Nanotechnology in agriculture: Next steps for understanding engineered nanoparticle exposure and risk

Highlights

• Current plant-nanoparticle interactions literature is dominated by high dose, short-term exposures conducted in model media

• Although somewhat contradictory, this literature generally suggests low overall phytotoxicity from nanoparticle exposure

• An ecologically relevant systems approach is needed that includes environmentally realistic studies with sensitive endpoints

Abstract

The potential uses and benefits of nanotechnology in agriculture are significant, including producing greater quantities of food with lower cost, energy, and waste. However, many questions regarding the risk of these approaches in food production remain unanswered. A robust literature assessing the toxicity of engineered nanomaterials to terrestrial\agricultural plant species has begun to develop. However, much of this literature has focused on short term, high dose exposure scenarios often conducted in model media. Although important to determining inherent nanomaterial hazard, these studies are inadequate for assessing the actual risk posed to agricultural systems, including for sensitive receptors such as humans. Although the existing literature is somewhat contradictory, it is notable that the overall findings seem to suggest low to moderate toxicity to terrestrial plant species. However, what is now needed is a systems-level approach investigating more subtle yet potentially more significant impacts of nanomaterial exposure in agricultural systems, including the use of a range of more sensitive endpoints that can mechanistically characterize toxicity. This article will identify these and other key knowledge gaps and also highlight critical next steps for understanding the balance between nanotechnology applications and implications in agriculture and food production.

Introduction

The use of nanotechnology in agriculture has created a great interest, offering the potential for significantly enhanced agricultural productivity and efficiency with lower cost and less waste (Scott and Chen, 2013, Kah, 2015). Importantly, the emergence of these applications in agriculture and other sectors has also raised safety concerns over environmental and human health; the resulting field of nanotoxicology has developed in an effort to answer critical questions of hazard, exposure and ultimate risk.

Since 2000, over 10,000 articles have been published that investigate the environmental health and safety of engineered nanoparticles (ENP) (nanoEHS), with more than 50% of those studies occurring in the last three years (Krug, 2014). Early (2006–2010) efforts at the Organization for Economic Cooperation and Development (OECD) focused on a priority list of ENP, which included fullerenes (C₆₀), SWCNTs, MWCNTs, silver, iron, titanium dioxide, aluminum oxide, cerium oxide, zinc oxide, silicon dioxide, dendrimers, nanoclays and gold nanoparticles. The desire was to evaluate the intrinsic characteristics of each material, with OECD testing strategies and evaluation based on “physical–chemical properties, environmental degradation and accumulation, environmental toxicology and mammalian toxicology.” It is worth noting that only a limited number of these studies were focused on terrestrial plant species. For example, of the 10,000 papers published since 2000 on nanoEHS, less than a third addressed plant species. However, more recently a number of reviews on plant-NM interactions have been published (Rico et al., 2011, Miralles et al., 2012, Gardea-Torresdey et al., 2014, Yin et al., 2012, Ma et al., 2015). What is clear is that the majority of plant-ENP investigations have focused on high dose, short exposure scenarios, often have conducted in simplified or model media. Although these types of investigations are a necessary first step when beginning to evaluate the hazard of a potential class of emerging contaminants, the resulting data set is insufficient for addressing more complex issues of exposure and actual risk.

In reviewing the growing number of studies in this area, it is clear that there are many contradictory findings but notably, the majority of the work suggests low-to-moderate overall phytotoxicity in terrestrial plant species. There are obvious exceptions to this trend but again, many of these findings of negative effects are at high (and likely unrealistic) doses. Also, notably lacking in many of these studies is soil as the exposure media; given what is known about the behavior of other contaminants in complex natural matrices such as soil, one may predict significantly lower toxicity than observed in model media (Schwab et al., 2015). Given this lack of clear overt phytotoxicity, the research community should now refocus efforts on more subtle systems-level processes that can be investigated under conditions of environmental relevance. For example, negative effects on processes such as nutrient cycling/acquisition or plant-microbe interactions (nitrogen fixation, mycorrhizal symbioses) may in fact pose greater risk to agroecosystem function and integrity. A semi-comprehensive list of topics and scenarios in need of investigation is below. This should not be interpreted as a list of items to be treated separately but instead as the integrated basis for a systems-level approach to accurately and quantitatively understand ENP fate and effects in agricultural systems (Fig. 1).