Physiological Effects of Copper Oxide Nanoparticles and Arsenic on

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Physiological Effects of Copper Oxide Nanoparticles and Arsenic on the Growth and Life Cycle of Rice (O.sativa japonica 'Koshihikari') Jing Liu, Madie Simms, Shuai Song, Ryan S. King, and George P. Cobb Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.8b03731 • Publication Date (Web): 07 Nov 2018 Downloaded from http://pubs.acs.org on November 9, 2018

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Physiological Effects of Copper Oxide Nanoparticles and Arsenic on the Growth and

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Life Cycle of Rice (O.sativa japonica ’Koshihikari’)

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Jing Liu a*, Madie Simms a, Shuai Song b, Ryan S King a, George P Cobb a

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a

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One Bear Place #97266, Waco, Texas, USA, 76798-7266

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b

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Yingze West Street # 79, Taiyuan, Shanxi, China 030024

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Emails:

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*Jing

Department of Environmental Science, Baylor University

Department of Civil Engineering, Taiyuan University of Technology

Liu (Corresponding author): [email protected]

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Madie Simms: [email protected]

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Shuai Song: [email protected]

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Ryan S King: [email protected]

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George P Cobb: [email protected]

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ABSTRACT

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A factorial study was conducted to evaluate the phytotoxicity of copper oxide nanoparticles

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(nCuO, 0.1–100 mg/L), arsenic (As, 0 and 10 mg/kg) and their interaction to rice plants (O.sativa

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japonica ’Koshihikari’) during the life cycle. No significant effect was observed on seed

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germination. Main effects of nCuO and As were observed on lengths and biomasses of seedling

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shoots and roots, and on root branching. The interaction between nCuO and As also significantly

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influenced these parameters. nCuO addition increased Cu uptake in seedlings and generally

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improved seedling growth. With As addition, As was highly concentrated in roots and increased

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in shoots, and seedling growth was also inhibited. Additionally, nCuO and As had significant

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main and interaction effects on mature plant dry biomass, panicle number, total grain weight,

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average grain weight, and several other panicle parameters. Moreover, nCuO and As interacted

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to affect panicle emergence. nCuO also decreased As accumulation in dehusked-grains. The

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accelerated heading stage by nCuO may help shorten the life cycle of rice plants, thereby

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reducing As accumulation in grains. This study is the first to examine the influence of nCuO in

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combination with As on the life cycle of rice plants.

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Keywords: physiological effects, copper oxide nanoparticles, arsenic, rice, life cycle

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INTRODUCTION

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High geogenic content of arsenic (As) or anthropogenic activities (e.g., mining, smelting,

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agrochemical application) elevate As concentrations in biota and abiotic media, which poses

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direct or indirect ecological and human health risks. Arsenic causes phytotoxicity in various

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plants, including rice (Oryza sativa) 1-5. Soil/water-plant systems also limit the transfer of

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excessive metals to the food chain. Even so, food from terrestrial and aquatic plants can be a

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primary source of metals for humans. Rice is the main food source of inorganic As for humans,



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relative to other dietary staples 6, because the unique physiology of rice plants for living in

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flooded conditions facilitates As accumulation from water 7. Rice-dominated diets present a

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chronic exposure route that may cause global health concerns, since rice nourishes about half of

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the world’s population 8. The relationship between As concentrations in human hair and those in

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rice and agricultural soils supports the soil-plant exposure pathway of humans to As and the

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inextricable linkage between ecosystems and humans 9.

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Nanotechnology serves various industrial and domestic purposes including removal of heavy

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metals (e.g., As, Cr, Cd, Pb, etc.) from water systems using nano-absorbents 10, 11. Particularly,

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nano-copper oxide (nCuO), one of the most widely used nanoparticles (NPs), has advantages

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over other nanomaterials as an As sorbent 12, which may in turn alleviate As phytotoxicity.

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Moreover, Cu-based chemicals have been used in agriculture over several centuries 13. nCuO has

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the potential to enhance the antimicrobial and fungicidal efficiencies of Cu due to the large

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surface area to volume ratio. Soils in certain areas of the world are copper deficient, which

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affects plant growth and crop food quality 14. nCuO exposure can increase Cu concentrations in

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growing plants 15, 16. Rapid nanotechnology development may pose environmental and human

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health risks while benefiting society. nCuO can enter the environment from manufacturing

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byproducts, wastewater discharge in nano-industry, and nano-product disposal after application.

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Adverse effects of nanomaterials, including nCuO, have been observed in plants including rice

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17, 18.

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plants before widespread agricultural application, and to evaluate any differentiating effects as

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compared to bulk CuO. Furthermore, the interaction of nCuO and As in the environment is

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poorly understood, as are the mechanisms of resultant uptake by rice plants. This research

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investigated the effects of nCuO and As co-exposure during the entire life cycle of rice plants.

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The hypotheses are: 1) nCuO and As have individual main effects on rice seed germination and

Understanding of potential nCuO effects on crops is needed to minimize phytotoxicity to


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developmental parameters during the life cycle, 2) nCuO and As interactions alter rice plant

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growth during the life cycle, and 3) nCuO can alleviate some adverse effects of As on rice plant

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growth and reduce As accumulation in dehusked rice grains.

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MATERIALS AND METHODS

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Life Cycle Test in the Greenhouse

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Two types of commercial soils (60% Grainger, Catalog # 2258, 40% Lowe’s, # 235384) were

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homogenized as growth media for rice (O.sativa japonica ’Koshihikari’, Kitazawa Seed

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Company, CA, USA). Arsenic (0 and 10 mg/kg) in the form of Na2HAsO4·7H2O (Sigma-

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Aldrich, lot # BCBM0939V) was added to the soil mixture and equilibrated for one week. nCuO

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(Nano-Arc®, 97.5%, 23–37 nm, APS powder, Alfa Aesar, MA, USA) was prepared at six

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concentrations (0, 0.1, 1.0, 10, 50,100 mg/L) in 20% Hoagland’s solution [Supporting

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Information (SI), Table S1]. There were 12 treatments (2×6 combinations of nCuO and As),

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including one control with neither As nor nCuO, and one treatment that received only As.

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Twenty replicate growth containers (Berry Plastics ID: T60785CP, 2.5 L) were prepared for each

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treatment. Ten seeds were wet-seeded in each container, and seedlings were thinned to 2 well-

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established ones on day 18. The study was conducted in a greenhouse for 131 d. Procedural

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details are included in SI.

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Characterization of Nanoparticles and Soils

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Hydrodynamic diameter and zeta potential of nCuO in Hoagland’s solution were determined

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with a Malvern Zetasizer Nano ZS before addition to growth containers (SI Table S2). nCuO dry

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powder was imaged with a scanning electron microscope (SEM, FEI Company). NPs in

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solutions were sampled on day 14 and characterized using a transmission electron microscope

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(TEM, JEM-1010, JEOL Inc.) with a dried aliquot on a formvar-carbon coated 200 mesh Cu4 ACS Paragon Plus Environment


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TEM grid (SI Figure S4). Soil particles were characterized with Mastersizer 2000 for size

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distribution. Standard soil properties were also characterized using standard methods (SI Table

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S3).

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Seed Germination and Seedling Growth Measurements

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Seed germination was monitored daily until seedling collection on day 18. Shoot length (SL,

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from the root-shoot junction to the tip of the longest leaf) and root length (RL, from the root-

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shoot junction to the tip of the primary root) were measured along with the number of root

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branches (NRB) (primary root and adventitious roots) and dry weights (DWs) of shoots and

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roots.

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Heading Process, Panicle and Plant Biomass Measurements

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Panicles numbers were recorded daily once the heading process began, when the tip of a panicle

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emerged from the sheath of a flag leaf. The following parameters were recorded for each

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replicate container after harvesting panicles and plants: total number of ripe panicles (TNRP),

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each panicle axis length (PAL), numbers of primary branches and secondary branches per

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panicle (PBN and SBN), spikelet numbers per panicle (SN), total dry weight of panicles (TPW,

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including the axes of panicles and branches, and all spikelets), total grain dry weight (TGW), dry

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weights (DWs) of mature plant straw and roots. Average grain dry weight (AGW) was

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determined for each treatment. Grain to straw and root to straw dry weight ratios (GSR and RSR)

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were also determined.

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Copper and Arsenic Concentrations in Growth Media, Seedlings, and Grains

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Total Cu and As concentrations in the growth media (soil and solution), 18-d seedling shoots and

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roots, and dehusked-grains were determined by ICP-MS (Agilent 7900) after digestion (adapted

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method from USEPA 3050B for solid samples, adapted method from USEPA 200.8 for solution 5 ACS Paragon Plus Environment

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samples) 19, 20. Total Cu and As concentrations were measured in the test solution and in the soil

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mixture before adding solutions and after harvesting plants (SI Table S4-6).

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Statistical Analysis

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Statistical analyses were performed with individual growth containers as the statistical unit.

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Generalized linear models (GLMs) were used to analyze the effects of nCuO and As on the

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growth parameters of rice plants and the interaction of nCuO and As on these parameters.

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Generalized linear mixed modeling (GLMM) was used to analyze the effect of nCuO and As on

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the heading process with repeated measurement throughout the experiment. Analysis of variance

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(ANOVA) was conducted to determine the main effects of nCuO and As, and their interaction

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effects. Means were considered significantly different when p < 0.05. Regression models were

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developed between parameters to analyze their relationships. All statistical analyses were

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performed in R (version 3.3.2) with details provided in SI.

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RESULTS

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The soil particle characterized by size with Mastersizer 2000 was 4.2% ± 0.2%, 56% ± 1% and

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40% ± 1.2% of clay, silt and sand, respectively. The soil texture was classified as silt loam 21.

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Organic matter content ranged from 3.5% to 3.9% in soils before growing plants, which

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explained the high exchange capacity (18.8–29.0 meq /100 g) of soil colloids (SI Table S3).

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Exchangeable cations associated with soil colloids were Ca2+, Mg2+, K+, and Na+. Their base

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saturation percentages were 70.2%–76.1%, 12.3%–15.4%, 9.0%–11.6%, 2.7%–4.1%,

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respectively. These exchangeable cations are generally available to plants by replacing hydrogen

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ions from root hairs 21. The measured high phosphorus in basic soils after rice harvest indicated a

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proper nutrient application 22.



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Seed Germination and 18-d Seedling Growth

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Mean rice seed germination success ranged from 87%–94% and was independent of nCuO or As

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addition (p > 0.31, SI Figure S5).

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Significant individual main effects of As and nCuO were observed on the SL, although no

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difference was found in nCuO treatments compared with control. The interaction between As

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and nCuO was also significant (p < 0.05) (Figure 1, SI Table S7). nCuO decreased SL at 100

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mg/L compared with 1.0 mg/L, and As alone increased SL by 12% compared with control.

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Arsenic addition to the high nCuO treatment (100 mg/L) increased the SL by 18% relative to the

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corresponding nCuO treatment alone. More prominent main effects and interaction of As and

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nCuO were observed for shoot DW compared to the SL. nCuO treatments at or above 1.0 mg/L

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increased shoot DW by 20%–30% (p < 0.05). Whereas, As addition to higher nCuO

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concentrations (50 and 100 mg/L) decreased shoot DW by 13% and 15%, respectively,

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corresponding to the same nCuO concentration alone (p < 0.05).

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Seedling RL was influenced by both As and nCuO (p < 0.05), and there was a significant

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interaction between the two substances. Specifically, nCuO alone increased RL by 34%–49%

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compared with control (in treatments at or above 1.0 mg/L), while RL was decreased by 16%–

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18% by As addition compared with the same concentration (1.0, 10 and 100 mg/L) of nCuO (p
6.2 mg/L phosphorus), which were observed in our study, may also have enhanced

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As desorption from nCuO or other sorption surfaces due to the competition for adsorption sites12.

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In addition, organic and inorganic root exudates (e.g., low molecular organic acids such as citrate

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and malate, and CO2) also changed the environment (e.g., pH, Eh, organic matter content, CEC)

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in the rhizosphere 39, 45. Thus, the interaction of As with nCuO was more complex in our study.

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The increase in shoot biomass that we observed at high nCuO concentrations (50 and 100 mg/L)

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was possibly due to the adequate uptake of Cu in the shoot (17.3 and 18.3 mg/kg), which is

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within the range of 15–26 mg/kg found by other research groups 46. For example, organic matter

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decreases the Cu bioavailability, while polyfunctional acids in plant exudates increase Cu

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bioavailability 40, 45. According to our previous 72-h aggregation and dissolution experiment 38,

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decreased seedling biomass caused by 0.1 mg/L nCuO, was probably because nCuO equilibrated

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at a smaller size after the aggregation dominated phase (48 h) and these smaller nCuO particles

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interacted with plants.

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Intrinsic Regulatory Mechanism

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Overall, roots are more sensitive than shoots to environmental stressors because roots are the

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dominant location for hormone (e.g., cytokinins) generation 47. Roots not only anchor the plant,

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assure supplies of water, minerals and nutrients, but also influence hormonal messages in shoots.

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Roots can change the output of root hormones or precursors (e.g. cytokinins or the ethylene

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precursor 1-aminocyclopropane-1-carboxylic acid) to shoots or act as sinks for shoot produced

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phloem-mobile hormones [e.g. abscisic acid (ABA)] 48. 19 ACS Paragon Plus Environment

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Effects on root growth can be explained by inter-regulated intrinsic and extrinsic response

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pathways. External stress (e.g., As) can influence hormone messages in roots and shoots by

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altering gene expressions that regulate phytohormone biosynthesis, inactivation, and signaling 49.

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In our study, RBN was increased by nCuO and decreased by As, indicating that both chemicals

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may have differentially influenced processes that regulate root cell division and branching

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process, which needs further study.

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Human Health Implication of Copper and Arsenic Accumulation in Dehusked-grains

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Dehusked rice grains, the edible part for humans, present an exposure pathway for As to

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potentially affect human health. In our study, As accumulation in dehusked-grains decreased at

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all test nCuO+As treatments compared with As alone treatment (SI, Table S12). The lowest As

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accumulation in the dehusked-grains among all As treatments was 128 ± 15.4 ng/g, which was

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observed in the As+nCuO 50 mg/L treatment and was 36% lower than the WHO maximum safe

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concentration of As in white rice (200 ng/g) for humans 50. Whereas, the confidence interval of

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As in dehusked-grains for As alone treatment included 200 ng/g (SI Table S12). A 60-kg person

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with a daily ingestion of 200 g of rice containing 200 ng/g As would experience an As exposure

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rate at 0.67 µg/kg/day. This is lower than the no-observed-adverse-effect level (NOAEL, 0.80

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µg/kg/day) for human cardiovascular effects (ischemic heart disease, mortality), hepatic effects

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(increased serum alkaline phosphatase and bilirubin), dermal effects (hyperkeratosis and

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hyperpigmentation), and intelligence performance 51. In contrast, rice containing 128 ng/g As

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translates to an exposure of 0.43 µg/kg/day, which approximates the NOAEL (0.40 µg/kg/day)

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for gastrointestinal effects (gastrointestinal irritation, diarrhea, nausea), dermal effects

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(pigmentation changes with hyperkeratosis). The Minimal Risk Level for effects (other than

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cancer) is also set at 0.4 µg/kg/day 51. Therefore, 128 µg/kg/day can lower As exposure and



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avoid known human effects as reported by US ATSDR for humans who consume at least 200 g

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of rice per day 51.

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Furthermore, although As inhibited nCuO induced increases in panicle emergence, the negative

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correlation between Cu and As accumulation in dehusked-grains indicated an antiport process of

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the two elements by rice grains, of which the mechanism is yet unclear.

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Our study is the first study to evaluate the interaction of As and nCuO on the effects during the

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life cycle of rice plants 52. By combining nCuO and As into one study and working in silt loam

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growth media containing As at concentrations near the average As concentration in soil from

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Texas, USA and lower than previously reported experiments, we have extended the knowledge

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of rice sensitivity to commonly encountered elements in the environments. nCuO not only

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contains the essential element Cu which can serve as an antimicrobial agent for rice plant, nCuO

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also has the potential to decrease As bioavailability These are promising characteristics for

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application in agriculture. More studies are underway to better understand nCuO and As

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accumulation and speciation in rice plants and grains, which may facilitate existing work to

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address possible influences of nCuO and As on food safety and the nutritional quality of rice.

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ACKNOWLEDGMENT

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This work was supported by “C. Gus Glasscock, Jr. Endowed Fund for Excellence in

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Environmental Sciences in the College of Arts and Sciences” at Baylor University. The authors

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thank Robert Doyle for sharing the greenhouse. The authors thank Dr.Alejandro Ramirez (Baylor

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University Mass Spectrometry Center) and Dr. Bernd Zechmann (Center for Microscopy and

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Imaging, Baylor University) for technical support, and Steve Dorwkin for facilitating soil

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particle size analysis.

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DECLARATION OF INTEREST STATEMENT

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The authors report no competing financial interest, and are responsible for the publication.

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SUPPORTING INFORMATION AVAILABLE.

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Additional text describing fertilizer application, soil property characterization and statistical

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analysis; 6 figures showing the conceptual model of treatment preparation and exposure process,

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record of light intensity, temperature and humidity, images with SEM and TEM of grain husk

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and nanoparticles, seed germination percentages, and relationships between rice panicle

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parameters; 13 tables showing Hoagland’s solution composition, nCuO characterization, Cu and

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As concentrations in the growth media, and physiological parameters of 18-d rice seedlings and

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mature rice plants, uptake of Cu and As in seedling shoots and roots, and accumulation of Cu

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and As in dehusked-grains. This information is available free of charge via the Internet at

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http://pubs.acs.org.



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