Interactions between engineered nanomaterials and agricultural crops: implications for food safety

552 Deng et al. / J Zhejiang Univ-Sci A (Appl Phys & Eng) 2014 15(8):552-572 Journal of Zhejiang University-SCIENCE A (Applied Physics & Engineering) ISSN 1673-565X (Print); ISSN 1862-1775 (Online) www.zju.edu.cn/jzus; www.springerlink.com E-mail: Review: Interactions between engineered nanomaterials and agricultural crops: implications for food safety* Ying-qing DENG1, Jason C. WHITE2, Bao-shan XING†‡1 (1Stockbridge School of Agriculture, University of Massachusetts, Amherst, MA 01003, USA) 2 ( Department of Analytical Chemistry, The Connecticut Agricultural Experiment Station, New Haven, CT 06504, USA) † E-mail: Received June 8, 2014; Revision accepted June 24, 2014; Crosschecked July 18, 2014 Abstract: Engineered nanomaterials (ENMs) are being discharged into the environment and to agricultural fields, with unknown impacts on crop species. In this paper, we review the literature on ENMs uptake, translocation/distribution, and generational transmission in various crop species, as well as potential material trophic transfer. Previous studies reveal that ENM-exposed crops exhibit adaptive processes in response to stress, including endocytosis/endosome activities, production of antioxidant enzymes, regulation of genes related to cell division/extension and membrane transport. Some agronomic traits of crops are compromised during the adaption response, including photosynthesis, fruit yields, nutritional quality and nitrogen fixation. Cultivation of crops in ENMs-contaminated environments has unknown implications for food safety and quality. Notably, mechanisms underlying ENMs phytotoxicity and bioavailability are unclear. Additional investigations focused on developing novel techniques for in vivo identification/characterization of ENMs are critically needed. Given the abundance of uncertainty in the literature, it is clear that more research is urgently needed in the area of ENMs-crop interactions; only then can one accurately assess exposure, risk, and overall implications for food safety and also enable guidance development for the sustainable implementation of nanotechnology in agriculture and food production/manufacturing. Key words: Engineered nanomaterials (ENMs), Uptake, Trophic transfer, Food safety, Toxicity and impact doi:10.1631/jzus.A1400165 Document code: A CLC number: X503 1 Introduction Nanotechnology has revolutionized many facets of modern society through extensive application in the fields of material science, energy, environmental remediation, agriculture, and medicine. As this technology continues to expand, nano-scale materials will inevitably being discharged into the environment and have become emerging contaminants of concern. Importantly, the implications of nanotechnology for the environment and agriculture ‡ Corresponding author Project supported by the US Department of Agriculture-Agriculture and Food Research Initiative (USDA-AFRI) (No. 2011-67006-30181) and the USDA-AFRI Hatch Program (No. MAS 00978) © Zhejiang University and Springer-Verlag Berlin Heidelberg 2014 * remain unclear; without this fundamental knowledge, development of regulations and guidelines for safe use of engineered nanomaterials (ENMs) will not be possible. The dramatic increase in worldwide production and application of ENMs is due to novel and useful material properties that become evident at the nanoscale. On the scale of nanometers, the relatively large surface area of ENMs results in enhanced chemical/biological activity. In addition, quantum effects become significant with size reduction, subsequently changing particle optical, electrical, and magnetic behaviors. However, great variation exists among different ENMs, including size, shape, physical conformation, specific surface area, surface charge, and the presence of coatings/functionality (Hassellov et al., 2008; Parsons et al., 2010; Pan and Deng et al. / J Zhejiang Univ-Sci A (Appl Phys & Eng) 2014 15(8):552-572 Xing, 2012). From the perspective of nanobiological interactions, the most attractive ENMs traits include a high degree of surface reactivity and a size-dependent ability to cross biological membranes. Because ENMs will be on the same scale as the key components of cells, including proteins, nucleic acids, lipids, and cellular organelles, significant particle-cellular interactions (both positive and negative) can be anticipated (Fadeel et al., 2007; Auffan et al., 2009). The widespread presence of ENMs in the environment will bring significant and unique challenges to food safety and security. The global production and application of ENMs make particle accumulation in soil and groundwater inevitable. Plant species exposed to ENMs over time may undergo morphological, physiological, genetic, and epigenetic changes that may subsequently affect crop growth, yield, or nutritional status. Furthermore, after ENM transfer from soil to the edible/ reproductive organs of crops, particles may accumulate in the food chain with unknown consequences to humans and other sensitive receptors. As such, consumption of food products from contaminated soil presents an unknown risk to public and environmental health. There are many studies reporting the results of ENM toxicity tests conducted on model organisms and aquatic species such as Arabidopsis thaliana (Liu et al., 2010; Wang H. et al., 2011) and algae (He et al., 2012). These studies and others provide evidence of both beneficial and detrimental effects on plants upon ENMs exposure. However, the literature is far too anemic to shed light on the responses of edible terrestrial plants with regard to food safety and overall nanotechnology sustainability. In this review we summarize and interpret the literature on ENM-crop interactions so as to further efforts to achieve a comprehensive understanding of (1) the exposure conditions and scenarios of agricultural crops to ENMs in the environment; (2) the uptake pattern of ENMs internalization and translocation in vivo; (3) potential trophic transfer; and (4) the impact of ENMs on agricultural crops at morphological, physiological, and genetic/epigenetic levels. Based on this review, we will identify critical knowledge gaps and highlight future research priorities. 553 2 Exposure scenarios 2.1 ENMs in real environments Although ENMs are ubiquitous in the environment, actual data measuring ENMs concentrations in various media is scarce (Klaine et al., 2008). Much of this is due to limited techniques for separation/ extraction, characterization, and quantitation of ENMs environmental samples. One group has predicted environmental ENMs concentrations through probabilistic material flow analysis (Mueller and Nowack, 2008; Gottschalk et al., 2009; 2013). As described in their work, the annual increase of ENMs in sludge amended EU or US soil was predicted to range from 1 ng/kg for fullerenes to 89 µg/kg for nano-TiO2 (Gottschalk et al., 2009). However, the predicted data are highly variable due to the poorly d (...truncated)