticles (NPs) are considered an emerging contaminant when in high concentration, and their effects on crops and soil microorganisms pose new concerns and challenges. Arbuscular mycorrhizal (AM) fungi (AMF) form mutualistic symbioses with most vascular plants, and putatively contribute to reducing nanotoxicity in plants. Here, we studied the interactions between ZnO NPs and maize plants inoculated with or without AMF in ZnO NPs-spiked soil. ZnO NPs had no significant adverse effects at 400 mg/kg, but inhibited both maize growth and AM colonization at concentrations at and above 800 mg/kg. Sufficient addition of ZnO NPs decreased plant mineral nutrient acquisition, photosynthetic pigment concentrations, and root activity. Furthermore, ZnO NPs caused Zn concentrations in plants to increase in a dose-dependent pattern. As the ZnO NPs dose increased, we also found a positive correlation with soil diethylenetriaminepentaacetic acid (DTPA)-extractable Zn. However, AM inoculation significantly alleviated the negative effects induced by ZnO NPs: inoculated-plants experienced increased growth, nutrient uptake, photosynthetic pigment content, and SOD activity in leaves. Mycorrhizal plants also exhibited decreased ROS accumulation, Zn concentrations and bioconcentration factor (BCF), and lower soil DTPA-extractable Zn concentrations at high ZnO NPs doses. Our results demonstrate that, at high contamination levels, ZnO NPs cause toxicity to AM symbiosis, but AMF help alleviate ZnO NPs-induced phytotoxicity by decreasing Zn bioavailability and accumulation, Zn partitioning to shoots, and ROS production, and by increasing mineral nutrients and antioxidant capacity. AMF may play beneficial roles in alleviating the negative effects and environmental risks posed by ZnO NPs in agroecosystems.

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.